Arsenomics: omics of arsenic metabolism in plants

Rudra Deo Tripathi; Preeti Tripathi; Sanjay Dwivedi; Sonali Dubey; Sandipan Chatterjee; Debasis Chakrabarty; Prabodh K. Trivedi

doi:10.3389/fphys.2012.00275

Arsenomics: omics of arsenic metabolism in plants

Tripathi, Rudra Deo; Tripathi, Preeti; Dwivedi, Sanjay; Dubey, Sonali; Chatterjee, Sandipan; Chakrabarty, Debasis; Trivedi, Prabodh K. 2012-07-23 00:00:00 REVIEW ARTICLE published: 23 July 2012 doi: 10.3389/fphys.2012.00275 Rudra Deo Tripathi*, Preeti Tripathi , Sanjay Dwivedi , Sonali Dubey , Sandipan Chatterjee , Debasis Chakrabarty and Prabodh K. Trivedi Council of Scientiﬁc and Industrial Research-National Botanical Research Institute (CSIR-NBRI), Lucknow, India Edited by: Arsenic (As) contamination of drinking water and groundwater used for irrigation can lead Andrew Meharg, University of to contamination of the food chain and poses serious health risk to people worldwide. Aberdeen, UK To reduce As intake through the consumption of contaminated food, identiﬁcation of Reviewed by: the mechanisms for As accumulation and detoxiﬁcation in plant is a prerequisite to Frans Maathuis, University of York, develop efﬁcient phytoremediation methods and safer crops with reduced As levels. UK Steve McGrath, Rothamsted Transcriptome, proteome, and metabolome analysis of any organism reﬂects the total Research, UK biological activities at any given time which are responsible for the adaptation of the *Correspondence: organism to the surrounding environmental conditions. As these approaches are very Rudra Deo Tripathi, Plant Ecology important in analyzing plant As transport and accumulation, we termed “Arsenomics” and Environmental Science Division, as approach which deals transcriptome, proteome, and metabolome alterations during Council of Scientiﬁc and Industrial Research-National Botanical As exposure. Although, various studies have been performed to understand modulation Research Institute (CSIR-NBRI), in transcriptome in response to As, many important questions need to be addressed Rana Pratap Marg, Lucknow 226 regarding the translated proteins of plants at proteomic and metabolomic level, resulting 001, India. in various ecophysiological responses. In this review, the comprehensive knowledge e-mail: [email protected] generated in this area has been compiled and analyzed. There is a need to strengthen Arsenomics which will lead to build up tools to develop As-free plants for safe consumption. Keywords: arsenic, arsenomics, transcriptomics, proteomics, metabolomics INTRODUCTION different plant parts is essential for estimating the risks posed by As-contaminated soils to humans and wildlife populations. As Arsenic (As) is ubiquitously present in the environment and is released into the environment in both inorganic and organic highly toxic to all forms of life. Currently, the environmental forms. Arsenate [As(V)] and arsenite [As(III)] are the inor- fate and behavior of As is receiving increased attention due to ganic and more predominant phytoavailable forms of As in soil the As crisis in South-East Asia. In recent decades, millions of solution, as well as most common As species in crop plants. people have suffered from As poisoning as a result of drinking As- Organic As species such as monomethylarsenic acid and dimethy- contaminated water extracted from shallow tube wells (Christen, larsonic acid as also present in the environment to a lesser degree 2001). Large areas of Bangladesh, West Bengal and other states (Tripathi et al., 2007; Zhao et al., 2010). Arsenate and phos- in India and Vietnam rely on As-contaminated ground-water for phate are chemically similar and arsenate acts as a phosphate irrigation of staple crops such as rice (Nickson et al., 1998; Berg analog, thereby being transport into the cell via the phosphate et al., 2001; Christen, 2001; Abedin et al., 2002). Consequently, transporters (Meharg and Macnair, 1991). Through a series of in addition to exposure through drinking-water, people are being As(V) and Pi transport studies, it was concluded that suppres- exposed to As through ingestion of food, which has been contam- sion of the high afﬁnity Pi uptake system decreases the uptake inated by irrigation with As rich water. A third potential route of As(V) (Meharg and Macnair, 1992; Clark et al., 2000; Meharg of exposure is from livestock and their products, where livestock and Hartley-Whitaker, 2002; Lee et al., 2003). In contrast, As(III) have been fed on As-contaminated vegetation. Understanding and undissociated methylated As species are transported through how As is taken up by plants and subsequently accumulated in the nodulin 26-like intrinsic (NIP) aquaporin channels (Zhao et al., 2010; Mosa et al., 2012). Both inorganic forms of As Abbreviations: As, arsenic; As (V), arsenate; As(III), arsenite; AR, arsenate reduc- are highly toxic as As(V) interferes with phosphate metabolism tase; AsA, ascorbate; DAsA, dehydroascorbate; APX, ascorbate peroxidase; CAT, catalase; CS, cysteine synthase; DHAR, dehydroascorbate reductase; FBAII, fruc- (such as phosphorylation and ATP synthesis) and As(III) binds tose bisphosphate aldolase II; FBPase, fructose 1,6 bisphosphatase; GR, glu- to vicinal sulfydryl groups of proteins affecting their structures tathione reductase; GST, glutathione-S-transeferase; GPX, guaiacol peroxidase; or catalytic functions (Tripathi et al., 2007; Zhao et al., 2010). GSH, reduced glutathione; JA, jasmonic acid; MDHAR, monodehydroascor- Exposure to As(V) generates reactive oxygen species (ROS) in bate reductase; NIPs- nodulin26-like intrinsic proteins; PC, phytochelatin; PCS, phytochelatin synthase; POD, peroxidase; Prx, peroxiredoxin; PGK, phospho- plant tissues, which induces oxidative stresses such as lipid per- glycerate kinase; ROS, reactive oxygen species; SAM, S-adenosyl-L-methionine; oxidation (Ahsan et al., 2008; Tripathi et al., 2012). Exposure to SAMS, S-adenosylmethionine synthetase; SOD, superoxide dismutase; Trx, thiore- As(III) also enhances activity of a number of enzymes involved doxin; TK, transketolase; γ-EC, γ-glutamyl cysteine; γ-ECS, γ-glutamyl cysteine synthatase. in the antioxidant responses (Requejo and Tena, 2005; Rai et al., www.frontiersin.org July 2012 | Volume 3 | Article 275 | 1 Tripathi et al. Arsenomics 2011). A number of genes or enzymes involved in glutathione can be directly compared to As in drinking water, assuming equal synthesis and metabolism for As sequestration are upregulated in bioavailability of As in the rice matrix and in water. The percent- rice seedlings exposed to As(V) (Ahsan et al., 2008; Norton et al., age of As in rice grain has been shown to vary by global distri- 2008a). This probably reﬂects a higher demand for GSH under bution. Rice produced in the U.S. contained a mean of 42% As As stress. Arsenate is readily reduced to As(III) in planta, which compared to 60 and 80% for European and Bangladesh/Indian is detoxiﬁed by complexation with either thiol-rich peptides such rice, respectively, (Williams et al., 2005). Another study (Zavala as reduced glutathione (GSH) and phytochelatins (PCs) or vac- et al., 2008) made the suggestion that methylation of As occurs uolar sequestration (Zhao et al., 2010) or a combination of both. within rice and that genetic differences lead to the characteri- To reduce the As uptake through consumption of contaminated zation of two type rice such as DMA and Inorganic As types. plant foods, understanding the mechanisms of As uptake and Rice from the U.S. was predominantly the DMA type, whereas detoxiﬁcation is a prerequisite. PCs are GSH derived peptides rice from Asia and Europe was the Inorganic As type, suggesting that chelated As and participate in ﬁrst step of As detoxiﬁca- that the consumption of DMA rice type has lesser human health tion. Recent ﬁndings demonstrated that AtABCC1 and AtABCC2 risk than the inorganic As rice type. However, other differences in are major vacuolar PC-As transporters (Song et al., 2010)in the soil environment may be important. Latest work that demon- Arabidopsis thaliana. In the hyperaccumulator plant Pteris vittata, strates that plants are unable to methylate As (Lomax et al., 2012) As(V) once taken up by the root is reduced to As(III) which is and instead take up methylated As produced by microorganisms then transported to the lamina of the frond where it is stored as in the soil environment. Therefore it is unlikely for genetic dif- free As(III) (Zhao et al., 2008). Recently the vacuolar transporter ferences to exist for the methylation of As ,however a number of (ACR3) essential for As(III) transport and As tolerance has been studies have demonstrated that there is genetic differences in the identiﬁed in the vacuolar membrane of the gametophyte of P. vit- accumulation of total As in rice grains (Williams et al., 2005, 2007; tata (Indriolo et al., 2010). The yeast vacuolar transporter Ycf1p, Dwivedi et al., 2010, 2012). a member of the ATP-binding cassette (ABC) superfamily, con- Though considerable progress has been made in elucidating fers As(III) resistance by transporting glutathione-S-conjugated the mechanism of plant As uptake and metabolism including tol- arsenite [As(III)-(GS) ]intothe vacuole (Ghosh et al., 1999). erance and toxicity aspects, there is a pressing need to summarize The small duck weed Wolﬁa globosa accumulates 10 times more these outcomes in terms of omic technologies. A better under- As than Azolla species, this higher accumulation is attributed to stand of the mechanisms involved in assimilation and metabo- the lack of a root to frond translocation barrier (Zhang et al., lization of As will led to development of mitigation strategies 2009). In a survey of aquatic and terrestrial vegetation of West against this widespread contamination of the food chain. Here, Bengal (India), high root to shoot As translocation (i.e., translo- we focused on the harmonized response of the plant in terms of cation factor (TF) > 1.0) was observed for Phyllanthus amarus omic technologies, which is the nontargeted identiﬁcation of var- (Tripathi et al., 2011). A detailed account of P. vittata and other ious products (transcripts, proteins, and metabolites) during As ferns as hyperaccumulators involving higher translocation has stress in a speciﬁc biological sample. The aim of this review is to been reviewed (Zhao et al., 2010). Among the crop plants, rice is (a) provide an in-depth overview about genomic, transcriptomic, much more highly efﬁcient in As accumulation than other cereals, proteomic, and metabolomic approaches of plant for both As such as wheat and barley (Williams et al., 2007; Su et al., 2010). tolerance and detoxiﬁcation, (b) explore how genomic, transcrip- The higher accumulation is due to enhanced As bioavailability tomic, proteomic, and metabolomic networks can be connected (due to being grown in anaerobic paddy conditions), and trans- to underlying plant mechanisms during As stress, and (c) dis- port of As(III) through highly efﬁcient Si transport in rice (Ma cuss the need to investigate integrative biochemical networks in et al., 2008; Zhao et al., 2010). Enhanced accumulation of As in As metabolism. Here the As-mediated alteration in plant biologi- rice is a potentially an important route of human exposure to As, cal process is summarized in terms of genomics, proteomics, and especially in populations with a rice-based diet. However, As tox- metabolomics in the following sections. icity varies greatly with species. For example, As concentrations −1 GENOMIC AND TRANSCRIPTIONAL REGULATION in ﬁsh and shellﬁsh can reach 10 mg kg (Schoof et al., 1999) DURING ARSENIC STRESS and are approximately 10–100 times the levels found in rice grain. ARSENIC TRANSPORTERS However, most As in seafood is present in organic form such as arsenobetaine and arsenocholine that are considered to be non- Analysis of the rice and Arabidopsis genomes revealed presence toxic to humans [acute toxicity∼103 times less than inorganic As of at least 13 and 9 members of the phosphate transporter (Pht1) (As )]. Four species of As are commonly reported in rice grain; family in these species, respectively, (Okumura et al., 1998; Mudge As(III), As(V), monomethylarsonic acid (MMA), and dimethy- et al., 2002; Paszkowski et al., 2002). Shin et al. (2004)indi- larsenic acid (DMA). The dominant species are usually As(III) cated that Pht1;1 and Pht1;4 mediate a signiﬁcant proportion and DMA, although the analysis for As(III) and As(V) is often of the As(V) uptake in Arabidopsis. Arsenite is the dominant As jointly reported as As ’(Williams et al., 2005). The As content species in reducing environments, such as ﬂooded paddy soils i i in rice grains can vary from 10–90% of total As (Heikens et al., (Meharg and Jardine, 2003). Bienert et al. (2008) showed that the 2007), but the reason for this variability has not been established. Nodulin26-like Intrinsic Proteins (NIPs) OsNIP2;1 and OsNIP3;2 Discussion of the health risk of As in rice has largely been based from rice are bi-directional As(III) channels. Direct transport on its As content because these species have generally been con- assays using yeast cells conﬁrmed their ability to facilitate As(III) sidered to be more toxic than MMA and DMA (NRC, 1999) and transport across cell membranes. Ma et al. (2008)reported that Frontiers in Physiology | Plant Physiology July 2012 | Volume 3 | Article 275 | 2 Tripathi et al. Arsenomics two different types of transporters mediate transport of As(III), accumulation in the rice grain. Besides, an epistatic interaction from the external medium to the xylem. Transporters belong- for grain As also looks promising to decrease the concentration ing to the NIP subfamily of aquaporins in rice are permeable of this carcinogen (Norton et al., 2012). Recently, As concen- to As(III) but not to As(V). Mutation in OsNIP2;1 (Lsi1,a sil- trations in different tissues of maize was analyzed using a RIL icon inﬂux transporter) signiﬁcantly decreased As(III) uptake. population (Ding et al., 2011). In this study, three QTLs for As Furthermore, in the rice mutants defective in the silicon efﬂux concentration in leaves were mapped on chromosomes 1, 5, and transporter, Lsi2, As(III) transport to the xylem and accumulation 8, respectively. For As concentration in the bracts, two QTLs were in shoots and grain decreased substantially. Mutation in Lsi2 had identiﬁed, which accounted for around 10% of the observed phe- a much greater impact on As accumulation in shoots and grains in notypic variance. For As concentration in the stems, three QTLs ﬁeld-grown rice than Lsi1. The efﬁcient Si uptake pathway in rice were detected with around 8–15% phenotypic variance. Three also allows inadvertent passage of As(III), thus explaining why QTLs were identiﬁed for kernels on chromosomes 3, 5, and 7, rice is efﬁcient in accumulation of As (Ma et al., 2008). However, respectively, with around 9–11% phenotypic variance. Only one knockout of these transporters may not provide solution to As common chromosomal region between SSR marker bnlg1811 and accumulation, as NIPs facilitate the uptake of vital nutrients such umc1243 was detected for QTLs qLAV1 and qSAC1. These results as boron and silicon (Ma et al., 2008). demonstrated that the As accumulation in different tissues in maize was controlled by different molecular mechanisms. GENE MAPPING FOR ARSENIC AND OTHER ELEMENTS ACCUMULATION DIFFERENTIAL EXPRESSION OF VARIOUS GENES DURING An As tolerance gene has been identiﬁed and mapped to chro- ARSENIC STRESS mosome 6 in rice. The collocation of As tolerance gene with a The effect of As exposure on genome-wide expression was also phosphate uptake QTL in another population of rice provided examined in rice by different groups (Norton et al., 2008a; circumstantial evidence for a mechanism involving the behavior Chakrabarty et al., 2009; Yu et al., 2012). A group of defense of As(V) as a phosphate analog, in agreement with the behavior and stress-responsive transporters including; sulphate trans- of an As resistance gene found in populations of Holocus lana- porters, heat-shock proteins, metallothioneins, multidrug and tus (Dasgupta et al., 2004). Recently, the genetic mapping of the toxic compound extrusion (MATE) transporters, glutathione- tolerance of root growth to As(V) using the Bala X Azucena pop- S-transferase, multidrug resistance proteins, glutathione conju- ulation suggested involvement of epistatic interaction involving gated transportes, metal transporter viz. NRAMP1, and genes of three major genes, two on chromosome 6 and one on chromo- sulfate-metabolizing proteins were commonly upregulated in rice some 10. The study provided physiological evidence that genes during As(V) stress in both the studies (Norton et al., 2008a; related to phosphate transport is unlikely to be behind the genetic Chakrabarty et al., 2009). In contrast, phosphate transporter, zinc loci conferring tolerance (Norton et al., 2008b). However, Zhang transporter, aquaporin gene, amino acid transporters, and per- et al. (2007) measured As accumulation in roots and shoots at the oxidases (PODs) were commonly downregulated, however, some seedling stage and brown rice at maturity of the parental culti- gene like cytochrome P450, oxidoreductase were differentially vars (CJ06/TN1) and their double haploid lines after exposure to regulated in rice seedling challenged with As(V). Yu et al. (2012) 210 mg As/kg As in a pot experiment. Four QTLs for As concen- ﬁrst used high-throughput sequencing technology to study tran- trations were detected in the genetic map. At the seedling stage, scriptomes of plant response to As stress. Overall, by genome- one QTL was mapped on chromosome 2 for As accumulation wide transcriptome and miRNA analyses in rice seedlings treated in shoots which explained 24% of the observed phenotypic vari- with As(III), they found a large number of potentially interest- ance and another QTL for As accumulation in roots was detected ing genes in relation to As(III) stress, especially As(III)-responsive on chromosome 3. At maturity, two QTLs for As accumulation transporters and TFs (transcription factors). The change in the in grains were found on chromosomes 6 and 8, which explained expression of genes related to lipid metabolism and phytohor- 26 and 35% of the phenotypic variance, respectively. This study mone pathways after As(III) exposure was striking, indicating that also showed that the QTL on chromosome 8 was identiﬁed for rice invests more energy and resources into immediate defense As concentrations in grain at maturity and shoot phosphorus (P) needs than into normal growth requirements. concentrations at seedling stage. A study targeting genetic map- Arsenate and As(III) stresses modulated metabolic path- ping of the rice ionome in leaves and grains identiﬁed QTLs for ways networks affecting various physiological processes necessary 17 elements including As, Se, Fe, and Cd. In general, there were for plant growth and development (Chakrabarty et al., 2009). no QTL clusters suggesting independent regulation of each ele- Arsenate stress led to upregulation or downregulation of addi- ment. An epistatic interaction for grain As appears promising tional genes in comparison to As(III), but one glutaredoxin to decrease the concentration of this carcinogenic metalloid in (Os01g26912) is expressed speciﬁcally in the AsIII-treated shoots. thericegrain (Norton et al., 2010). Further, these workers while In one of our studies, four rice genotypes responded differentially identifying QTL for rice grain element composition on an As under As(V) and As(III) stress in terms of gene expression and impacted soil from China, found a correlation between ﬂower- antioxidant defenses (Rai et al., 2011). Arsenate challenge leads ing time and number of element concentrations in grains, which to altered gene expression in a large number of genes involved revealed co-localization between ﬂowering time QTLs and grain in classical oxidative stress response, however, phytochelatin syn- element QTLs. Therefore, this study concluded that ﬂowering thase (PCS) and arsenic reductase (AR) levels were not altered time is one of the major factor that controls As and other element signiﬁcantly. This study suggested that the rice cultivar, IET-4786, www.frontiersin.org July 2012 | Volume 3 | Article 275 | 3 Tripathi et al. Arsenomics is very sensitive to As stress due to reduction of both sulphate in Arabidopsis. At the same time, in both the plants 2 GSTs were assimilation pathway and antioxidant defense enzymes in As downregulated. While most of the cytochrome P450 were upreg- detoxiﬁcation in contrast to the tolerant cultivar, Triguna. The ulated in rice, none of these were upregulated in Arabidopsis.In other two varieties (PNR-546 and IR-36) exhibited intermedi- contrast to A. thaliana, the germin like protein was upregulated ary responses involving regulation of these genes during As stress in rice. Many genes encoding ferritins, ZFP (Zinc ﬁnger pro- (Rai et al., 2011). The differential expression pattern of sulphate tein), patatin, acid phosphates, serine/threonine proteine kinases, transporters were observed for the varieties after As(V) exposure integral membrane proteins, and hydrolases always were down (Kumar et al., 2011). Most of the sulphate transporters studied regulated in both monocot and dicots (Abercrombie et al., 2008; were down-regulated in the sensitive variety IET-4786 after expo- Chakrabarty et al., 2009). The data suggests that though there are sure to As(V). Interestingly, differential alternative splicing for common mechanisms for As metabolisms in dicot and monocot OsSultr1;1 was also observed for all the lines after As exposure. A plants, differential mechanisms may also exists. decrease in accumulation was observed for the largest splice vari- ant containing both the introns at higher concentrations of As(V) ARSENIC TOLERANCE IN TRANSGENIC PLANTS and As(III). In the case of sensitive rice variety, accumulation of Gasic and Korban (2007) reported that overexpression of the the entire splice variant decreased with increasing concentration A. thaliana phytochelatin synthase AtPCS1 gene in Indian mus- of As(V). These results clearly suggest that the expression of sul- tard enhanced tolerance to As and Cd. Similarly, Song et al. phate transporter gene family with respect to heavy metal stress is (2010) showed that in the absence of two ABCC-type trans- regulated differentially in different cultivars. porters, AtABCC1 and AtABCC2, A. thaliana is extremely sen- However, several common processes were affected by As(V) sitive to As and As-based herbicides. Heterologous expression and As(III). Differential expression of several genes that showed of these ABCC transporters in phytochelatin (PC)-producing the highest contrast in a microarray analysis was validated by Saccharomyces cerevisiae enhanced As tolerance and accumu- following the quantitative changes in the levels of individual tran- lation. Furthermore, membrane vesicles isolated from yeasts scripts following challenge with As(V)and As(III). Abercrombie exhibited a pronounced As(III)–PC transport activity. Recently, et al. (2008) ﬁrst studied the transcriptional response of a Indriolo et al. (2010) characterized two genes from P. vittata dicot plants, Arabidopsis thaliana, to As(V) stress using oligonu- (ACR3 and ACR3;1), which encode proteins similar to the ACR3 cleotide microarrays. The study suggested that As(V) stress As(III) efﬂuxer of yeast. It was also showed that ACR3 is local- strongly induces Cu/Zn superoxide dismutase activity (SOD), but ized to the vacuolar membrane in gametophytes, indicating that represses the production of Fe SOD. The study also suggested it likely effuxes As(III) into vacuoles for sequestration. A single involvement of several other genes related to antioxidant systems, copy of ACR3 genes is present in moss, other ferns and gym- various transcription factors, tonoplast proteins, and proteins nosperms but absent in ﬂowering plants. The absence of ACR3 associated with cell wall growth. A comparative biochemical and genes in both monocots and eudicots may preclude their ability to transcriptional proﬁling of two contrasting varieties (tolerant and hyperaccumulate As, which is consistent with the observation that sensitive to As) of Brassica juncea indicated upregulation of sul- no As-hyperaccumulating angiosperm has ever been identiﬁed. fate transporters and auxin and jasmonate biosynthesis pathway Why the highly conserved ACR3 gene was lost in the angiosperm genes, whereas, there was downregulation of ethylene biosyn- lineage may never be known, but its loss coincides with their thesis and cytokinin responsive genes in As tolerant plant in reliance on insects and other animals for pollination and fruit dis- contrast to sensitive plant (Srivastava et al., 2009). In another persal. On the other hand, the selection of As hyperaccumulation experiment, Paulose et al. (2010) studied expression proﬁling in P. vittata, may have evolved as a deterrent and in response to of dicot Crambe abyssinica under As(V) stress using PCR-Select herbivores, as it has recently been shown that insects avoid eating Suppression Subtraction Hybridization (SSH) approach. Their P. vittata grown in the presence of As, preferring those not grown study revealed novel insights into the plant defense mechanisms, in As (Rathinasabapathi et al., 2007). In another study, exam- and the regulation of genes and gene networks in response to arse- ining heterologous expression of the yeast As(III) efﬂux system, nate toxicity. The differential expression of transcripts encoding ACR3 was cloned from yeast and transformed into wild-type and glutathione-S-transferases (GSTs), antioxidant As genes, sulfur nip7;1 Arabidopsis (Ali et al., 2012). At the cellular level, all trans- metabolism genes, heat-shock proteins, metal transporters, and genic lines showed increased tolerance to As(III) and As(V) and a enzymes in the ubiquitination pathway of protein degradation, greater capacity for As(V) efﬂux. With intact plants, three of four as well as several unknown novel proteins serve as molecular stably transformed lines showed improved growth, whereas only evidence for the physiological responses to As(V) stress in plants. transgenic lines in the wild-type background showed increased A comparative evaluation of As responsive genes in mono- efﬂux of As(III) into the external medium. The presence of ACR3 cots and dicots offered interesting observations (Table 1). Various hardly affected tissue As levels, but increased As translocation PODs genes always showed a down regulation (2–24 fold) in to the shoot. Expressing Saccharomyces cerevisiae ScACR3 in rice monocots, however, upregulation of two PODs was recorded in enhanced As(III) Efﬂux and also reduced As accumulation in dicots. MT like proteins was upregulated in monocots. Five fer- rice grains (Duan et al., 2012). In the transgenic lines, As con- rodoxins were down regulated in rice but not in A. thaliana. centrations in shoots and roots were about 30% lower than in Peptidyl prolyl cis-trans isomerase was highly upregulated in rice the wild type, while the As translocation factors were similar in contrast to A. thaliana. Interestingly, 9 GSTs were upregu- between transgenic lines and the wild type. The roots of trans- lated in rice, whereas only one was observed to be upregulated genic plants exhibited signiﬁcantly higher As efﬂux activities than Frontiers in Physiology | Plant Physiology July 2012 | Volume 3 | Article 275 | 4 Tripathi et al. Arsenomics Table 1 | Sets of differentially regulated genes in monocot (O. sativa) and dicot (A. thaliana) plants during “As” stress. Description of gene Monocot Dicot Locus Fold change (+/−) Locus Fold change (+/−) Peroxidase Os05g04410 (−) 4.14 At5g64100 (+)2.50 Os05g04450 (−) 5.94 At1g05250 (+)1.90 Os03g36560 (−) 3.69 At5g17820 (+)1.68 Os07g01410 (−) 5.74 At1g05240 (+)2.05 Os04g59160 (−) 12.60 At3g49120 (−)1.77 Os04g59160 (−) 8.33 At5g64120 (−)1.84 Os04g59260 (−) 3.67 At4g25980 (−)1.52 Os03g25330 (−)3.73 Os03g25340 (−)4.63 Os03g55410 (−)2.33 Os05g06970 (−)2.98 Os07g31610 (−) 10.54 Os04g59190 (−) 34.18 Os05g06970 (−)2.98 Os07g31610 (−) 10.54 Os04g59190 (−) 34.18 Os10g39160 (−)7.71 Os01g18970 (−) 10.62 Os07g44480 (−) 24.42 Os07g44460 (−)7.04 Os07g44460 (−)12.11 Metallothionein-like protein 1 Os12g38064 (+) 2.60 At1g07600 (+)1.67 Os12g38300 (+)2.44 Os04g44250 (+)3.42 Ferredoxin, chloroplast Os08g01380 (−) 3.49 At1g10960 (+)1.53 Os08g01380 (−)3.63 Os08g01380 (−)2.75 Os01g25484 (−)3.67 Os01g64120 (−)4.43 Glycosyl hydrolase family 1 protein Os02g20360 (+) 2.62 At3g09260 (+)1.67 Os01g54300 (−)3.50 Peptidyl prolyl cis-trans isomerase Os04g28420 (+) 18.72 At3g62030 (+)1.64 Hypothetical protein Os08g45120 (+) 5.76 At2g06480 (+)1.58 Os03g07510 (+)3.14 Os08g04560 (+)3.74 Os11g16990 (−)7.55 Glutathione S-transferase Os01g72140 (+) 2.53 At1g78370 (+)1.68 Os01g49710 (+) 3.40 At1g02930 (−)2.10 Os10g20350 (+) 3.31 At1g02920 (−)2.88 Os753122 (+)2.68 Os03g13390 (+)4.01 Os06g44010 (+)2.48 Os07g23570 (+)3.29 Os03g46110 (+)4.91 Os06g13190 (+)2.41 Os01g27630 (−)6.29 Os01g27390 (−)2.46 Catalase Os03g03910 (−) 4.52 At1g20620 (−)1.59 Cationic peroxidase Os01g18950 (−) 20.77 At4g25980 (−)1.52 Lipoxygenase Os08g39850 (+) 4.21 At1g72520 (−)2.41 Os03g49260 (−)2.66 (Continued) www.frontiersin.org July 2012 | Volume 3 | Article 275 | 5 Tripathi et al. Arsenomics Table 1 | Continued Description of gene Monocot Dicot Locus Fold change (+/−) Locus Fold change (+/−) Cytochrome P450 83B1 Os03g55240 (+) 3.07 At4g31500 (−)1.71 Os08g39730 (+) 6.09 At3g48520 (−)1.56 Os02g36190 (+)2.95 Os01g43740 (+)8.51 Os01g38110 (+)7.76 Os01g43774 (+) 30.16 Os01g50170 (+)2.80 Os03g57640 (+)3.00 Os09g27260 (+)8.10 Os03g26210 (+)2.49 Os09g10340 (−)2.74 Germin-like protein Os03g06970 (+) 7.19 At5g39160 (−)1.51 At5g39190 (−)2.13 Ferritin Os12g01530 (−) 3.45 At5g01600 (−)1.78 Os12g01530 (−) 3.29 At3g56090 (−)1.52 Os11g01530 (−)4.58 Zinc ﬁnger protein Os06g04920 (−) 2.72 At3g46090 (−)1.51 At3g46080 (−)1.59 At5g27420 (−)1.75 Acid phosphatase Os07g48320 (−) 3.15 At3g17790 (−)1.62 Gycosyl hydrolase family 17 protein Os02g20360 (−) 2.62 At3g55430 (−)1.53 At4g31140 (−)1.71 At4g19810 (−)1.96 At5g20250 (−)1.52 Xloglucan endotransglucosylase/ hydrolase Os02g17900 (−) 17.69 At4g30280 (−)1.63 Os02g17880 (−) 10.85 At4g14130 (−)2.00 Os06g22919 (−) 10.29 At5g57560 (−)1.68 Patatin Os08g37250 (−) 3.47 At2g26560 (−)1.81 Os08g37250 (−)4.58 Serine/threonine protein kinase Os02g43370 (−) 3.31 At3g08720 (−)1.55 Os12g05394 (−)3.27 Os09g12240 (−)3.49 Integral membrane family protein Os04g45520 (−) 18.34 At4g15610 (−)1.58 NAC domain-containing protein Os10g21630 (+) 5.81 At5g08790 (−)1.53 Os02g15340 (−)3.71 Compilation of data based on monocot O. sativa (Chakrabarty et al., 2009) and dicot (A. thaliana) (Abercrombie et al., 2008) plants during arsenate stress. Upregulated (+), Down regulated (−). those of the wild type. Importantly, ScACR3 expression signiﬁ- by Grispen et al. (2009) by overexpressing AtMT2b in Nicotiana cantly reduced As accumulation in rice straws and grains. When tabacum. It was observed that the highest AtMT2b expressing grown in ﬂooded soil irrigated with As(III)-containing water, line exhibited a signiﬁcant decrease in As accumulation in roots, the As concentration in husk and brown rice of the transgenic but an increased accumulation in shoots, while the total amount lines was reduced by 30 and 20%, respectively, compared with of As taken up remained unchanged. This clearly suggested that the wild type. This study reports a potential strategy to reduce AtMT2b expression may enhance As root to shoot transport. Rice As accumulation in the food chain by expressing heterologous transgenics overexpressing As(III)-S-adenosyl methyl transferase genes in crops. Recently, Sundaram et al. (2009) overexpressed (arsM) has been found to methylate As, and gave 10 fold higher the P. vittata glutaredoxin PvGRX5 gene in Arabidopsis.It was volatile arsenical, maintaining low As levels in rice seed along observed that two lines of A. thaliana constitutively expressing with MMA(V) and DMA(V) in the roots and shoots of trans- PvGrx5 cDNA were signiﬁcantly more tolerant than vector con- genic rice (Meng et al., 2011). The upregulation of Met synthase trol and wild-type lines on the basis of germination, root growth and AdoMet synthetase could correlate with As(III) methylation. and whole plant growth under As stress. A study was conducted Although the amounts of methylated As were small, this may Frontiers in Physiology | Plant Physiology July 2012 | Volume 3 | Article 275 | 6 Tripathi et al. Arsenomics offer a new stratagem for As phytoremediation. Shukla et al. proteome level. A summary of upregulated and downregulated (2012) demonstrated that transgenic tobacco plants expressing proteins during As stress in different plant species is presented Ceratophyllum demersum phytochelatin synthase CdPCS1 had a in Table 2. Expression patterns of maize (Zea mays) root and several fold increase in PC content, precursor non protein thiols, leaf proteins in response to As stress were described for the ﬁrst and enhanced accumulation of As without signiﬁcant decrease in time by Requejo and Tena (2005, 2006). They showed that 10% plant growth. of detectable proteins in maize roots were differentially regu- lated by As; seven of the eleven proteins that were identiﬁed PROTEOME MODULATION DURING ARSENIC STRESS are involved in cellular homeostasis for redox perturbation, sug- gesting that oxidative stress is a major process underlying As During the last decade, several groups have made use of transcrip- tome analysis to investigate the expression patterns of genes in toxicity in plants (Requejo and Tena, 2005). To gain a compre- hensive understanding of the precise mechanisms underlying the plants under As stress (Abercrombie et al., 2008; Norton et al., 2008a; Chakrabarty et al., 2009). Such analysis of gene expres- toxicity of As to rice, the metabolism and defense reactions in As nontolerant plants have recently been examined by Ahsan sion at the mRNA level has enhanced our understanding of the responses of plants to As stress. However, transcriptional anal- et al. (2008). This was done by carrying out a comparative pro- ysis has a number of limitations (Rose et al., 2004), including teomic analysis of rice roots in combination with physiological poor correlations between changes in the expression of mRNAs and biochemical analyses. The comparative proteomic analyses and those of their corresponding proteins (Gygi et al., 1999). identiﬁed 23 differentially expressed proteins in rice roots, includ- Though correlation between mRNA and protein has been noticed ing those predicted as S-adenosylmethionine synthetase (SAMS), (Joosen et al., 2007; Li et al., 2007), protein expression is also cysteine synthase (CS), and novel proteins including tyrosine- speciﬁc protein phosphatase protein, and omega domain contain- regulated at the translational and post-translational levels. Thus, gaining information at the translational and post-translational ing GST. These differentially expressed proteins are functionally involved in cell signaling, stress and detoxiﬁcation, defense and levels can offer deeper insights into the responses and functional interactions of proteins. development, and protein biosynthesis. On the basis of phys- iological and proteomic investigations, it is proposed that As Although large numbers of physiological and biochemical analyses have been performed (Hartley-Whitaker et al., 2001; stress in plants generates ROS, triggering signaling molecules Liu et al., 2005; Williams et al., 2005; Rahman et al., 2007), such as jasmonic acid (JA) and S-adenosyl-L-methionine (SAM), little is known about As stress-elicited changes in plants at the and activating the detoxiﬁcation process, which mainly involves Table 2 | A review of “As” modulated proteins in different plant species during proteomic analysis. Plant species Plant No. of responsive proteins Research outcome References part used and proteomic analysis used Z. mays Root 11, 2-DE, MALDI-TOF MS Upregulation of antioxidant enzymes related proteins Requejo and viz. SODs, GPXs, and peroxiredoxin (Prx) besides four Tena, 2005 additional, functionally heterogeneous, proteins (e.g., ATP synthase, succinyl-CoA synthetase, cytochrome P450, and guanine nucleotide-binding protein b subunit) suggest that the induction of oxidative stress is a main process underlying As toxicity in plants Z. mays Shoot 7, 2-DE, MALDI-TOF MS Down regulation of Translation initiation factor eIF-5A, Requejo and ATP synthase, CS, malate dehydrogenase, protein Tena, 2006 kinase C inhibitor, Tn10 transposase-like protein, and guanine nucleotide binding protein during As stress O. sativa Root 23, 2-DE, MALDI-TOF MS GSH plays a central role in protecting cells against As Ahsan et al., 2008 stress due to synchronous function of SAMS, CS, GSTs, and GR O. sativa Leaf 6, 2-DE, MALDI-TOF MS Down-regulation of RuBisCO and chloroplast 29 kDa Ahsan et al., 2010 ribonucleo proteins under As stress may be the possible causes of the decreased photosynthesis rate P. vittata (G. Frond 19, 2-DE hybrid quadrupole-TOF Multiple forms of glyceraldehyde-3-phosphate Bona et al., 2010 mosseae- MS dehydrogenase, phosphoglycerate kinase, and inoculated) enolase, was upregulated in G. mosseae-inoculated plants, suggests a central role for glycolytic enzymes in As metabolism A. tenuis Leaf 2-DE hybrid quadrupole-TOF MS prominent fragmentation of the RubisCO protein due Duquesnoy et al., to As toxicity 2009 www.frontiersin.org July 2012 | Volume 3 | Article 275 | 7 Tripathi et al. Arsenomics GSH/PC biosynthesis (Ahsan et al., 2008). Interestingly, these resistance in the As hyperaccumulator fern P. vittata,acDNA for pathways are coordinately regulated, with GSH playing a cen- a glutaredoxin (Grx) Pv5–6 was isolated from a frond expression tral role in the complex cellular network. Arsenite and As(V) cDNA library based on the ability of the cDNA to increase As differentially modulated physiological response in Hydrilla ver- resistance in Escherichia coli. The deduced amino acid sequence ticillata, where As(V) stress resulted in activation of the antiox- of Pv5–6 showed high homology with an Arabidopsis chloro- idant defence system, while As(III) responses involved preva- plastic Grx and contained two CXXS putative catalytic motifs. lence of As complexing PCs (Srivastava et al., 2007). Elevated Puriﬁed recombinant Pv5–6 exhibited glutaredoxin activity that levels of antioxidants and PCs were also observed in C. demer- was increased at 10 mM As(V). Site-speciﬁc mutation of Cys sum during As(V) exposure, suggesting the modulation of spe- to Ala resulted in the loss of both GRX activity and As resis- ciﬁc proteins by As induced stress (Mishra et al., 2008). The tance. PvGrx5 has an important role in regulating intracellular As induced antioxidative responses were also validated by pro- As(III) levels, by either directly or indirectly modulating the teomic changes in germinating rice seedlings during As exposure. aquaglyceroporin (Sundaram et al., 2008). Further study of isozymes of SOD, APX, POD, and glutathione Other than these investigations, no proteomic analyses have reductase (GR) validated that As accumulation generated oxida- been carried out on responses of dicotyledonous plants includ- tive stress, which was more pronounced in As(III) treatment ing Arabidopsis, to As stress. Therefore, there is a need for an (Shri et al., 2009). Ahsan et al. (2010)also reported the ﬁrst extended proteomic analysis of the responses of the root systems proteome map of rice leaves under As stress along with phys- of dicotyledonous model plants systems to As stress to gain a bet- iological and biochemical responses. The increased activity of ter understanding of the molecular basis of this response. This several proteins associated with energy metabolism, such as will allow the determination of whether monocot and dicot plants NADP-dependent malic enzyme, NAD-dependent formate dehy- both employ the same defense mechanisms under As stress, and drogenase, and glyceraldehyde-3-phosphate dehydrogenase sug- to identify novel As-responsive proteins for future studies. gest that an increased amount of energy is required to adapt to As stress. However, the down-regulation of RuBisCO and chloro- METABOLOME MODULATION DURING ARSENIC STRESS plast 29 kDa ribonucleoproteins might be the possible causes of Despite the fact that transcriptomic approaches provide almost the decreased photosynthesis rate under As stress. Contrary to complete coverage and proteomics approaches are now capable of this ﬁnding, Duquesnoy et al. (2009) identiﬁed a set of Agrostis detecting most of the cellular protein complement, metabolomics tenuis leaf proteins differentially expressed in response to As is currently capable of determining only a small fraction of the exposure including a major functionally homogeneous group of metabolites found in any one cell. As well as to validate the enzymes including oxygen-evolving enhancer protein, RuBisCO outcome of differential transcriptomic studies along with pro- small and large subunits, RuBisCO activase, and ATP synthase teomic analyses in As stressed plant, metabolome analysis is involved in the Calvin or Krebs cycle. Bona et al. (2010)also needed to investigate the unexplored properties of biological demonstrated the protein expression proﬁle of P. vittata fronds systems. The more challenging aspect of metabolomic technolo- in plants inoculated with one of the two AM fungi (Gigaspora gies is the reﬁned analysis of quantitative dynamics in biological mosseae or Gigaspora margarita) with and without As treatment. systems. For metabolomics, gas and liquid chromatography cou- Up-regulation of multiple forms of glyceraldehyde-3-phosphate pled to mass spectrometry are well suited for coping with high dehydrogenase, phosphoglycerate kinase (PGK), and enolase, pri- sample numbers in reliable measurement times with respect to marily in G. mosseae-inoculated plants, suggests a central role for both technical accuracy and the identiﬁcation and quantitation glycolytic enzymes in As metabolism. Moreover, a putative As of small-molecular-weight metabolites. However to best of our transporter, PgPOR29, has been identiﬁed as an up-regulated pro- knowledge, there is very limited studies have been performed to tein by As treatment. Proteomics in conjunction with morpholog- recognize the modulation of differential metabolomic pathway ical, physiological, and biochemical variables has been employed during As stress. for the ﬁrst time by Pandey et al. (2011) to unravel survival strate- ROLE OF GLUTATHIONE AND PHYTOCHELATIN DURING ARSENIC gies of the diazotrophic cyanobacterium Anabaena sp. PCC7120. Down-regulation of PGK, fructose bisphosphate aldolase II (FBA STRESS II), fructose 1,6 bisphosphatase (FBPase), transketolase (TK), and In most of the studies, metabolites involved in antioxidant sys- ATP synthase on day 1 and their signiﬁcant recovery on the day 15 tems, PCs and related molecules involved in biosynthesis of presumably maintained the glycolysis, pentose phosphate path- PCs have been analyzed during As stress. A list of several As way (PPP) and turnover rate of Calvin cycle, hence survival of the responsive metabolites has been mentioned in the Table 3.The test organism. Up-regulation of CAT, peroxiredoxin (Prx), thiore- raised level of some metal detoxifying thiolic ligand such as doxin (Trx), and oxidoreductase appears to protect the cells from glutathione were also noticed in ferns such as P. vittata, P. ensi- oxidative stress. Appreciable induction in PC content, GST activ- formis (Singh et al., 2006), aquatic plants such as H. verti- ity and transcripts of PCS, AR and As(III) efﬂux genes-asr1102, cilata and C. demersum (Srivastava et al., 2007; Mishra et al., alr1097 reiterates their role in As sequestration and shielding of 2008), and crop plants like B. juncea and O. sativa (Srivastava the organism from As toxicity. While up-regulated metabolic and et al., 2009; Tripathi et al., 2012). While concomitant reduc- antioxidative defense proteins, PC and GST work synchronously, tion in glutathione and S-nitrosoglutathione (GSNO) content the ars genes play a central role in detoxiﬁcation and survival were observed in A. thaliana suggesting the altered GR and S- of Anabaena under As stress. To elucidate the mechanisms of As nitrosoglutathione reductase activities during higher As exposure Frontiers in Physiology | Plant Physiology July 2012 | Volume 3 | Article 275 | 8 Tripathi et al. Arsenomics Table 3 | Metabolites in different plant species during arsenic stress. Metabolites studied Plant species Research outcome References Valine, metheionine, leucine, O. sativa Most of the NEEAs were increased Dwivedi et al., 2010, 2012 in most of the cultivars during As alanine histidine, alanine, proline, glutamic acid, stress, while EAAs were decreased cysteine in most of the cultivar Proline, glutamic acid, S. oleracea Increased during As(V) stress Pavlík et al., 2010 aspartic acid alanine Proline O. sativa Induced during As(III) stress Mishra and Dubey (2006) Cysteine H. verticillata, C. demersum, Increased during As(V) stress Srivastava et al., 2007, 2009; Mishra B. juncea, O. sativa et al., 2008; Tripathi et al., 2012 γ-glutamyl cysteine A. thaliana Increased synthesis during As(V) Dhankher et al., 2002; Li et al., 2004 stress Glutathione A. thaliana, P. vittata, P. ensiformis, Increased during As(V) stress Dhankher et al., 2002; Li et al., 2004; H. verticillata, C. demersum, except in A. thaliana Singh et al., 2006; Srivastava et al., B. juncea, O. sativa, A. thaliana 2007, 2009; Mishra et al., 2008; Tripathi et al., 2012 S-nitrosoglutathione A. thaliana Decreased during As(V) stress Leterrier et al., 2012 Phytochelatins A. thaliana, H. verticillata, Various species of phytochelatins Dhankher et al., 2002; Li et al., 2004; C. demersum, O. sativa were increased during As stress Srivastava et al., 2007; Mishra et al., 2008; Tripathi et al., 2012 Ascorbic acid P. vittata, P. ensiformis, O. sativa Increased during As(V) stress Singh et al., 2006; Tripathi et al., 2012 Malondialdehyde P. vittata, P. ensiformis, Increased during As(V) stress Singh et al., 2006; Srivastava et al., H. verticillata, C. demersum, 2007; Mishra et al., 2008; Tripathi et al., O. sativa 2012 Nitric oxide H. verticillata, O. sativa, A. thaliana Increased during As(V) stress Srivastava et al., 2011; Leterrier et al., 2012; Tripathi et al., 2012 Polyamines (spermidine, T. pratense Polyamines increased only at lower Mascher et al., 2002 spermine) and diamine doses but diamine increased at (putrescine) higher doses during As(V) stress ATP,ADP, NADH, NAD, H. verticillata Level of ATP,NADP,NADH Srivastava et al., 2011 NADPH, NADP decreased, while level of ADP, NADPH and NAD increased during As(V) exposure (Leterrier et al., 2012). Similarly induced level of PCs were also suggests that PCs play a limited role for the hypertolerance observed in H. verticillata, C. demersum, and O. sativa (Srivastava of As in P. vittata. Similarly, Raab et al. (2007)demonstrated et al., 2007; Mishra et al., 2008; Tripathi et al., 2012)under As the As concentration-dependent formation of As–PC complex, stress. Earlier, As-PC complexes were studied in H. lanatus and redistribution and metabolism of As after arrested As uptake in P. cretica using parallel metal(loid)-speciﬁc-ICPMS and organic- Helianthus annuus. The amount and number of As–PC com- speciﬁc-ESI-MS detection systems (Raab et al., 2004). In an in plexes increased exponentially with concentration up to 13.7 μM vitro experiment using a mixture of GSH, PC ,and PC ,As As and As(III)–PC and GS–As(III)–PC complexes were the 2 3 3 2 preferred the formation of the As(III)-PC complex over GSH- dominant species. In another study, Liu et al. (2010)quantiﬁed As(III)-PC , As(III)-(GSH) , As(III)-PC , or As(III)-(PC ) .In As(III)-thiol complexes and free thiol compounds in A. thaliana 2 3 2 2 2 H. lanatus, the As(III)-PC complex was the dominant complex, exposed to As(V). In wild-type roots, 69% of As(III) was com- although GSH, PC ,and PC were found in the tissue extract. plexed as As(III)-PC , As(III)-PC , and As(III)-(PC ) while in 2 3 4 3 2 2 P. cretica only synthesizes PC and forms dominantly the GSH- roots of the GSH-deﬁcient mutant (cad2-1) and the PC-deﬁcient As(III)-PC complex. In both plant species, As is dominantly mutant (cad1-3) very little of As was complexed with As(III)-PCs in non-bound inorganic forms, with 13% being present in PC and As(III)-(GS) , respectively. This conferred approximately 20 complexes for H. lanatus and 1% in P. cretica.Phytochelatin times more tolerance for the wild type than the mutants. These synthesis was induced upon exposure to As(V) in P. vittata, mutants showed signiﬁcantly higher accumulation of As(III) in with only PC detected in the plant (Zhao et al., 2003). The As shoots and efﬂuxed larger amount of As(III) than the wild type, concentration correlated signiﬁcantly with PC concentration in suggesting that enhancing PC synthesis in roots may be an effec- roots and shoots of P. vittata, but not with GSH. Chelation of tive strategy to reduce As translocation to the edible organs only a small proportion (1–3%) of the As with PCs in P. vittata of food crops. Furthermore, transgenic Arabidopsis expressing www.frontiersin.org July 2012 | Volume 3 | Article 275 | 9 Tripathi et al. Arsenomics very high levels of the bacterial γ-glutamylcysteine synthetase P. ensiformis, H. verticillata, C. demersum.Nitric oxide, a sig- (ECS) gene and PCS had several fold higher concentrations of naling molecule was also found to be induced during As(V) γ-glutamylcysteine (EC), GSH, and PCs than the wild type, and stress condition in H. verticillata, O. sativa, and A. thaliana show tolerance to As (Dhankher et al., 2002; Li et al., 2004). (Srivastava et al., 2011; Tripathi et al., 2012; Leterrier et al., 2012). The protection provided by polyamines against oxida- tive stress has been proposed to involve scavenging free radicals CHANGES IN AMINO ACID PROFILING (Drolet et al., 1986) and the reduction of lipid peroxidation Variation in amino acid content was observed in different plant (Borrell et al., 1997). Mascher et al. (2002)demonstrated that species during As exposure. Dwivedi et al. (2010) performed a levels of polyamines viz., spermidine, spermine increased only at simulated pot experiment, using environmentally relevant con- lower doses but diamine increased at higher doses during As(V) centrations of As, analyzed the amino acid proﬁle in grain of stress in red clover (Trifolium pretense). Another study concluded various rice genotypes. This study demonstrated that Speciﬁc −1 that redox state and energetic equilibrium analyzed in terms of As Uptake (SAU, μgg dw), which indicates the ability of As ATP/ADP NADH/NAD, NADPH/NADP, GSH/GSSG, and AsA/ uptake by rice per unit root under As exposure, was different DAsA ratios, were found to be altered due to As toxicity in H. ver- between rice genotypes, and found in the order of As tolerant ticillata (Srivastava et al., 2011). Hence, variation in metabolite Triguna (134) > IR-36 (71.5) > PNR-519 (53) > sensitive IET- −1 proﬁling during As exposure in different plant species signify that 4786 (29). However, the grain As concentration (μgg dw) order plants modulate their metabolome to respond against As stress. was IR-36 (1.5) > Triguna (1) > PNR-519 (0.5) > IET-4786 (0.3). They concluded that most of the essential amino acids (EAAs) metabolites such as valine, metheionine, leucine, alanine, and FUTURE PROSPECTS nonessential amino acids (NEAAs) viz. histidine, alanine, proline, As presents a health hazard to human populations world-wide glutamic acid, and cysteine increased in most of the rice geno- due to its mobilization and accumulation in plant parts. As types during As(V) exposure. Further to validate this ﬁnding a accumulation and homeostasis require the co-ordination of sev- ﬁeld experiment was conducted, determining the amino acid pro- eral processes working simultaneously to regulate uptake, long- ﬁle of sixteen rice genotypes differing in grain As accumulation, distance transport, and distribution of metalloid to different cells grown at three sites with different soil As concentrations in West and tissues. In the last few years, various QTLs as well as genes Bengal and India. Grain As accumulation negatively correlated including those encoding transporters, genes mediating As accu- with EAAs which were more prominent in high As accumulat- mulation, vacuolar sequestration, and distribution breakthroughs ing rice genotypes (HAARGs). Conversely, NEAAs showed an in As speciation with a diverse range of advanced techniques increase in low As accumulating rice genotypes (LAARGs) but opening a new and unheralded insight to cellular speciation, such a decrease in HAARGs. EAAs like isoleucine, leucine, valine, as micro-XAS and coupled HPLC-ICP-MS - ESI-MS. The eval- phenylalanine, and tyrosine also decreased in most of the geno- uation of transcriptomic, proteomic, and metabolomic analyses types (Dwivedi et al., 2012). Some other amino acids for example indicate that thiol peptides like glutathione and PCs play a central proline, glutamic acid, aspartic acid, and alanine also increased role in As detoxiﬁcation, as well as various antioxidant defense during As(V) stress in Spinacia oleracea (Pavlík et al., 2010). system response against As induced oxidative stress. However, not Among stress responsive amino acids, proline is a much studied many studies have been carried out to study global change in molecules and can function as an osmolyte, free radical scavenger term of transcriptome, proteome, and metabolome. A compar- and also protects the cell membrane against damage. The level of ative evaluation of proteome, transcriptome, and metabolomic proline has also been observed to be elevated in O. sativa during approaches in tolerant and sensitive varieties of plants such as rice As (III) stress (Mishra and Dubey, 2006). The S-containing amino and other plants, including Arabdopsis, may offer huge oppor- acid, cysteine, plays a central role in As detoxiﬁcation, as it is a tunities for the deeper understanding to develop As tolerant primary metabolite for synthesis of GSH and PCs. The cysteine plants, including safer crops for human consumption (Figure 1). content increased in some aquatic plants such as H. verticillata, Further, studies pertaining to transcriptional responses show rootless plant C. demersum, andcropplants B. juncea, O. sativa expression of several genes with unclear or unknown biological during As stress (Srivastava et al., 2007, 2009; Mishra et al., 2008; functions, providing future targets for plant Arsenomics research. Tripathi et al., 2012). However, the QTLs analysis in various As stressed plant species provide an insight into the genetic basis of As uptake and accumu- OTHER METABOLITES lation and will be useful for molecular breeding for As tolerance in Some low molecular antioxidant like ascorbate (AsA) and dehy- rice. Epistatic interaction for grain As appear promising to reduce droascorbate (DAsA), which work as non-enzymatic antioxidants the health risk due to this carcinogen. Understanding of these in the glutathione-ascorbate cycle for free radical scavenging, omics approaches which will lead to Arsenomics and use of infor- were also analyzed in some plants during As(V) exposure. As(V) mation generated could help to breed plants with low As in edible exposure caused an increase in the ratio of AsA/DAsA in P. plant parts, along with the species of As present being of low toxi- vitatta, P. ensiformis, H. verticillata, and O. sativa (Singh et al., city. Therefore, future research should focus on ﬁlling gaps in our 2006; Srivastava et al., 2011; Tripathi et al., 2012) indicating knowledge, taking advantages of modern analytical tools and a the signiﬁcant role of ascorbate for As induced stress amelio- combination of different omics approaches for enhanced As phy- ration. Malondialdehyde (MDA), the byproduct of lipid perox- toremediation and development of As tolerant crops with safer idation was also increased during As(V) expsoure in P. vittata, grain As levels. Frontiers in Physiology | Plant Physiology July 2012 | Volume 3 | Article 275 | 10 Tripathi et al. Arsenomics FIGURE 1 | Omics of As accumulation and tolerance: comparative study of As tolerant and sensitive plants at various levels such as genome, transcriptome, proteome, and metabolome to generate information to develop low grain As crops using breeding and molecular tools. University of Aberdeen, UK for scientiﬁc and linguistic ACKNOWLEDGMENTS improvement of the manuscript. Preeti Tripathi and Sonali The authors are thankful to Director, CSIR-National Botanical Dubey are thankful to Council of Scientiﬁc and Industrial Research Institute, Lucknow, for the facilities and for the Research, New Delhi, India, for the award of Senior Research ﬁnancial support from the network projects (NWP) (CSIR), Fellowship. New Delhi, India. We are also grateful to G. J. Norton, REFERENCES and Lee, B.-H. (2010). Analysis of of plant aquaporins facilitate the and Tuli, R. (2009). Comparative Abedin,M.J., Feldmann, J.,and arsenic stress-induced differentially bi-directional diffusion of As(OH) transcriptome analysis of arse- Meharg, A. A. (2002). Uptake kinet- expressed proteins in rice leaves by and Sb(OH) across membranes. nate and arsenite stresses in ics of arsenic species in rice plants. two-dimensional gel electrophore- BMC Plant Biol. 6, 26. rice seedlings. Chemosphere 74, Plant Physiol. 128, 1120–1128. sis coupled with mass spectrometry. 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The that could be construed as a potential of arsenic metabolism in plants. Front. under the terms of the Creative role of phytochelatins in arsenic conﬂict of interest. Physio. 3:275. doi: 10.3389/fphys. Commons Attribution License, tolerance in the hyperaccumulator 2012.00275 which permits use, distribution Pteris vittata. New Phytol. 159, Received: 11 January 2012; accepted: 27 This article was submitted to Frontiers in and reproduction in other forums, 403–410. June 2012; published online: 23 July Plant Physiology, a specialty of Frontiers provided the original authors and source 2012. in Physiology. are credited and subject to any copyright Conﬂict of Interest Statement: The Citation: Tripathi RD, Tripathi Copyright © 2012 Tripathi, notices concerning any third-party authors declare that the research P, Dwivedi S, Dubey S, Tripathi, Dwivedi, Dubey, Chatterjee, graphics etc. Frontiers in Physiology | Plant Physiology July 2012 | Volume 3 | Article 275 | 14 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Frontiers in Physiology Pubmed Central http://www.deepdyve.com/lp/pubmed-central/arsenomics-omics-of-arsenic-metabolism-in-plants-aEbAPP2td0

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Publisher: Pubmed Central
Copyright: Copyright © 2012 Tripathi, Tripathi, Dwivedi, Dubey, Chatterjee, Chakrabarty and Trivedi.
ISSN: 1664-042X
eISSN: 1664-042X
DOI: 10.3389/fphys.2012.00275
Publisher site: See Article on Publisher Site

Abstract

REVIEW ARTICLE published: 23 July 2012 doi: 10.3389/fphys.2012.00275 Rudra Deo Tripathi*, Preeti Tripathi , Sanjay Dwivedi , Sonali Dubey , Sandipan Chatterjee , Debasis Chakrabarty and Prabodh K. Trivedi Council of Scientiﬁc and Industrial Research-National Botanical Research Institute (CSIR-NBRI), Lucknow, India Edited by: Arsenic (As) contamination of drinking water and groundwater used for irrigation can lead Andrew Meharg, University of to contamination of the food chain and poses serious health risk to people worldwide. Aberdeen, UK To reduce As intake through the consumption of contaminated food, identiﬁcation of Reviewed by: the mechanisms for As accumulation and detoxiﬁcation in plant is a prerequisite to Frans Maathuis, University of York, develop efﬁcient phytoremediation methods and safer crops with reduced As levels. UK Steve McGrath, Rothamsted Transcriptome, proteome, and metabolome analysis of any organism reﬂects the total Research, UK biological activities at any given time which are responsible for the adaptation of the *Correspondence: organism to the surrounding environmental conditions. As these approaches are very Rudra Deo Tripathi, Plant Ecology important in analyzing plant As transport and accumulation, we termed “Arsenomics” and Environmental Science Division, as approach which deals transcriptome, proteome, and metabolome alterations during Council of Scientiﬁc and Industrial Research-National Botanical As exposure. Although, various studies have been performed to understand modulation Research Institute (CSIR-NBRI), in transcriptome in response to As, many important questions need to be addressed Rana Pratap Marg, Lucknow 226 regarding the translated proteins of plants at proteomic and metabolomic level, resulting 001, India. in various ecophysiological responses. In this review, the comprehensive knowledge e-mail: [email protected] generated in this area has been compiled and analyzed. There is a need to strengthen Arsenomics which will lead to build up tools to develop As-free plants for safe consumption. Keywords: arsenic, arsenomics, transcriptomics, proteomics, metabolomics INTRODUCTION different plant parts is essential for estimating the risks posed by As-contaminated soils to humans and wildlife populations. As Arsenic (As) is ubiquitously present in the environment and is released into the environment in both inorganic and organic highly toxic to all forms of life. Currently, the environmental forms. Arsenate [As(V)] and arsenite [As(III)] are the inor- fate and behavior of As is receiving increased attention due to ganic and more predominant phytoavailable forms of As in soil the As crisis in South-East Asia. In recent decades, millions of solution, as well as most common As species in crop plants. people have suffered from As poisoning as a result of drinking As- Organic As species such as monomethylarsenic acid and dimethy- contaminated water extracted from shallow tube wells (Christen, larsonic acid as also present in the environment to a lesser degree 2001). Large areas of Bangladesh, West Bengal and other states (Tripathi et al., 2007; Zhao et al., 2010). Arsenate and phos- in India and Vietnam rely on As-contaminated ground-water for phate are chemically similar and arsenate acts as a phosphate irrigation of staple crops such as rice (Nickson et al., 1998; Berg analog, thereby being transport into the cell via the phosphate et al., 2001; Christen, 2001; Abedin et al., 2002). Consequently, transporters (Meharg and Macnair, 1991). Through a series of in addition to exposure through drinking-water, people are being As(V) and Pi transport studies, it was concluded that suppres- exposed to As through ingestion of food, which has been contam- sion of the high afﬁnity Pi uptake system decreases the uptake inated by irrigation with As rich water. A third potential route of As(V) (Meharg and Macnair, 1992; Clark et al., 2000; Meharg of exposure is from livestock and their products, where livestock and Hartley-Whitaker, 2002; Lee et al., 2003). In contrast, As(III) have been fed on As-contaminated vegetation. Understanding and undissociated methylated As species are transported through how As is taken up by plants and subsequently accumulated in the nodulin 26-like intrinsic (NIP) aquaporin channels (Zhao et al., 2010; Mosa et al., 2012). Both inorganic forms of As Abbreviations: As, arsenic; As (V), arsenate; As(III), arsenite; AR, arsenate reduc- are highly toxic as As(V) interferes with phosphate metabolism tase; AsA, ascorbate; DAsA, dehydroascorbate; APX, ascorbate peroxidase; CAT, catalase; CS, cysteine synthase; DHAR, dehydroascorbate reductase; FBAII, fruc- (such as phosphorylation and ATP synthesis) and As(III) binds tose bisphosphate aldolase II; FBPase, fructose 1,6 bisphosphatase; GR, glu- to vicinal sulfydryl groups of proteins affecting their structures tathione reductase; GST, glutathione-S-transeferase; GPX, guaiacol peroxidase; or catalytic functions (Tripathi et al., 2007; Zhao et al., 2010). GSH, reduced glutathione; JA, jasmonic acid; MDHAR, monodehydroascor- Exposure to As(V) generates reactive oxygen species (ROS) in bate reductase; NIPs- nodulin26-like intrinsic proteins; PC, phytochelatin; PCS, phytochelatin synthase; POD, peroxidase; Prx, peroxiredoxin; PGK, phospho- plant tissues, which induces oxidative stresses such as lipid per- glycerate kinase; ROS, reactive oxygen species; SAM, S-adenosyl-L-methionine; oxidation (Ahsan et al., 2008; Tripathi et al., 2012). Exposure to SAMS, S-adenosylmethionine synthetase; SOD, superoxide dismutase; Trx, thiore- As(III) also enhances activity of a number of enzymes involved doxin; TK, transketolase; γ-EC, γ-glutamyl cysteine; γ-ECS, γ-glutamyl cysteine synthatase. in the antioxidant responses (Requejo and Tena, 2005; Rai et al., www.frontiersin.org July 2012 | Volume 3 | Article 275 | 1 Tripathi et al. Arsenomics 2011). A number of genes or enzymes involved in glutathione can be directly compared to As in drinking water, assuming equal synthesis and metabolism for As sequestration are upregulated in bioavailability of As in the rice matrix and in water. The percent- rice seedlings exposed to As(V) (Ahsan et al., 2008; Norton et al., age of As in rice grain has been shown to vary by global distri- 2008a). This probably reﬂects a higher demand for GSH under bution. Rice produced in the U.S. contained a mean of 42% As As stress. Arsenate is readily reduced to As(III) in planta, which compared to 60 and 80% for European and Bangladesh/Indian is detoxiﬁed by complexation with either thiol-rich peptides such rice, respectively, (Williams et al., 2005). Another study (Zavala as reduced glutathione (GSH) and phytochelatins (PCs) or vac- et al., 2008) made the suggestion that methylation of As occurs uolar sequestration (Zhao et al., 2010) or a combination of both. within rice and that genetic differences lead to the characteri- To reduce the As uptake through consumption of contaminated zation of two type rice such as DMA and Inorganic As types. plant foods, understanding the mechanisms of As uptake and Rice from the U.S. was predominantly the DMA type, whereas detoxiﬁcation is a prerequisite. PCs are GSH derived peptides rice from Asia and Europe was the Inorganic As type, suggesting that chelated As and participate in ﬁrst step of As detoxiﬁca- that the consumption of DMA rice type has lesser human health tion. Recent ﬁndings demonstrated that AtABCC1 and AtABCC2 risk than the inorganic As rice type. However, other differences in are major vacuolar PC-As transporters (Song et al., 2010)in the soil environment may be important. Latest work that demon- Arabidopsis thaliana. In the hyperaccumulator plant Pteris vittata, strates that plants are unable to methylate As (Lomax et al., 2012) As(V) once taken up by the root is reduced to As(III) which is and instead take up methylated As produced by microorganisms then transported to the lamina of the frond where it is stored as in the soil environment. Therefore it is unlikely for genetic dif- free As(III) (Zhao et al., 2008). Recently the vacuolar transporter ferences to exist for the methylation of As ,however a number of (ACR3) essential for As(III) transport and As tolerance has been studies have demonstrated that there is genetic differences in the identiﬁed in the vacuolar membrane of the gametophyte of P. vit- accumulation of total As in rice grains (Williams et al., 2005, 2007; tata (Indriolo et al., 2010). The yeast vacuolar transporter Ycf1p, Dwivedi et al., 2010, 2012). a member of the ATP-binding cassette (ABC) superfamily, con- Though considerable progress has been made in elucidating fers As(III) resistance by transporting glutathione-S-conjugated the mechanism of plant As uptake and metabolism including tol- arsenite [As(III)-(GS) ]intothe vacuole (Ghosh et al., 1999). erance and toxicity aspects, there is a pressing need to summarize The small duck weed Wolﬁa globosa accumulates 10 times more these outcomes in terms of omic technologies. A better under- As than Azolla species, this higher accumulation is attributed to stand of the mechanisms involved in assimilation and metabo- the lack of a root to frond translocation barrier (Zhang et al., lization of As will led to development of mitigation strategies 2009). In a survey of aquatic and terrestrial vegetation of West against this widespread contamination of the food chain. Here, Bengal (India), high root to shoot As translocation (i.e., translo- we focused on the harmonized response of the plant in terms of cation factor (TF) > 1.0) was observed for Phyllanthus amarus omic technologies, which is the nontargeted identiﬁcation of var- (Tripathi et al., 2011). A detailed account of P. vittata and other ious products (transcripts, proteins, and metabolites) during As ferns as hyperaccumulators involving higher translocation has stress in a speciﬁc biological sample. The aim of this review is to been reviewed (Zhao et al., 2010). Among the crop plants, rice is (a) provide an in-depth overview about genomic, transcriptomic, much more highly efﬁcient in As accumulation than other cereals, proteomic, and metabolomic approaches of plant for both As such as wheat and barley (Williams et al., 2007; Su et al., 2010). tolerance and detoxiﬁcation, (b) explore how genomic, transcrip- The higher accumulation is due to enhanced As bioavailability tomic, proteomic, and metabolomic networks can be connected (due to being grown in anaerobic paddy conditions), and trans- to underlying plant mechanisms during As stress, and (c) dis- port of As(III) through highly efﬁcient Si transport in rice (Ma cuss the need to investigate integrative biochemical networks in et al., 2008; Zhao et al., 2010). Enhanced accumulation of As in As metabolism. Here the As-mediated alteration in plant biologi- rice is a potentially an important route of human exposure to As, cal process is summarized in terms of genomics, proteomics, and especially in populations with a rice-based diet. However, As tox- metabolomics in the following sections. icity varies greatly with species. For example, As concentrations −1 GENOMIC AND TRANSCRIPTIONAL REGULATION in ﬁsh and shellﬁsh can reach 10 mg kg (Schoof et al., 1999) DURING ARSENIC STRESS and are approximately 10–100 times the levels found in rice grain. ARSENIC TRANSPORTERS However, most As in seafood is present in organic form such as arsenobetaine and arsenocholine that are considered to be non- Analysis of the rice and Arabidopsis genomes revealed presence toxic to humans [acute toxicity∼103 times less than inorganic As of at least 13 and 9 members of the phosphate transporter (Pht1) (As )]. Four species of As are commonly reported in rice grain; family in these species, respectively, (Okumura et al., 1998; Mudge As(III), As(V), monomethylarsonic acid (MMA), and dimethy- et al., 2002; Paszkowski et al., 2002). Shin et al. (2004)indi- larsenic acid (DMA). The dominant species are usually As(III) cated that Pht1;1 and Pht1;4 mediate a signiﬁcant proportion and DMA, although the analysis for As(III) and As(V) is often of the As(V) uptake in Arabidopsis. Arsenite is the dominant As jointly reported as As ’(Williams et al., 2005). The As content species in reducing environments, such as ﬂooded paddy soils i i in rice grains can vary from 10–90% of total As (Heikens et al., (Meharg and Jardine, 2003). Bienert et al. (2008) showed that the 2007), but the reason for this variability has not been established. Nodulin26-like Intrinsic Proteins (NIPs) OsNIP2;1 and OsNIP3;2 Discussion of the health risk of As in rice has largely been based from rice are bi-directional As(III) channels. Direct transport on its As content because these species have generally been con- assays using yeast cells conﬁrmed their ability to facilitate As(III) sidered to be more toxic than MMA and DMA (NRC, 1999) and transport across cell membranes. Ma et al. (2008)reported that Frontiers in Physiology | Plant Physiology July 2012 | Volume 3 | Article 275 | 2 Tripathi et al. Arsenomics two different types of transporters mediate transport of As(III), accumulation in the rice grain. Besides, an epistatic interaction from the external medium to the xylem. Transporters belong- for grain As also looks promising to decrease the concentration ing to the NIP subfamily of aquaporins in rice are permeable of this carcinogen (Norton et al., 2012). Recently, As concen- to As(III) but not to As(V). Mutation in OsNIP2;1 (Lsi1,a sil- trations in different tissues of maize was analyzed using a RIL icon inﬂux transporter) signiﬁcantly decreased As(III) uptake. population (Ding et al., 2011). In this study, three QTLs for As Furthermore, in the rice mutants defective in the silicon efﬂux concentration in leaves were mapped on chromosomes 1, 5, and transporter, Lsi2, As(III) transport to the xylem and accumulation 8, respectively. For As concentration in the bracts, two QTLs were in shoots and grain decreased substantially. Mutation in Lsi2 had identiﬁed, which accounted for around 10% of the observed phe- a much greater impact on As accumulation in shoots and grains in notypic variance. For As concentration in the stems, three QTLs ﬁeld-grown rice than Lsi1. The efﬁcient Si uptake pathway in rice were detected with around 8–15% phenotypic variance. Three also allows inadvertent passage of As(III), thus explaining why QTLs were identiﬁed for kernels on chromosomes 3, 5, and 7, rice is efﬁcient in accumulation of As (Ma et al., 2008). However, respectively, with around 9–11% phenotypic variance. Only one knockout of these transporters may not provide solution to As common chromosomal region between SSR marker bnlg1811 and accumulation, as NIPs facilitate the uptake of vital nutrients such umc1243 was detected for QTLs qLAV1 and qSAC1. These results as boron and silicon (Ma et al., 2008). demonstrated that the As accumulation in different tissues in maize was controlled by different molecular mechanisms. GENE MAPPING FOR ARSENIC AND OTHER ELEMENTS ACCUMULATION DIFFERENTIAL EXPRESSION OF VARIOUS GENES DURING An As tolerance gene has been identiﬁed and mapped to chro- ARSENIC STRESS mosome 6 in rice. The collocation of As tolerance gene with a The effect of As exposure on genome-wide expression was also phosphate uptake QTL in another population of rice provided examined in rice by different groups (Norton et al., 2008a; circumstantial evidence for a mechanism involving the behavior Chakrabarty et al., 2009; Yu et al., 2012). A group of defense of As(V) as a phosphate analog, in agreement with the behavior and stress-responsive transporters including; sulphate trans- of an As resistance gene found in populations of Holocus lana- porters, heat-shock proteins, metallothioneins, multidrug and tus (Dasgupta et al., 2004). Recently, the genetic mapping of the toxic compound extrusion (MATE) transporters, glutathione- tolerance of root growth to As(V) using the Bala X Azucena pop- S-transferase, multidrug resistance proteins, glutathione conju- ulation suggested involvement of epistatic interaction involving gated transportes, metal transporter viz. NRAMP1, and genes of three major genes, two on chromosome 6 and one on chromo- sulfate-metabolizing proteins were commonly upregulated in rice some 10. The study provided physiological evidence that genes during As(V) stress in both the studies (Norton et al., 2008a; related to phosphate transport is unlikely to be behind the genetic Chakrabarty et al., 2009). In contrast, phosphate transporter, zinc loci conferring tolerance (Norton et al., 2008b). However, Zhang transporter, aquaporin gene, amino acid transporters, and per- et al. (2007) measured As accumulation in roots and shoots at the oxidases (PODs) were commonly downregulated, however, some seedling stage and brown rice at maturity of the parental culti- gene like cytochrome P450, oxidoreductase were differentially vars (CJ06/TN1) and their double haploid lines after exposure to regulated in rice seedling challenged with As(V). Yu et al. (2012) 210 mg As/kg As in a pot experiment. Four QTLs for As concen- ﬁrst used high-throughput sequencing technology to study tran- trations were detected in the genetic map. At the seedling stage, scriptomes of plant response to As stress. Overall, by genome- one QTL was mapped on chromosome 2 for As accumulation wide transcriptome and miRNA analyses in rice seedlings treated in shoots which explained 24% of the observed phenotypic vari- with As(III), they found a large number of potentially interest- ance and another QTL for As accumulation in roots was detected ing genes in relation to As(III) stress, especially As(III)-responsive on chromosome 3. At maturity, two QTLs for As accumulation transporters and TFs (transcription factors). The change in the in grains were found on chromosomes 6 and 8, which explained expression of genes related to lipid metabolism and phytohor- 26 and 35% of the phenotypic variance, respectively. This study mone pathways after As(III) exposure was striking, indicating that also showed that the QTL on chromosome 8 was identiﬁed for rice invests more energy and resources into immediate defense As concentrations in grain at maturity and shoot phosphorus (P) needs than into normal growth requirements. concentrations at seedling stage. A study targeting genetic map- Arsenate and As(III) stresses modulated metabolic path- ping of the rice ionome in leaves and grains identiﬁed QTLs for ways networks affecting various physiological processes necessary 17 elements including As, Se, Fe, and Cd. In general, there were for plant growth and development (Chakrabarty et al., 2009). no QTL clusters suggesting independent regulation of each ele- Arsenate stress led to upregulation or downregulation of addi- ment. An epistatic interaction for grain As appears promising tional genes in comparison to As(III), but one glutaredoxin to decrease the concentration of this carcinogenic metalloid in (Os01g26912) is expressed speciﬁcally in the AsIII-treated shoots. thericegrain (Norton et al., 2010). Further, these workers while In one of our studies, four rice genotypes responded differentially identifying QTL for rice grain element composition on an As under As(V) and As(III) stress in terms of gene expression and impacted soil from China, found a correlation between ﬂower- antioxidant defenses (Rai et al., 2011). Arsenate challenge leads ing time and number of element concentrations in grains, which to altered gene expression in a large number of genes involved revealed co-localization between ﬂowering time QTLs and grain in classical oxidative stress response, however, phytochelatin syn- element QTLs. Therefore, this study concluded that ﬂowering thase (PCS) and arsenic reductase (AR) levels were not altered time is one of the major factor that controls As and other element signiﬁcantly. This study suggested that the rice cultivar, IET-4786, www.frontiersin.org July 2012 | Volume 3 | Article 275 | 3 Tripathi et al. Arsenomics is very sensitive to As stress due to reduction of both sulphate in Arabidopsis. At the same time, in both the plants 2 GSTs were assimilation pathway and antioxidant defense enzymes in As downregulated. While most of the cytochrome P450 were upreg- detoxiﬁcation in contrast to the tolerant cultivar, Triguna. The ulated in rice, none of these were upregulated in Arabidopsis.In other two varieties (PNR-546 and IR-36) exhibited intermedi- contrast to A. thaliana, the germin like protein was upregulated ary responses involving regulation of these genes during As stress in rice. Many genes encoding ferritins, ZFP (Zinc ﬁnger pro- (Rai et al., 2011). The differential expression pattern of sulphate tein), patatin, acid phosphates, serine/threonine proteine kinases, transporters were observed for the varieties after As(V) exposure integral membrane proteins, and hydrolases always were down (Kumar et al., 2011). Most of the sulphate transporters studied regulated in both monocot and dicots (Abercrombie et al., 2008; were down-regulated in the sensitive variety IET-4786 after expo- Chakrabarty et al., 2009). The data suggests that though there are sure to As(V). Interestingly, differential alternative splicing for common mechanisms for As metabolisms in dicot and monocot OsSultr1;1 was also observed for all the lines after As exposure. A plants, differential mechanisms may also exists. decrease in accumulation was observed for the largest splice vari- ant containing both the introns at higher concentrations of As(V) ARSENIC TOLERANCE IN TRANSGENIC PLANTS and As(III). In the case of sensitive rice variety, accumulation of Gasic and Korban (2007) reported that overexpression of the the entire splice variant decreased with increasing concentration A. thaliana phytochelatin synthase AtPCS1 gene in Indian mus- of As(V). These results clearly suggest that the expression of sul- tard enhanced tolerance to As and Cd. Similarly, Song et al. phate transporter gene family with respect to heavy metal stress is (2010) showed that in the absence of two ABCC-type trans- regulated differentially in different cultivars. porters, AtABCC1 and AtABCC2, A. thaliana is extremely sen- However, several common processes were affected by As(V) sitive to As and As-based herbicides. Heterologous expression and As(III). Differential expression of several genes that showed of these ABCC transporters in phytochelatin (PC)-producing the highest contrast in a microarray analysis was validated by Saccharomyces cerevisiae enhanced As tolerance and accumu- following the quantitative changes in the levels of individual tran- lation. Furthermore, membrane vesicles isolated from yeasts scripts following challenge with As(V)and As(III). Abercrombie exhibited a pronounced As(III)–PC transport activity. Recently, et al. (2008) ﬁrst studied the transcriptional response of a Indriolo et al. (2010) characterized two genes from P. vittata dicot plants, Arabidopsis thaliana, to As(V) stress using oligonu- (ACR3 and ACR3;1), which encode proteins similar to the ACR3 cleotide microarrays. The study suggested that As(V) stress As(III) efﬂuxer of yeast. It was also showed that ACR3 is local- strongly induces Cu/Zn superoxide dismutase activity (SOD), but ized to the vacuolar membrane in gametophytes, indicating that represses the production of Fe SOD. The study also suggested it likely effuxes As(III) into vacuoles for sequestration. A single involvement of several other genes related to antioxidant systems, copy of ACR3 genes is present in moss, other ferns and gym- various transcription factors, tonoplast proteins, and proteins nosperms but absent in ﬂowering plants. The absence of ACR3 associated with cell wall growth. A comparative biochemical and genes in both monocots and eudicots may preclude their ability to transcriptional proﬁling of two contrasting varieties (tolerant and hyperaccumulate As, which is consistent with the observation that sensitive to As) of Brassica juncea indicated upregulation of sul- no As-hyperaccumulating angiosperm has ever been identiﬁed. fate transporters and auxin and jasmonate biosynthesis pathway Why the highly conserved ACR3 gene was lost in the angiosperm genes, whereas, there was downregulation of ethylene biosyn- lineage may never be known, but its loss coincides with their thesis and cytokinin responsive genes in As tolerant plant in reliance on insects and other animals for pollination and fruit dis- contrast to sensitive plant (Srivastava et al., 2009). In another persal. On the other hand, the selection of As hyperaccumulation experiment, Paulose et al. (2010) studied expression proﬁling in P. vittata, may have evolved as a deterrent and in response to of dicot Crambe abyssinica under As(V) stress using PCR-Select herbivores, as it has recently been shown that insects avoid eating Suppression Subtraction Hybridization (SSH) approach. Their P. vittata grown in the presence of As, preferring those not grown study revealed novel insights into the plant defense mechanisms, in As (Rathinasabapathi et al., 2007). In another study, exam- and the regulation of genes and gene networks in response to arse- ining heterologous expression of the yeast As(III) efﬂux system, nate toxicity. The differential expression of transcripts encoding ACR3 was cloned from yeast and transformed into wild-type and glutathione-S-transferases (GSTs), antioxidant As genes, sulfur nip7;1 Arabidopsis (Ali et al., 2012). At the cellular level, all trans- metabolism genes, heat-shock proteins, metal transporters, and genic lines showed increased tolerance to As(III) and As(V) and a enzymes in the ubiquitination pathway of protein degradation, greater capacity for As(V) efﬂux. With intact plants, three of four as well as several unknown novel proteins serve as molecular stably transformed lines showed improved growth, whereas only evidence for the physiological responses to As(V) stress in plants. transgenic lines in the wild-type background showed increased A comparative evaluation of As responsive genes in mono- efﬂux of As(III) into the external medium. The presence of ACR3 cots and dicots offered interesting observations (Table 1). Various hardly affected tissue As levels, but increased As translocation PODs genes always showed a down regulation (2–24 fold) in to the shoot. Expressing Saccharomyces cerevisiae ScACR3 in rice monocots, however, upregulation of two PODs was recorded in enhanced As(III) Efﬂux and also reduced As accumulation in dicots. MT like proteins was upregulated in monocots. Five fer- rice grains (Duan et al., 2012). In the transgenic lines, As con- rodoxins were down regulated in rice but not in A. thaliana. centrations in shoots and roots were about 30% lower than in Peptidyl prolyl cis-trans isomerase was highly upregulated in rice the wild type, while the As translocation factors were similar in contrast to A. thaliana. Interestingly, 9 GSTs were upregu- between transgenic lines and the wild type. The roots of trans- lated in rice, whereas only one was observed to be upregulated genic plants exhibited signiﬁcantly higher As efﬂux activities than Frontiers in Physiology | Plant Physiology July 2012 | Volume 3 | Article 275 | 4 Tripathi et al. Arsenomics Table 1 | Sets of differentially regulated genes in monocot (O. sativa) and dicot (A. thaliana) plants during “As” stress. Description of gene Monocot Dicot Locus Fold change (+/−) Locus Fold change (+/−) Peroxidase Os05g04410 (−) 4.14 At5g64100 (+)2.50 Os05g04450 (−) 5.94 At1g05250 (+)1.90 Os03g36560 (−) 3.69 At5g17820 (+)1.68 Os07g01410 (−) 5.74 At1g05240 (+)2.05 Os04g59160 (−) 12.60 At3g49120 (−)1.77 Os04g59160 (−) 8.33 At5g64120 (−)1.84 Os04g59260 (−) 3.67 At4g25980 (−)1.52 Os03g25330 (−)3.73 Os03g25340 (−)4.63 Os03g55410 (−)2.33 Os05g06970 (−)2.98 Os07g31610 (−) 10.54 Os04g59190 (−) 34.18 Os05g06970 (−)2.98 Os07g31610 (−) 10.54 Os04g59190 (−) 34.18 Os10g39160 (−)7.71 Os01g18970 (−) 10.62 Os07g44480 (−) 24.42 Os07g44460 (−)7.04 Os07g44460 (−)12.11 Metallothionein-like protein 1 Os12g38064 (+) 2.60 At1g07600 (+)1.67 Os12g38300 (+)2.44 Os04g44250 (+)3.42 Ferredoxin, chloroplast Os08g01380 (−) 3.49 At1g10960 (+)1.53 Os08g01380 (−)3.63 Os08g01380 (−)2.75 Os01g25484 (−)3.67 Os01g64120 (−)4.43 Glycosyl hydrolase family 1 protein Os02g20360 (+) 2.62 At3g09260 (+)1.67 Os01g54300 (−)3.50 Peptidyl prolyl cis-trans isomerase Os04g28420 (+) 18.72 At3g62030 (+)1.64 Hypothetical protein Os08g45120 (+) 5.76 At2g06480 (+)1.58 Os03g07510 (+)3.14 Os08g04560 (+)3.74 Os11g16990 (−)7.55 Glutathione S-transferase Os01g72140 (+) 2.53 At1g78370 (+)1.68 Os01g49710 (+) 3.40 At1g02930 (−)2.10 Os10g20350 (+) 3.31 At1g02920 (−)2.88 Os753122 (+)2.68 Os03g13390 (+)4.01 Os06g44010 (+)2.48 Os07g23570 (+)3.29 Os03g46110 (+)4.91 Os06g13190 (+)2.41 Os01g27630 (−)6.29 Os01g27390 (−)2.46 Catalase Os03g03910 (−) 4.52 At1g20620 (−)1.59 Cationic peroxidase Os01g18950 (−) 20.77 At4g25980 (−)1.52 Lipoxygenase Os08g39850 (+) 4.21 At1g72520 (−)2.41 Os03g49260 (−)2.66 (Continued) www.frontiersin.org July 2012 | Volume 3 | Article 275 | 5 Tripathi et al. Arsenomics Table 1 | Continued Description of gene Monocot Dicot Locus Fold change (+/−) Locus Fold change (+/−) Cytochrome P450 83B1 Os03g55240 (+) 3.07 At4g31500 (−)1.71 Os08g39730 (+) 6.09 At3g48520 (−)1.56 Os02g36190 (+)2.95 Os01g43740 (+)8.51 Os01g38110 (+)7.76 Os01g43774 (+) 30.16 Os01g50170 (+)2.80 Os03g57640 (+)3.00 Os09g27260 (+)8.10 Os03g26210 (+)2.49 Os09g10340 (−)2.74 Germin-like protein Os03g06970 (+) 7.19 At5g39160 (−)1.51 At5g39190 (−)2.13 Ferritin Os12g01530 (−) 3.45 At5g01600 (−)1.78 Os12g01530 (−) 3.29 At3g56090 (−)1.52 Os11g01530 (−)4.58 Zinc ﬁnger protein Os06g04920 (−) 2.72 At3g46090 (−)1.51 At3g46080 (−)1.59 At5g27420 (−)1.75 Acid phosphatase Os07g48320 (−) 3.15 At3g17790 (−)1.62 Gycosyl hydrolase family 17 protein Os02g20360 (−) 2.62 At3g55430 (−)1.53 At4g31140 (−)1.71 At4g19810 (−)1.96 At5g20250 (−)1.52 Xloglucan endotransglucosylase/ hydrolase Os02g17900 (−) 17.69 At4g30280 (−)1.63 Os02g17880 (−) 10.85 At4g14130 (−)2.00 Os06g22919 (−) 10.29 At5g57560 (−)1.68 Patatin Os08g37250 (−) 3.47 At2g26560 (−)1.81 Os08g37250 (−)4.58 Serine/threonine protein kinase Os02g43370 (−) 3.31 At3g08720 (−)1.55 Os12g05394 (−)3.27 Os09g12240 (−)3.49 Integral membrane family protein Os04g45520 (−) 18.34 At4g15610 (−)1.58 NAC domain-containing protein Os10g21630 (+) 5.81 At5g08790 (−)1.53 Os02g15340 (−)3.71 Compilation of data based on monocot O. sativa (Chakrabarty et al., 2009) and dicot (A. thaliana) (Abercrombie et al., 2008) plants during arsenate stress. Upregulated (+), Down regulated (−). those of the wild type. Importantly, ScACR3 expression signiﬁ- by Grispen et al. (2009) by overexpressing AtMT2b in Nicotiana cantly reduced As accumulation in rice straws and grains. When tabacum. It was observed that the highest AtMT2b expressing grown in ﬂooded soil irrigated with As(III)-containing water, line exhibited a signiﬁcant decrease in As accumulation in roots, the As concentration in husk and brown rice of the transgenic but an increased accumulation in shoots, while the total amount lines was reduced by 30 and 20%, respectively, compared with of As taken up remained unchanged. This clearly suggested that the wild type. This study reports a potential strategy to reduce AtMT2b expression may enhance As root to shoot transport. Rice As accumulation in the food chain by expressing heterologous transgenics overexpressing As(III)-S-adenosyl methyl transferase genes in crops. Recently, Sundaram et al. (2009) overexpressed (arsM) has been found to methylate As, and gave 10 fold higher the P. vittata glutaredoxin PvGRX5 gene in Arabidopsis.It was volatile arsenical, maintaining low As levels in rice seed along observed that two lines of A. thaliana constitutively expressing with MMA(V) and DMA(V) in the roots and shoots of trans- PvGrx5 cDNA were signiﬁcantly more tolerant than vector con- genic rice (Meng et al., 2011). The upregulation of Met synthase trol and wild-type lines on the basis of germination, root growth and AdoMet synthetase could correlate with As(III) methylation. and whole plant growth under As stress. A study was conducted Although the amounts of methylated As were small, this may Frontiers in Physiology | Plant Physiology July 2012 | Volume 3 | Article 275 | 6 Tripathi et al. Arsenomics offer a new stratagem for As phytoremediation. Shukla et al. proteome level. A summary of upregulated and downregulated (2012) demonstrated that transgenic tobacco plants expressing proteins during As stress in different plant species is presented Ceratophyllum demersum phytochelatin synthase CdPCS1 had a in Table 2. Expression patterns of maize (Zea mays) root and several fold increase in PC content, precursor non protein thiols, leaf proteins in response to As stress were described for the ﬁrst and enhanced accumulation of As without signiﬁcant decrease in time by Requejo and Tena (2005, 2006). They showed that 10% plant growth. of detectable proteins in maize roots were differentially regu- lated by As; seven of the eleven proteins that were identiﬁed PROTEOME MODULATION DURING ARSENIC STRESS are involved in cellular homeostasis for redox perturbation, sug- gesting that oxidative stress is a major process underlying As During the last decade, several groups have made use of transcrip- tome analysis to investigate the expression patterns of genes in toxicity in plants (Requejo and Tena, 2005). To gain a compre- hensive understanding of the precise mechanisms underlying the plants under As stress (Abercrombie et al., 2008; Norton et al., 2008a; Chakrabarty et al., 2009). Such analysis of gene expres- toxicity of As to rice, the metabolism and defense reactions in As nontolerant plants have recently been examined by Ahsan sion at the mRNA level has enhanced our understanding of the responses of plants to As stress. However, transcriptional anal- et al. (2008). This was done by carrying out a comparative pro- ysis has a number of limitations (Rose et al., 2004), including teomic analysis of rice roots in combination with physiological poor correlations between changes in the expression of mRNAs and biochemical analyses. The comparative proteomic analyses and those of their corresponding proteins (Gygi et al., 1999). identiﬁed 23 differentially expressed proteins in rice roots, includ- Though correlation between mRNA and protein has been noticed ing those predicted as S-adenosylmethionine synthetase (SAMS), (Joosen et al., 2007; Li et al., 2007), protein expression is also cysteine synthase (CS), and novel proteins including tyrosine- speciﬁc protein phosphatase protein, and omega domain contain- regulated at the translational and post-translational levels. Thus, gaining information at the translational and post-translational ing GST. These differentially expressed proteins are functionally involved in cell signaling, stress and detoxiﬁcation, defense and levels can offer deeper insights into the responses and functional interactions of proteins. development, and protein biosynthesis. On the basis of phys- iological and proteomic investigations, it is proposed that As Although large numbers of physiological and biochemical analyses have been performed (Hartley-Whitaker et al., 2001; stress in plants generates ROS, triggering signaling molecules Liu et al., 2005; Williams et al., 2005; Rahman et al., 2007), such as jasmonic acid (JA) and S-adenosyl-L-methionine (SAM), little is known about As stress-elicited changes in plants at the and activating the detoxiﬁcation process, which mainly involves Table 2 | A review of “As” modulated proteins in different plant species during proteomic analysis. Plant species Plant No. of responsive proteins Research outcome References part used and proteomic analysis used Z. mays Root 11, 2-DE, MALDI-TOF MS Upregulation of antioxidant enzymes related proteins Requejo and viz. SODs, GPXs, and peroxiredoxin (Prx) besides four Tena, 2005 additional, functionally heterogeneous, proteins (e.g., ATP synthase, succinyl-CoA synthetase, cytochrome P450, and guanine nucleotide-binding protein b subunit) suggest that the induction of oxidative stress is a main process underlying As toxicity in plants Z. mays Shoot 7, 2-DE, MALDI-TOF MS Down regulation of Translation initiation factor eIF-5A, Requejo and ATP synthase, CS, malate dehydrogenase, protein Tena, 2006 kinase C inhibitor, Tn10 transposase-like protein, and guanine nucleotide binding protein during As stress O. sativa Root 23, 2-DE, MALDI-TOF MS GSH plays a central role in protecting cells against As Ahsan et al., 2008 stress due to synchronous function of SAMS, CS, GSTs, and GR O. sativa Leaf 6, 2-DE, MALDI-TOF MS Down-regulation of RuBisCO and chloroplast 29 kDa Ahsan et al., 2010 ribonucleo proteins under As stress may be the possible causes of the decreased photosynthesis rate P. vittata (G. Frond 19, 2-DE hybrid quadrupole-TOF Multiple forms of glyceraldehyde-3-phosphate Bona et al., 2010 mosseae- MS dehydrogenase, phosphoglycerate kinase, and inoculated) enolase, was upregulated in G. mosseae-inoculated plants, suggests a central role for glycolytic enzymes in As metabolism A. tenuis Leaf 2-DE hybrid quadrupole-TOF MS prominent fragmentation of the RubisCO protein due Duquesnoy et al., to As toxicity 2009 www.frontiersin.org July 2012 | Volume 3 | Article 275 | 7 Tripathi et al. Arsenomics GSH/PC biosynthesis (Ahsan et al., 2008). Interestingly, these resistance in the As hyperaccumulator fern P. vittata,acDNA for pathways are coordinately regulated, with GSH playing a cen- a glutaredoxin (Grx) Pv5–6 was isolated from a frond expression tral role in the complex cellular network. Arsenite and As(V) cDNA library based on the ability of the cDNA to increase As differentially modulated physiological response in Hydrilla ver- resistance in Escherichia coli. The deduced amino acid sequence ticillata, where As(V) stress resulted in activation of the antiox- of Pv5–6 showed high homology with an Arabidopsis chloro- idant defence system, while As(III) responses involved preva- plastic Grx and contained two CXXS putative catalytic motifs. lence of As complexing PCs (Srivastava et al., 2007). Elevated Puriﬁed recombinant Pv5–6 exhibited glutaredoxin activity that levels of antioxidants and PCs were also observed in C. demer- was increased at 10 mM As(V). Site-speciﬁc mutation of Cys sum during As(V) exposure, suggesting the modulation of spe- to Ala resulted in the loss of both GRX activity and As resis- ciﬁc proteins by As induced stress (Mishra et al., 2008). The tance. PvGrx5 has an important role in regulating intracellular As induced antioxidative responses were also validated by pro- As(III) levels, by either directly or indirectly modulating the teomic changes in germinating rice seedlings during As exposure. aquaglyceroporin (Sundaram et al., 2008). Further study of isozymes of SOD, APX, POD, and glutathione Other than these investigations, no proteomic analyses have reductase (GR) validated that As accumulation generated oxida- been carried out on responses of dicotyledonous plants includ- tive stress, which was more pronounced in As(III) treatment ing Arabidopsis, to As stress. Therefore, there is a need for an (Shri et al., 2009). Ahsan et al. (2010)also reported the ﬁrst extended proteomic analysis of the responses of the root systems proteome map of rice leaves under As stress along with phys- of dicotyledonous model plants systems to As stress to gain a bet- iological and biochemical responses. The increased activity of ter understanding of the molecular basis of this response. This several proteins associated with energy metabolism, such as will allow the determination of whether monocot and dicot plants NADP-dependent malic enzyme, NAD-dependent formate dehy- both employ the same defense mechanisms under As stress, and drogenase, and glyceraldehyde-3-phosphate dehydrogenase sug- to identify novel As-responsive proteins for future studies. gest that an increased amount of energy is required to adapt to As stress. However, the down-regulation of RuBisCO and chloro- METABOLOME MODULATION DURING ARSENIC STRESS plast 29 kDa ribonucleoproteins might be the possible causes of Despite the fact that transcriptomic approaches provide almost the decreased photosynthesis rate under As stress. Contrary to complete coverage and proteomics approaches are now capable of this ﬁnding, Duquesnoy et al. (2009) identiﬁed a set of Agrostis detecting most of the cellular protein complement, metabolomics tenuis leaf proteins differentially expressed in response to As is currently capable of determining only a small fraction of the exposure including a major functionally homogeneous group of metabolites found in any one cell. As well as to validate the enzymes including oxygen-evolving enhancer protein, RuBisCO outcome of differential transcriptomic studies along with pro- small and large subunits, RuBisCO activase, and ATP synthase teomic analyses in As stressed plant, metabolome analysis is involved in the Calvin or Krebs cycle. Bona et al. (2010)also needed to investigate the unexplored properties of biological demonstrated the protein expression proﬁle of P. vittata fronds systems. The more challenging aspect of metabolomic technolo- in plants inoculated with one of the two AM fungi (Gigaspora gies is the reﬁned analysis of quantitative dynamics in biological mosseae or Gigaspora margarita) with and without As treatment. systems. For metabolomics, gas and liquid chromatography cou- Up-regulation of multiple forms of glyceraldehyde-3-phosphate pled to mass spectrometry are well suited for coping with high dehydrogenase, phosphoglycerate kinase (PGK), and enolase, pri- sample numbers in reliable measurement times with respect to marily in G. mosseae-inoculated plants, suggests a central role for both technical accuracy and the identiﬁcation and quantitation glycolytic enzymes in As metabolism. Moreover, a putative As of small-molecular-weight metabolites. However to best of our transporter, PgPOR29, has been identiﬁed as an up-regulated pro- knowledge, there is very limited studies have been performed to tein by As treatment. Proteomics in conjunction with morpholog- recognize the modulation of differential metabolomic pathway ical, physiological, and biochemical variables has been employed during As stress. for the ﬁrst time by Pandey et al. (2011) to unravel survival strate- ROLE OF GLUTATHIONE AND PHYTOCHELATIN DURING ARSENIC gies of the diazotrophic cyanobacterium Anabaena sp. PCC7120. Down-regulation of PGK, fructose bisphosphate aldolase II (FBA STRESS II), fructose 1,6 bisphosphatase (FBPase), transketolase (TK), and In most of the studies, metabolites involved in antioxidant sys- ATP synthase on day 1 and their signiﬁcant recovery on the day 15 tems, PCs and related molecules involved in biosynthesis of presumably maintained the glycolysis, pentose phosphate path- PCs have been analyzed during As stress. A list of several As way (PPP) and turnover rate of Calvin cycle, hence survival of the responsive metabolites has been mentioned in the Table 3.The test organism. Up-regulation of CAT, peroxiredoxin (Prx), thiore- raised level of some metal detoxifying thiolic ligand such as doxin (Trx), and oxidoreductase appears to protect the cells from glutathione were also noticed in ferns such as P. vittata, P. ensi- oxidative stress. Appreciable induction in PC content, GST activ- formis (Singh et al., 2006), aquatic plants such as H. verti- ity and transcripts of PCS, AR and As(III) efﬂux genes-asr1102, cilata and C. demersum (Srivastava et al., 2007; Mishra et al., alr1097 reiterates their role in As sequestration and shielding of 2008), and crop plants like B. juncea and O. sativa (Srivastava the organism from As toxicity. While up-regulated metabolic and et al., 2009; Tripathi et al., 2012). While concomitant reduc- antioxidative defense proteins, PC and GST work synchronously, tion in glutathione and S-nitrosoglutathione (GSNO) content the ars genes play a central role in detoxiﬁcation and survival were observed in A. thaliana suggesting the altered GR and S- of Anabaena under As stress. To elucidate the mechanisms of As nitrosoglutathione reductase activities during higher As exposure Frontiers in Physiology | Plant Physiology July 2012 | Volume 3 | Article 275 | 8 Tripathi et al. Arsenomics Table 3 | Metabolites in different plant species during arsenic stress. Metabolites studied Plant species Research outcome References Valine, metheionine, leucine, O. sativa Most of the NEEAs were increased Dwivedi et al., 2010, 2012 in most of the cultivars during As alanine histidine, alanine, proline, glutamic acid, stress, while EAAs were decreased cysteine in most of the cultivar Proline, glutamic acid, S. oleracea Increased during As(V) stress Pavlík et al., 2010 aspartic acid alanine Proline O. sativa Induced during As(III) stress Mishra and Dubey (2006) Cysteine H. verticillata, C. demersum, Increased during As(V) stress Srivastava et al., 2007, 2009; Mishra B. juncea, O. sativa et al., 2008; Tripathi et al., 2012 γ-glutamyl cysteine A. thaliana Increased synthesis during As(V) Dhankher et al., 2002; Li et al., 2004 stress Glutathione A. thaliana, P. vittata, P. ensiformis, Increased during As(V) stress Dhankher et al., 2002; Li et al., 2004; H. verticillata, C. demersum, except in A. thaliana Singh et al., 2006; Srivastava et al., B. juncea, O. sativa, A. thaliana 2007, 2009; Mishra et al., 2008; Tripathi et al., 2012 S-nitrosoglutathione A. thaliana Decreased during As(V) stress Leterrier et al., 2012 Phytochelatins A. thaliana, H. verticillata, Various species of phytochelatins Dhankher et al., 2002; Li et al., 2004; C. demersum, O. sativa were increased during As stress Srivastava et al., 2007; Mishra et al., 2008; Tripathi et al., 2012 Ascorbic acid P. vittata, P. ensiformis, O. sativa Increased during As(V) stress Singh et al., 2006; Tripathi et al., 2012 Malondialdehyde P. vittata, P. ensiformis, Increased during As(V) stress Singh et al., 2006; Srivastava et al., H. verticillata, C. demersum, 2007; Mishra et al., 2008; Tripathi et al., O. sativa 2012 Nitric oxide H. verticillata, O. sativa, A. thaliana Increased during As(V) stress Srivastava et al., 2011; Leterrier et al., 2012; Tripathi et al., 2012 Polyamines (spermidine, T. pratense Polyamines increased only at lower Mascher et al., 2002 spermine) and diamine doses but diamine increased at (putrescine) higher doses during As(V) stress ATP,ADP, NADH, NAD, H. verticillata Level of ATP,NADP,NADH Srivastava et al., 2011 NADPH, NADP decreased, while level of ADP, NADPH and NAD increased during As(V) exposure (Leterrier et al., 2012). Similarly induced level of PCs were also suggests that PCs play a limited role for the hypertolerance observed in H. verticillata, C. demersum, and O. sativa (Srivastava of As in P. vittata. Similarly, Raab et al. (2007)demonstrated et al., 2007; Mishra et al., 2008; Tripathi et al., 2012)under As the As concentration-dependent formation of As–PC complex, stress. Earlier, As-PC complexes were studied in H. lanatus and redistribution and metabolism of As after arrested As uptake in P. cretica using parallel metal(loid)-speciﬁc-ICPMS and organic- Helianthus annuus. The amount and number of As–PC com- speciﬁc-ESI-MS detection systems (Raab et al., 2004). In an in plexes increased exponentially with concentration up to 13.7 μM vitro experiment using a mixture of GSH, PC ,and PC ,As As and As(III)–PC and GS–As(III)–PC complexes were the 2 3 3 2 preferred the formation of the As(III)-PC complex over GSH- dominant species. In another study, Liu et al. (2010)quantiﬁed As(III)-PC , As(III)-(GSH) , As(III)-PC , or As(III)-(PC ) .In As(III)-thiol complexes and free thiol compounds in A. thaliana 2 3 2 2 2 H. lanatus, the As(III)-PC complex was the dominant complex, exposed to As(V). In wild-type roots, 69% of As(III) was com- although GSH, PC ,and PC were found in the tissue extract. plexed as As(III)-PC , As(III)-PC , and As(III)-(PC ) while in 2 3 4 3 2 2 P. cretica only synthesizes PC and forms dominantly the GSH- roots of the GSH-deﬁcient mutant (cad2-1) and the PC-deﬁcient As(III)-PC complex. In both plant species, As is dominantly mutant (cad1-3) very little of As was complexed with As(III)-PCs in non-bound inorganic forms, with 13% being present in PC and As(III)-(GS) , respectively. This conferred approximately 20 complexes for H. lanatus and 1% in P. cretica.Phytochelatin times more tolerance for the wild type than the mutants. These synthesis was induced upon exposure to As(V) in P. vittata, mutants showed signiﬁcantly higher accumulation of As(III) in with only PC detected in the plant (Zhao et al., 2003). The As shoots and efﬂuxed larger amount of As(III) than the wild type, concentration correlated signiﬁcantly with PC concentration in suggesting that enhancing PC synthesis in roots may be an effec- roots and shoots of P. vittata, but not with GSH. Chelation of tive strategy to reduce As translocation to the edible organs only a small proportion (1–3%) of the As with PCs in P. vittata of food crops. Furthermore, transgenic Arabidopsis expressing www.frontiersin.org July 2012 | Volume 3 | Article 275 | 9 Tripathi et al. Arsenomics very high levels of the bacterial γ-glutamylcysteine synthetase P. ensiformis, H. verticillata, C. demersum.Nitric oxide, a sig- (ECS) gene and PCS had several fold higher concentrations of naling molecule was also found to be induced during As(V) γ-glutamylcysteine (EC), GSH, and PCs than the wild type, and stress condition in H. verticillata, O. sativa, and A. thaliana show tolerance to As (Dhankher et al., 2002; Li et al., 2004). (Srivastava et al., 2011; Tripathi et al., 2012; Leterrier et al., 2012). The protection provided by polyamines against oxida- tive stress has been proposed to involve scavenging free radicals CHANGES IN AMINO ACID PROFILING (Drolet et al., 1986) and the reduction of lipid peroxidation Variation in amino acid content was observed in different plant (Borrell et al., 1997). Mascher et al. (2002)demonstrated that species during As exposure. Dwivedi et al. (2010) performed a levels of polyamines viz., spermidine, spermine increased only at simulated pot experiment, using environmentally relevant con- lower doses but diamine increased at higher doses during As(V) centrations of As, analyzed the amino acid proﬁle in grain of stress in red clover (Trifolium pretense). Another study concluded various rice genotypes. This study demonstrated that Speciﬁc −1 that redox state and energetic equilibrium analyzed in terms of As Uptake (SAU, μgg dw), which indicates the ability of As ATP/ADP NADH/NAD, NADPH/NADP, GSH/GSSG, and AsA/ uptake by rice per unit root under As exposure, was different DAsA ratios, were found to be altered due to As toxicity in H. ver- between rice genotypes, and found in the order of As tolerant ticillata (Srivastava et al., 2011). Hence, variation in metabolite Triguna (134) > IR-36 (71.5) > PNR-519 (53) > sensitive IET- −1 proﬁling during As exposure in different plant species signify that 4786 (29). However, the grain As concentration (μgg dw) order plants modulate their metabolome to respond against As stress. was IR-36 (1.5) > Triguna (1) > PNR-519 (0.5) > IET-4786 (0.3). They concluded that most of the essential amino acids (EAAs) metabolites such as valine, metheionine, leucine, alanine, and FUTURE PROSPECTS nonessential amino acids (NEAAs) viz. histidine, alanine, proline, As presents a health hazard to human populations world-wide glutamic acid, and cysteine increased in most of the rice geno- due to its mobilization and accumulation in plant parts. As types during As(V) exposure. Further to validate this ﬁnding a accumulation and homeostasis require the co-ordination of sev- ﬁeld experiment was conducted, determining the amino acid pro- eral processes working simultaneously to regulate uptake, long- ﬁle of sixteen rice genotypes differing in grain As accumulation, distance transport, and distribution of metalloid to different cells grown at three sites with different soil As concentrations in West and tissues. In the last few years, various QTLs as well as genes Bengal and India. Grain As accumulation negatively correlated including those encoding transporters, genes mediating As accu- with EAAs which were more prominent in high As accumulat- mulation, vacuolar sequestration, and distribution breakthroughs ing rice genotypes (HAARGs). Conversely, NEAAs showed an in As speciation with a diverse range of advanced techniques increase in low As accumulating rice genotypes (LAARGs) but opening a new and unheralded insight to cellular speciation, such a decrease in HAARGs. EAAs like isoleucine, leucine, valine, as micro-XAS and coupled HPLC-ICP-MS - ESI-MS. The eval- phenylalanine, and tyrosine also decreased in most of the geno- uation of transcriptomic, proteomic, and metabolomic analyses types (Dwivedi et al., 2012). Some other amino acids for example indicate that thiol peptides like glutathione and PCs play a central proline, glutamic acid, aspartic acid, and alanine also increased role in As detoxiﬁcation, as well as various antioxidant defense during As(V) stress in Spinacia oleracea (Pavlík et al., 2010). system response against As induced oxidative stress. However, not Among stress responsive amino acids, proline is a much studied many studies have been carried out to study global change in molecules and can function as an osmolyte, free radical scavenger term of transcriptome, proteome, and metabolome. A compar- and also protects the cell membrane against damage. The level of ative evaluation of proteome, transcriptome, and metabolomic proline has also been observed to be elevated in O. sativa during approaches in tolerant and sensitive varieties of plants such as rice As (III) stress (Mishra and Dubey, 2006). The S-containing amino and other plants, including Arabdopsis, may offer huge oppor- acid, cysteine, plays a central role in As detoxiﬁcation, as it is a tunities for the deeper understanding to develop As tolerant primary metabolite for synthesis of GSH and PCs. The cysteine plants, including safer crops for human consumption (Figure 1). content increased in some aquatic plants such as H. verticillata, Further, studies pertaining to transcriptional responses show rootless plant C. demersum, andcropplants B. juncea, O. sativa expression of several genes with unclear or unknown biological during As stress (Srivastava et al., 2007, 2009; Mishra et al., 2008; functions, providing future targets for plant Arsenomics research. Tripathi et al., 2012). However, the QTLs analysis in various As stressed plant species provide an insight into the genetic basis of As uptake and accumu- OTHER METABOLITES lation and will be useful for molecular breeding for As tolerance in Some low molecular antioxidant like ascorbate (AsA) and dehy- rice. Epistatic interaction for grain As appear promising to reduce droascorbate (DAsA), which work as non-enzymatic antioxidants the health risk due to this carcinogen. Understanding of these in the glutathione-ascorbate cycle for free radical scavenging, omics approaches which will lead to Arsenomics and use of infor- were also analyzed in some plants during As(V) exposure. As(V) mation generated could help to breed plants with low As in edible exposure caused an increase in the ratio of AsA/DAsA in P. plant parts, along with the species of As present being of low toxi- vitatta, P. ensiformis, H. verticillata, and O. sativa (Singh et al., city. Therefore, future research should focus on ﬁlling gaps in our 2006; Srivastava et al., 2011; Tripathi et al., 2012) indicating knowledge, taking advantages of modern analytical tools and a the signiﬁcant role of ascorbate for As induced stress amelio- combination of different omics approaches for enhanced As phy- ration. Malondialdehyde (MDA), the byproduct of lipid perox- toremediation and development of As tolerant crops with safer idation was also increased during As(V) expsoure in P. vittata, grain As levels. Frontiers in Physiology | Plant Physiology July 2012 | Volume 3 | Article 275 | 10 Tripathi et al. Arsenomics FIGURE 1 | Omics of As accumulation and tolerance: comparative study of As tolerant and sensitive plants at various levels such as genome, transcriptome, proteome, and metabolome to generate information to develop low grain As crops using breeding and molecular tools. University of Aberdeen, UK for scientiﬁc and linguistic ACKNOWLEDGMENTS improvement of the manuscript. Preeti Tripathi and Sonali The authors are thankful to Director, CSIR-National Botanical Dubey are thankful to Council of Scientiﬁc and Industrial Research Institute, Lucknow, for the facilities and for the Research, New Delhi, India, for the award of Senior Research ﬁnancial support from the network projects (NWP) (CSIR), Fellowship. New Delhi, India. We are also grateful to G. J. Norton, REFERENCES and Lee, B.-H. (2010). Analysis of of plant aquaporins facilitate the and Tuli, R. (2009). Comparative Abedin,M.J., Feldmann, J.,and arsenic stress-induced differentially bi-directional diffusion of As(OH) transcriptome analysis of arse- Meharg, A. A. (2002). Uptake kinet- expressed proteins in rice leaves by and Sb(OH) across membranes. nate and arsenite stresses in ics of arsenic species in rice plants. two-dimensional gel electrophore- BMC Plant Biol. 6, 26. rice seedlings. Chemosphere 74, Plant Physiol. 128, 1120–1128. sis coupled with mass spectrometry. 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The that could be construed as a potential of arsenic metabolism in plants. Front. under the terms of the Creative role of phytochelatins in arsenic conﬂict of interest. Physio. 3:275. doi: 10.3389/fphys. Commons Attribution License, tolerance in the hyperaccumulator 2012.00275 which permits use, distribution Pteris vittata. New Phytol. 159, Received: 11 January 2012; accepted: 27 This article was submitted to Frontiers in and reproduction in other forums, 403–410. June 2012; published online: 23 July Plant Physiology, a specialty of Frontiers provided the original authors and source 2012. in Physiology. are credited and subject to any copyright Conﬂict of Interest Statement: The Citation: Tripathi RD, Tripathi Copyright © 2012 Tripathi, notices concerning any third-party authors declare that the research P, Dwivedi S, Dubey S, Tripathi, Dwivedi, Dubey, Chatterjee, graphics etc. Frontiers in Physiology | Plant Physiology July 2012 | Volume 3 | Article 275 | 14

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Arsenomics: omics of arsenic metabolism in plants

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