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doi: 10.1104/pp.18.00454pmid: N/A
The Origins of Protein Storage Vacuoles During seed development, protein reserves and minerals are stored in specialized vacuoles called protein storage vacuoles (PSVs). PSVs are functionally different from the lytic vacuoles (LVs) that serve a lysosome-like role in vegetative plant tissues. Embryonic vacuoles (EVs) also are present during early embryogenesis. Later, during the maturation phase of seed development, PSVs arise to accumulate storage reserves and ultimately become the only detectable vacuole. PSVs persist in embryonic cells until seed germination, when reserves are mobilized to provide nutrients for the growing seedling. Controversy exists as to whether PSVs arise de novo during seed development or originate from preexisting EVs. Feeney et al. (pp. 241–254) have tested these two hypotheses by studying PSV formation in Arabidopsis (Arabidopsis thaliana) embryos at different stages of seed maturation as well as in Arabidopsis leaves reprogrammed to an embryogenic fate by the induced expression of the LEAFY COTYLEDON2 transcription factor, a master regulator of seed maturation. The authors produced transgenic Arabidopsis lines expressing fluorescent protein-tagged markers for the tonoplast and the lumen of PSVs as well as tonoplast markers for preexisting vacuoles (LVs in leaves and EVs in seeds). In addition, they visualized PSVs using both fluorescent pH-sensitive stains and inherent PSV autofluorescence. Confocal and immunoelectron microscopy indicated that both storage proteins and tonoplast proteins typical of PSVs were delivered to the preexisting EVs or to the LVs in reprogrammed leaf cells. These results indicate that Arabidopsis PSVs arise by the remodeling of preexisting vacuoles rather than by the de novo biogenesis of PSVs. Calcium Dynamics in Chloroplasts Transient changes in intracellular free Ca2+ concentration ([Ca2+]) are involved in the sensing of a wide variety of abiotic and biotic stimuli in plants. The unique spatiotemporal patterns in [Ca2+] that result enable specific stimulus-response coupling. Several intracellular compartments of the plant cell participate in Ca2+ homeostasis, including the vacuole, endoplasmic reticulum, mitochondria, and plastids. Numerous studies indicate that chloroplasts require a fine-tuned control of the organellar Ca2+ concentration. It is known that free Ca2+ modulates crucial aspects of photosynthesis, including the assembly and function of PSII, the regulation of stromal enzymes of the Calvin cycle, as well as other plastid-localized processes such as the import of nucleus-encoded proteins and organelle division. However, little is known about the mechanisms that underlie the generation and dissipation of Ca2+ transients and the transduction of environmental signals within plastids or their localization inside the organelle. To investigate the involvement of thylakoids in Ca2+ homeostasis and in the modulation of chloroplast Ca2+ signals in vivo, Sello et al. (pp. 38–51) targeted the bioluminescent Ca2+ reporter aequorin (fused with YFP) to the lumen and the stromal surface of thylakoids in Arabidopsis. In resting conditions in the dark, free Ca2+ levels in the thylakoid lumen were maintained at about 0.5 mm, which was a 3- to 5-fold higher concentration than in the stroma. Monitoring of chloroplast Ca2+ dynamics in different intrachloroplast subcompartments (stroma, thylakoid membrane, and thylakoid lumen) revealed the occurrence of stimulus-specific Ca2+ signals, characterized by unique kinetic parameters. Oxidative and salt stresses initiated pronounced free Ca2+ changes in the thylakoid lumen. Evidence also was obtained for dark-stimulated intrathylakoid Ca2+ changes. The novel toolkit of thylakoid-targeted Ca2+ reporters reported upon advances our current understanding of Ca2+ regulation in chloroplasts and paves the way for future investigations on plant organellar Ca2+ signaling. Iron Accumulation and Fraxetin, a Coumarin Soil pH has a strong influence on the availability of mineral nutrients and the distribution of species in natural plant communities. Iron (Fe) solubility decreases dramatically with increasing pH. In alkaline soils, calcifuge (“chalk-fleeing”) species are unable to compete due to their inability to acquire sufficient Fe. Calcicole behavior (i.e. the ability to thrive on alkaline soils) has been attributed to the efficiency of Fe acquisition of a cultivar or species, a trait that strongly contributes to the ability to compete on such soils. In Arabidopsis, the scopoletin pathway is reprogrammed upon Fe deficiency to produce and secrete coumarins with Fe-mobilizing properties. In this issue, Tsai et al. (pp. 194–207) examine the biosynthesis and ecological role of Fe-mobilizing coumarins secreted by Fe-deficient Arabidopsis plants. More specifically, they show that scopoletin 8-hydroxylase (S8H) participates in Fe acquisition by mediating the biosynthesis of fraxetin (7,8-dihydroxy-6-methoxycoumarin), a coumarin derived from the scopoletin pathway. S8H is highly induced in roots of Fe-deficient plants. Mutants defective in the expression of S8H showed increased sensitivity to growth on pH 7 medium and reduced secretion of fraxetin. Transgenic lines overexpressing S8H exhibited an opposite phenotype. Homozygous s8h mutants grown on medium with immobilized Fe accumulated significantly more scopolin, the storage form of scopoletin. Supplementaion of a medium containing immobile Fe with fraxetin partially rescued the s8h mutants. In natural Arabidopsis accessions differing in their performance on medium containing immobilized Fe, the amount of secreted fraxetin was highly correlated with growth and Fe and chlorophyll contents, indicating that fraxetin secretion is a key factor in the calcicole-calcifuge behavior of plants. Leaf Metabolism in Response to Dark One of the more prevalent methods used to initiate plant senescence under laboratory conditions is to grow plants in prolonged dark conditions. The course of “dark-induced senescence” depends upon whether individual leaves on the plant or the entire plant is darkened: an individually darkened leaf initiates senescence much more rapidly than the leaves of an intact darkened plant. Combining transcriptomic and metabolomic approaches in Arabidopsis, Law et al. (pp. 132–150) present an overview of the metabolic strategies that are employed in response to these two different darkening treatments. They report that when entire plants are darkened, carbon starvation initiates a profound metabolic readjustment in which branched-chain amino acids and potentially monosaccharides released from cell wall loosening become important substrates for maintaining minimal ATP production. Concomitantly, the increased accumulation of amino acids with a high nitrogen-carbon ratio may provide a safety mechanism for the storage of metabolically derived cytotoxic ammonium and a pool of nitrogen that can be utilized upon the return to typical growth conditions. In contrast, in individually darkened leaves, a temporal and differential exchange of metabolites, including sugars and amino acids, between the darkened leaf and the rest of the plant is initiated. This active transport could be the basis for a progressive metabolic shift in the substrates fueling mitochondrial activities, which are central to the catabolic reactions facilitating the retrieval of nutrients from the senescing leaf. The authors propose a working model that provides an overview of the different metabolic strategies employed by plants in response to these two different darkening treatments. Phosphorous Deficiency and Photosynthesis Phosphorus (P) is an essential macronutrient, and P deficiency limits plant productivity. P influences many aspects of photosynthesis. P-deficient plants typically remain green and do not de velop leaf chlorosis, and yet P starvation immediately affects CO2 assimilation. Specifically, P deficiency is believed to affect CO2 assimilation by reducing the ATP-dependent regeneration of ribulose-1,5-bisphosphate in the Calvin cycle. Recent research, however, also has revealed that P deficiency affects electron transport to PSI. In this issue, Carstensen et al. (pp. 271–284) present a comprehensive biological model describing how P deficiency disrupts the photosynthetic machinery and the electron transport chain in barley (Hordeum vulgare). They report that P deficiency reduces the orthophosphate concentration in the chloroplast stroma to levels that inhibit ATP synthase activity. Under P deficiency, the enhanced electron flow through PSI increases the levels of NADPH, whereas ATP production remains restricted and, hence, reduces CO2 fixation. In parallel, lumen acidification activates the energy-dependent quenching component of the nonphotochemical quenching mechanism and prevents the overexcitation of PSII and damage to the leaf tissue. Consequently, plants can be severely affected by P deficiency for weeks without displaying any visual leaf symptoms. All of the processes in the photosynthetic machinery influenced by P deficiency appear to be fully reversible and can be restored in less than 1 h after resupply of P to the leaf tissue. Origin of Plant R Genes Plants rely on two branches of the innate immunity system to prevent or eliminate microbial infections: one involves cell surface receptors to respond to pathogen- or microbe-associated molecular patterns, and the other acts inside plant cells by using proteins with nucleotide-binding site (NBS) and leucine-rich repeat (LRR) domains. NBS-LRR proteins confer recognition of pathogen effectors either directly or indirectly and trigger disease resistance. Most of the plant disease-resistance genes (R genes) cloned so far encode NBS-LRR proteins. NBS-LRR proteins are typically classified into two major subfamilies based on the presence or absence of an N-terminal signaling domain. Those possessing the Toll/IL receptor (TIR) domain are referred to as TIR-NBS-LRR proteins; those without this domain are referred to as non-TIR-NBS-LRR proteins. Comparative genomic analyses show that R genes are widely distributed in land plants. However, no R genes have been reported in algae to date. Thus, plant R genes are generally thought to have originated in land plants, but this idea appears mistaken. Gao et al. (pp. 82–89) have performed comparative genomic and phylogenetic analyses of R genes in a wide variety of plants, with an emphasis on basal-branching plants. They report on the presence of R genes in the genomes of basal-branching streptophytes, including charophytes, liverworts, and mosses. Phylogenetic analyses suggest that plant R genes originated in charophytes and R proteins diversified into TIR-NBS-LRR proteins and non-TIR-NBS-LRR proteins in charophytes. Moreover, R proteins evolved in a modular fashion through frequent gain or loss of protein domains. Most of the R genes in basal-branching streptophytes underwent adaptive evolution, indicating an ancient involvement of R genes in plant-pathogen interactions. These findings provide novel insights into the origin and evolution of R genes and the mechanisms underlying the colonization of terrestrial environments by plants. Author notes www.plantphysiol.org/cgi/doi/10.1104/pp.18.00454 © 2018 American Society of Plant Biologists. All Rights Reserved. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model)
doi: 10.1104/pp.18.00235pmid: 29720530
The discovery of semidwarfing genes in wheat and rice was a crucial turning point of the Green Revolution in the late 1960s. The Green Revolution aimed to maintain per capita food supplies worldwide despite the projected doubling of global population by the end of the 20th century. Its main features were the introduction of new high-yielding wheat and rice varieties combined with intensified agricultural practices, including increased application of fertilizers, pesticides, and irrigation. Unfortunately, this higher intensity agriculture led to stem lodging (bending) and the consequent loss of grain yield. This issue was solved by introducing semidwarfing genes that resulted in varieties with shorter stalks that were strong enough to support the heavy grains and extra yield due to improved assimilate partitioning into the grains (Hedden, 2003). These Reduced height (Rht) genes have been widely used, and in the 1990s, their molecular basis was found to be due to mutations in a gibberellic acid (GA) signaling gene leading to reduced responsiveness to GA. In this issue, Ford et al. (2018) identify the gene underlying an alternative height-reducing mechanism for wheat. The commercial semidwarf durum cv Icaro, also called Rht18 for the semidwarfing gene responsible for its phenotype, was remutagenized and screened for “overgrowth” mutants. The identified overgrowth plants were 10 to 30 cm taller than the parental plant Icaro. Genetic analysis showed that the responsible mutations were most likely allelic and linked to Rht18, which was previously mapped to the centromeric region of chromosome 6A. Given the large size of the wheat genome, an elegant approach of specifically sequencing chromosome 6A, isolated by flow cytometry sorting, was used to discover the causal mutations. This approach revealed that several independent lines of both tetraploid and hexaploid (bread) wheat contained mutations in the predicted coding region of GA 2-oxidaseA9 (GA2oxA9), which catalyzes the deactivation of bioactive GAs. The mutations occurred at conserved amino acid positions and reduced or eliminated GA2oxA9 activity. GA2oxA9 expression was greater in the elongating peduncle and leaf tissue of the semidwarf lines than of the tall parents. Ford and coworkers determined the GA contents in these lines and found that the levels of bioactive GA1 were reduced, suggesting that flux through the GA biosynthetic pathway was reduced. Ford et al. present a mechanistic model of GA2oxA9-mediated regulation of plant height (Fig. 1). Increased expression of GA2oxA9 in the semidwarf cultivar enhances conversion of GA12 to inactive GA110. This competing reaction decreases flux through the biosynthetic pathway that gives rise to bioactive GA1. Less GA1 causes a reduction in plant height. In the suppressor mutants with impaired GA2oxA9, the conversion of GA12 to GA110 is inhibited. Consequently, normal flux through the GA biosynthetic pathway, normal GA1 content, and plant height are restored. Ford and coworkers conclude that GA2oxA9 is likely responsible for both the semidwarf and overgrowth phenotypes. Figure 1. Open in new tabDownload slide Model of GA2oxA9-mediated modulation of plant height. GA2oxA9 stimulates the conversion of GA12 to inactive GA110 and of GA53 to GA97. Reduced flux through the GA biosynthetic pathway lowers bioactive GA1 content, resulting in semidwarfism. Mutations in GA2oxA9 impair competing GA12 and GA53 metabolism and restore flux through the GA biosynthetic pathway, GA1 content, and plant height. (Figure from Ford et al., 2018, figure 7.) Figure 1. Open in new tabDownload slide Model of GA2oxA9-mediated modulation of plant height. GA2oxA9 stimulates the conversion of GA12 to inactive GA110 and of GA53 to GA97. Reduced flux through the GA biosynthetic pathway lowers bioactive GA1 content, resulting in semidwarfism. Mutations in GA2oxA9 impair competing GA12 and GA53 metabolism and restore flux through the GA biosynthetic pathway, GA1 content, and plant height. (Figure from Ford et al., 2018, figure 7.) This work illustrates the rapid progress in wheat research by highlighting the steps taken beyond the conventional, laborious techniques of gene cloning. In particular, isolating individual chromosomes reduces the complexity of the polyploid wheat genome. The authors demonstrate that suppressor screens in which chromosome isolation is combined with next-generation sequencing and new bioinformatic tools (Sánchez-Martín et al., 2016) can more easily identify genes underlying a phenotype of interest. Further work is needed to elucidate the precise molecular mechanism by which GA2oxA9 expression and activity are regulated. However, the authors anticipate that their discovery will provide wheat breeders with a range of new semidwarf mutants not genetically linked to the widely used Rht-B1 and Rht-D1 alleles. LITERATURE CITED Ford AB , Foo E, Sharwood R, Karafiatova M, Vrána J, MacMillan C, Nichols DS, Steuernagel B, Uauy C, Doležel J, et al. ( 2018 ) Rht18 semidwarfism in wheat is due to increased GA 2-oxidaseA9 expression and reduced GA content . Plant Physiol 177 : 168 – 180 Google Scholar Crossref Search ADS PubMed WorldCat Hedden P ( 2003 ) The genes of the Green Revolution . Trends Genet 19 : 5 – 9 Google Scholar Crossref Search ADS PubMed WorldCat Sánchez-Martín J , Steuernagel B, Ghosh S, Herren G, Hurni S, Adamski N, Vrána J, Kubaláková M, Krattinger SG, Wicker T, et al. ( 2016 ) Rapid gene isolation in barley and wheat by mutant chromosome sequencing . Genome Biol 17 : 221 Google Scholar Crossref Search ADS PubMed WorldCat Author notes 1 Address correspondence to [email protected]. www.plantphysiol.org/cgi/doi/10.1104/pp.18.00235 © 2018 American Society of Plant Biologists. All Rights Reserved. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model)
doi: 10.1104/pp.18.00350pmid: 29720531
The humble spud. Simple, unassuming, yet vital in supporting a large proportion of the world’s population. Historically speaking, much of the research performed on potatoes (Solanum tuberosum) has gone into enhancing their disease resistance, justifiably so given the severe famines brought about through potato blight in the mid-1800s and early 1900s. More recently, however, researchers have turned to studying other aspects of potato development in hopes of enhancing crop yields. The Green Revolution of the 1960s dramatically enhanced global production of wheat (Triticum aestivum), rice (Oryza sativa), and maize (Zea mays). This increase was brought about (in part) through the development of semidwarf varieties of these crops. The compact structure of these semidwarf varieties made them more resistant to mechanical damage and enabled their planting at much higher densities. Despite the huge gains achieved in these cereal crops, there have been relatively few attempts to apply the concepts of the Green Revolution to potatoes (and tubers in general; Villordon et al., 2014). In this issue of Plant Physiology, Crocco et al. (2018) report on the overexpression of a B-box transcription factor (AtBBX21) from the model plant species Arabidopsis (Arabidopsis thaliana) in potato. The resulting transgenic lines assumed a short, stocky structure with thick stems and leaves. They had very high levels of chlorophyll and accordingly very efficient photosynthesis. They also accumulated anthocyanins and phenolics, which enabled their photosynthetic machinery to better withstand high light levels. Additionally, these plants responded less to simulated shade, an important trait for plants grown in monoculture. Significantly, the outcome of these phenotypic traits was a 15% increase in tuber yield. AtBBX21 is a positive regulator of light signaling in Arabidopsis, so it is assumed that its overexpression in potato is comparable to a hyperresponsiveness to light. There have been previous attempts to express other components of the Arabidopsis light signaling pathway in potato, notably the gene encoding the predominant red light photoreceptor phytochrome B (phyB; Thiele et al., 1999; Boccalandro et al., 2003). Overexpression of AtPHYB has many similar effects to overexpression of AtBBX21. AtPHYB overexpressors have a compact phenotype, are more tolerant of competition from their neighbors, photosynthesize more efficiently, and have higher yields (Thiele et al., 1999; Boccalandro et al., 2003). However, it has been shown that AtPHYB overexpression in Arabidopsis is accompanied by a strong reduction in water use efficiency (Boccalandro et al., 2009). Crocco et al. show that overexpression of AtBBX21 in potato has no negative effects on water use efficiency, a crucial trait for a drought-sensitive crop like potato. It may be that overexpression of AtPHYB activates the entire photomorphogenic response, whereas overexpression of a transcriptional regulator like AtBBX21 activates only a subset of this developmental pathway. Our understanding of what AtBBX21 does on the molecular level is still in its infancy. AtBBX21 belongs to a subset of the BBX protein family (subfamily IV; Crocco and Botto, 2013). The members of subfamily IV have contradictory roles in light signaling, with some promoting and some repressing photomorphogenic development. Members of this group are often thought of as modulators that fine-tune plant responses to abiotic cues (Sarmiento, 2013). We know that AtBBX21 interacts with a key regulator of light responses in plants, ELONGATED HYPOCOTYL5 (AtHY5; Datta et al., 2007). AtBBX21 also promotes AtHY5 expression, and the hyperphotomorphogenic phenotype of an AtBBX21 overexpressor in Arabidopsis is dependent on the presence of AtHY5 (Xu et al., 2016). Therefore, it is possible that the overexpression of AtBBX21 in potato acts to enhance the expression of the native StHY5 gene. Crocco et al. ascribe the increased tuber number in their AtBBX21 overexpressor lines to an increase in photosynthetic efficiency. However, recent developments suggest that there could also be more direct effects on root development. Root system architecture has a strong effect on tuberization (Villordon et al., 2014), and recent studies in Arabidopsis have shown that AtHY5 directly influences the structure of the root (Chen et al., 2016; van Gelderen et al., 2018). It is therefore tempting to speculate that StHY5 could play a direct role in tuber formation. Crocco et al. have shown that the modulation of crop traits through heterologous expression of B-box proteins has great promise for the development of new crops. It will be exciting to see if the same approach yields similar benefits in other species. LITERATURE CITED Boccalandro HE , Ploschuk EL, Yanovsky MJ, Sánchez RA, Gatz C, Casal JJ ( 2003 ) Increased phytochrome B alleviates density effects on tuber yield of field potato crops . Plant Physiol 133 : 1539 – 1546 Google Scholar Crossref Search ADS PubMed WorldCat Boccalandro HE , Rugnone ML, Moreno JE, Ploschuk EL, Serna L, Yanovsky MJ, Casal JJ ( 2009 ) Phytochrome B enhances photosynthesis at the expense of water-use efficiency in Arabidopsis . Plant Physiol 150 : 1083 – 1092 Google Scholar Crossref Search ADS PubMed WorldCat Chen X , Yao Q, Gao X, Jiang C, Harberd NP, Fu X ( 2016 ) Shoot-to-root mobile transcription factor HY5 coordinates plant carbon and nitrogen acquisition . Curr Biol 26 : 640 – 646 Google Scholar Crossref Search ADS PubMed WorldCat Crocco CD , Ocampo GG, Ploschuk EL, Mantese A, Botto JF ( 2018 ) Heterologous expression of AtBBX21 enhances the rate of photosynthesis and alleviates photoinhibition in Solanum tuberosum . Plant Physiol 177 : 369 – 380 Google Scholar Crossref Search ADS PubMed WorldCat Crocco CD , Botto JF ( 2013 ) BBX proteins in green plants: insights into their evolution, structure, feature and functional diversification . Gene 531 : 44 – 52 Google Scholar Crossref Search ADS PubMed WorldCat Datta S , Hettiarachchi C, Johansson H, Holm M ( 2007 ) SALT TOLERANCE HOMOLOG2, a B-box protein in Arabidopsis that activates transcription and positively regulates light-mediated development . Plant Cell 19 : 3242 – 3255 Google Scholar Crossref Search ADS PubMed WorldCat Sarmiento F ( 2013 ) The BBX subfamily IV: additional cogs and sprockets to fine-tune light-dependent development . Plant Signal Behav 8 : e23831 Google Scholar Crossref Search ADS PubMed WorldCat Thiele A , Herold M, Lenk I, Quail PH, Gatz C ( 1999 ) Heterologous expression of Arabidopsis phytochrome B in transgenic potato influences photosynthetic performance and tuber development . Plant Physiol 120 : 73 – 82 Google Scholar Crossref Search ADS PubMed WorldCat van Gelderen K , Kang C, Paalman R, Keuskamp D, Hayes S, Pierik R ( 2018 ) Far-red light detection in the shoot regulates lateral root development through the HY5 transcription factor . Plant Cell 30 : 101 – 116 Google Scholar Crossref Search ADS PubMed WorldCat Villordon AQ , Ginzberg I, Firon N ( 2014 ) Root architecture and root and tuber crop productivity . Trends Plant Sci 19 : 419 – 425 Google Scholar Crossref Search ADS PubMed WorldCat Xu D , Jiang Y, Li J, Lin F, Holm M, Deng XW ( 2016 ) BBX21, an Arabidopsis B-box protein, directly activates HY5 and is targeted by COP1 for 26S proteasome-mediated degradation . Proc Natl Acad Sci USA 113 : 7655 – 7660 Google Scholar Crossref Search ADS PubMed WorldCat Author notes 1 Address correspondence to [email protected]. www.plantphysiol.org/cgi/doi/10.1104/pp.18.00350 © 2018 American Society of Plant Biologists. All Rights Reserved. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model)
doi: 10.1104/pp.18.00344pmid: 29720532
Oxygen (O2) is evolved during photosynthetic electron transport when water is split by the oxygen-evolving complex to provide protons and electrons to the chloroplastic electron chain, thereby generating ATP and NADPH—the energy source and reducing power for plant metabolism. The majority of this chemical energy is used to drive photosynthetic carbon metabolism, which consists of ribulose-1,5-bisphosphate carboxylation (photosynthetic carbon reduction cycle) and oxygenation (photosynthetic carbon oxidation cycle); with a combined electron requirement = JA. Four electrons are required for every O2 evolved so that gross O2 production (GOP) is related to linear electron transport (J) according to J/4. When linear electron transport is used only to drive CO2 fixation, the consumption of O2 and the release of CO2 by photosynthetic carbon oxidation and mitochondrial respiration is such that net O2 production (NOP) is equal to net CO2 assimilation (Anet; provided the respiratory quotient is 1, but see Tcherkez et al., 2017). Additionally, electrons can be used for alternative noncyclic electron transport (ANCET), including, for example, the photoreduction of O2 itself forming reactive oxygen species (Mehler-peroxidase reactions or “water-water cycle”; Asada, 1999), chloroplastic anabolism (e.g. lipids; Stumpf et al., 1963), the reduction of oxaloacetate to malate (which is exported to the mitochondria; Scheibe, 2004), and nitrogen assimilation (Bloom et al., 1989). ANCET has been hypothesized both as a way to regulate ATP/NADPH ratio to meet the changing energy demands of cellular metabolism and as a mechanism to prevent photodamage through utilizing excess reductant when the photon flux density exceeds the energy requirement of CO2 fixation (e.g. under high irradiance, cold temperatures, water stress closing stomata; e.g. Badger, 1985; Ort and Baker, 2002; Robinson, 1988). Importantly, there is no formal evidence for how electron flows interact, particularly under fluctuating light conditions (Morales et al., 2018). As ANCET allows for greater rates of linear electron transport to be sustained, total electron transport (Jt) will be greater than JA. Conversely, the effect on O2 uptake will be dependent on the metabolic pathway involved. For example, in the Mehler-peroxidase reactions, there is no net change in O2 so that NOP will remain equal to Anet. But in the reduction of nitrate, the ratio between N-linked O2 production and O2 consumption is highly dependent on the amino acid synthesized (Noctor and Foyer, 1998). In this case, NOP will not always equal Anet because O2 and CO2 may not be balanced in metabolism (Skillman, 2008). Consequently, concomitant measurements of CO2 and O2 fluxes are important to the understanding of how plants regulate the use of light energy, with different fates having very different metabolic outcomes. The earliest measurements of O2 evolution were unable to distinguish GOP from uptake of O2 (Hill, 1937). The mass spectrometry method established by Mehler and Brown (1952) solved this problem by employing O2 isotope tracers to independently monitor fluxes of 16O2 and 18O2. In this method, pure 18O2 was supplied to the gas headspace of a closed chamber, and the decline in 18O2 was attributed to O2 uptake. O2 evolved carries the same isotopic composition as the water from which it is generated; in this case, the dominant isotope in the water was 16O (Fig. 1). The 18O-labeling approach was further applied to leaf disks (e.g. Tourneux and Peltier, 1995), whole excised leaves (e.g. Volk and Jackson, 1972), and entire plants (Gerbaud and André, 1980), illuminating the fate of O2 in vivo. Figure 1. Open in new tabDownload slide Simple representation of the reactions that can be involved in gross O2 production and uptake of a photosynthesizing cell, showing how labeled 18O water results in the production of 18O2 in the approach developed by Gauthier et al. (2018). In the case of reactions within the peroxisome and mitochondria, this only represents net O2 consumption, i.e. there is both uptake and release occurring. PSII, Photosystem II; PSI, Photosystem I; Fd, Ferredoxin; M, Mehler reaction; PCR; photosynthetic carbon reduction; PCO, photosynthetic carbon oxidation; PGA, 3-phosphoglycerate; P-Glyc, phosphoglycolate; Glyox, glyoxylate; OAA, oxaloacetate; Mal, malate. Figure 1. Open in new tabDownload slide Simple representation of the reactions that can be involved in gross O2 production and uptake of a photosynthesizing cell, showing how labeled 18O water results in the production of 18O2 in the approach developed by Gauthier et al. (2018). In the case of reactions within the peroxisome and mitochondria, this only represents net O2 consumption, i.e. there is both uptake and release occurring. PSII, Photosystem II; PSI, Photosystem I; Fd, Ferredoxin; M, Mehler reaction; PCR; photosynthetic carbon reduction; PCO, photosynthetic carbon oxidation; PGA, 3-phosphoglycerate; P-Glyc, phosphoglycolate; Glyox, glyoxylate; OAA, oxaloacetate; Mal, malate. The limitation of closed gas exchange systems is that measurements can only be undertaken for short periods of time (seconds to minutes) before the CO2 concentration is depleted. Consequently, CO2:O2 is not constant, which changes the relative rates of carboxylation and oxygenation so that estimates of GOP and O2 uptake will be inaccurate. This limitation was overcome in the mass spectrometry approach by replacing CO2 consumed through periodic influx of CO2 into the chamber, allowing for steady-state quantification and extending the ability to measure O2 fluxes under a range of conditions and physiological states (Canvin et al., 1980). At the same time, advances were being made in the use of chlorophyll fluorescence, which provides information on PSII quantum yield (Baker, 2008). Genty et al. (1989) provided the empirical link between fluorescence and electron transport rate, replacing the need to directly measure O2 evolution. Chlorophyll fluorescence is now one of the most popular techniques in plant physiology because of its ease of use and relatively low cost. This has been aided by the capacity to multiplex fluorescence measurements with H2O and CO2 gas exchange in portable, commercially available instruments, opening up the possibility of measuring plant function outside of the laboratory. Consequently, in vivo measurements of O2 fluxes have substantially declined over the last 20 years. In this issue of Plant Physiology, Gauthier et al. (2018) remind us why it is so important to return our attention to O2, providing us with a new, elegant open-path system to measure O2 fluxes. Their method is a “reverse” isotopic approach, involving 18O-labeling of leaf water rather than the air so that the isotopic composition of O2 that is evolved during water splitting has a signature very different to that of ambient O2 (Fig. 1). The use of considerable 18O enrichment is imperative since the contribution of NOP in a background of 21% O2 is likely to be in the order of 0.05% (e.g. 100 μmol mol−1 NOP/210,000 μmol mol−1 ambient O2), making it difficult ordinarily to accurately detect a change in δ18O of O2 associated with NOP in the air surrounding the leaf. The method remains highly technical, requiring the use of three high-precision instruments. The isotopic composition and concentration of CO2 and H2O vapor are measured by laser spectroscopy, and the δ18O2 and δO2/N2 (to estimate O2 concentration) by mass spectrometry. A custom-made chamber is also required to house the excised leaf and its 18O-labeled water source, which helps to prevent leaks across the gaskets from around the petiole. Importantly, the open gas exchange system improves the ability to achieve steady-state measurements, and labeling water versus the use of pure 18O2 gas solves the affordability issue, which has greatly limited the adoption of open systems. While chlorophyll fluorescence has become the popular option for measuring electron transport rate, it is not without assumptions. For example, it is frequently assumed that leaves absorb 84% of incident photons and that 50% of these photons are absorbed by PSII; however, this may not always be the case (Baker, 2008). This may lead to an overestimate of electron transport rate when computed from fluorescence compared with measurements of GOP. Furthermore, accurate determination of JA is particularly relevant for the estimation of mesophyll conductance, which was one application highlighted by Gauthier et al. (2018). The Mehler-peroxidase reactions, which have been shown to range from 0% to 30% (Driever and Baker, 2011), would lead to an overestimate of electron fluxes associated with the photosynthetic carbon reduction/oxygenation cycles in both methods. However, the advantage of the isotope labeling approach is that the contribution of the Mehler reaction to gross O2 production can be quantified by coupling measurements of GOP with NOP (e.g. Furbank et al., 1982; see Fig. 1). Now that we have a renewed ability to measure O2 fluxes, these assumptions should not be ignored. Besides understanding the trade-off between efficiency and photoprotection for improved agricultural production (Murchie and Niyogi, 2011), the different electron fates have important implications for understanding global O2 fluxes. Notably, O2 uptake associated with photorespiration, mitochondrial respiration, and the Mehler-peroxidase reactions have different isotope fractionation factors (Guy et al., 1993) so that the quantification of individual pathway fluxes is needed to constrain estimates of global primary production from δ18O information (Welp et al., 2011). It is high time we revisited the measurement of O2 fluxes, and the new method developed by Gauthier et al. (2018) provides us with the necessary capacity to do so. LITERATURE CITED Asada K ( 1999 ) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons . Annu Rev Plant Physiol Plant Mol Biol 50 : 601 – 639 Google Scholar Crossref Search ADS PubMed WorldCat Badger MR ( 1985 ) Photosynthetic oxygen exchange . Annu Rev Plant Physiol 36 : 27 – 53 Google Scholar Crossref Search ADS WorldCat Baker NR ( 2008 ) Chlorophyll fluorescence: a probe of photosynthesis in vivo . Annu Rev Plant Biol 59 : 89 – 113 Google Scholar Crossref Search ADS PubMed WorldCat Bloom AJ , Caldwell RM, Finazzo J, Warner RL, Weissbart J ( 1989 ) Oxygen and carbon dioxide fluxes from barley shoots depend on nitrate assimilation . Plant Physiol 91 : 352 – 356 Google Scholar Crossref Search ADS PubMed WorldCat Canvin DT , Berry JA, Badger MR, Fock H, Osmond CB ( 1980 ) Oxygen exchange in leaves in the light . Plant Physiol 66 : 302 – 307 Google Scholar Crossref Search ADS PubMed WorldCat Driever SM , Baker NR ( 2011 ) The water-water cycle in leaves is not a major alternative electron sink for dissipation of excess excitation energy when CO2 assimilation is restricted . Plant Cell Environ 34 : 837 – 846 Google Scholar Crossref Search ADS PubMed WorldCat Furbank RT , Badger MR, Osmond CB ( 1982 ) Photosynthetic oxygen exchange in isolated cells and chloroplasts of C3 plants . Plant Physiol 70 : 927 – 931 Google Scholar Crossref Search ADS PubMed WorldCat Gauthier PPG , Battle MO, Griffin KL, Bender ML ( 2018 ) Measurement of gross photosynthesis, respiration in the light, and mesophyll conductance using H2 18O labeling . Plant Physiol 177 : 62 – 74 Google Scholar Crossref Search ADS PubMed WorldCat Genty B , Briantais J-M, Baker NR ( 1989 ) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence . Biochim Biophys Acta 990 : 87 – 92 Google Scholar Crossref Search ADS WorldCat Gerbaud A , André M ( 1980 ) Effect of CO2, O2, and light on photosynthesis and photorespiration in wheat . Plant Physiol 66 : 1032 – 1036 Google Scholar Crossref Search ADS PubMed WorldCat Guy RD , Fogel ML, Berry JA ( 1993 ) Photosynthetic fractionation of the stable isotopes of oxygen and carbon . Plant Physiol 101 : 37 – 47 Google Scholar Crossref Search ADS PubMed WorldCat Hill R ( 1937 ) Oxygen evolved by isolated chloroplasts . Nature 139 : 881 – 882 Google Scholar Crossref Search ADS WorldCat Mehler AH , Brown AH ( 1952 ) Studies on reactions of illuminated chloroplasts. III. Simultaneous photoproduction and consumption of oxygen studied with oxygen isotopes . Arch Biochem Biophys 38 : 365 – 370 Google Scholar Crossref Search ADS PubMed WorldCat Morales A , Yin X, Harbinson J, Driever SM, Molenaar J, Kramer DM, Struik PC ( 2018 ) In silico analysis of the regulation of the photosynthetic electron transport chain in C3 plants . Plant Physiol 176 : 1247 – 1261 Google Scholar Crossref Search ADS PubMed WorldCat Murchie EH , Niyogi KK ( 2011 ) Manipulation of photoprotection to improve plant photosynthesis . 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J Exp Bot 59 : 1647 – 1661 Google Scholar Crossref Search ADS PubMed WorldCat Stumpf PK , Bové JM, Goffeau A ( 1963 ) Fat metabolism in higher plants. XX. Relation of fatty acid synthesis and photophosphorylation in lettuce chloroplast . Biochim Biophys Acta 70 : 260 – 270 Google Scholar Crossref Search ADS PubMed WorldCat Tcherkez G , Gauthier P, Buckley TN, Busch FA, Barbour MM, Bruhn D, Heskel MA, Gong XY, Crous KY, Griffin K, et al. ( 2017 ) Leaf day respiration: low CO2 flux but high significance for metabolism and carbon balance . New Phytol 216 : 986 – 1001 Google Scholar Crossref Search ADS PubMed WorldCat Tourneux C , Peltier G ( 1995 ) Effect of water deficit on photosynthetic oxygen exchange measured using 18O2 and mass spectrometry in Solanum tuberosum L. leaf discs . Planta 195 : 570 – 577 Google Scholar Crossref Search ADS WorldCat Volk RJ , Jackson WA ( 1972 ) Photorespiratory phenomena in maize: oxygen uptake, isotope discrimination, and carbon dioxide efflux . Plant Physiol 49 : 218 – 223 Google Scholar Crossref Search ADS PubMed WorldCat Welp LR , Keeling RF, Meijer HAJ, Bollenbacher AF, Piper SC, Yoshimura K, Francey RJ, Allison CE, Wahlen M ( 2011 ) Interannual variability in the oxygen isotopes of atmospheric CO2 driven by El Niño . Nature 477 : 579 – 582 Google Scholar Crossref Search ADS PubMed WorldCat Author notes 1 Address correspondence to [email protected]. www.plantphysiol.org/cgi/doi/10.1104/pp.18.00344 © 2018 American Society of Plant Biologists. All Rights Reserved. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model)
Ivanov, Rumen; Robinson, David G.
doi: 10.1104/pp.18.00322pmid: 29720533
Our knowledge of vacuole biogenesis and the transport of proteins to the vacuole has advanced consistently over the last 30 years. In meristematic cells, the tonoplast appears to develop directly out of the endoplasmic reticulum (Viotti et al., 2013). Once it is established as a functioning organelle, tonoplast proteins reach the vacuole in one of two main ways. A bulk flow process for tonoplast protein delivery originates at the trans-Golgi network (TGN) and proceeds through maturation into a multivesicular endosome that ultimately fuses with the vacuole (Brillada and Rojas-Pierce, 2017). Alternatively, vesicle transport from the TGN targets tonoplast proteins to this endosomal compartment. Studies using adaptor protein complex (AP) mutants indicate that the transport vectors in this latter case may be clathrin-coated vesicles. There is also some evidence to suggest that some of the TGN-derived vesicles (AP-4-positive, but lacking clathrin) might bypass the endosomes (Rosquete et al., 2018). In accordance with this notion, it has been recently demonstrated that two different tethering complexes (CORVET and HOPS) exist for fusion with the tonoplast in Arabidopsis (Arabidopsis thaliana; Takemoto et al., 2018). Thus, transport to the vacuole would appear to be more complicated than was previously thought. Plant cells maintain vacuoles for long timespans, and they continuously receive new membrane in the form of fusing vesicles or endosomes. Since vacuoles cannot enlarge indefinitely, they must somehow compensate by removing excess membrane proteins and lipids. This may occur by way of microautophagy, sometimes leading to “bulb” formation (Han et al., 2015; Maîtrejean and Vitale, 2012). Preliminary evidence indicating that bulb formation might be a selective rather than a bulk degradative process has been published (Saito et al., 2002). A possible selective removal of proteins from the tonoplast is also indirectly implied in the recent publication of Feeney et al. (2018), which documents the delivery of typical tonoplast proteins from the storage vacuole to lytic vacuoles during vacuole remodeling in Arabidopsis leaves. Exactly how such a transfer could occur is unclear, although vesicle-mediated retrograde transport might be inferred from the presence of a large set of endomembrane trafficking components in the vacuolar proteome, including small GTPases of the Arf and Rab7 classes (Carter et al., 2004). Remarkable new insights into how membrane proteins may be removed from the tonoplast have recently been provided by the group of Scott Emr working on the yeast vacuole. In one publication, Suzuki and Emr (2018) investigated the retrieval of the type I membrane protein Atg27 from the yeast vacuole membrane. Normally, this protein functions together with Atg9 in the formation of microvesicles that are required for autophagosome formation. However, by virtue of a Tyr-based motif in its cytoplasmic C-tail, it interacts with the AP3 adaptor complex and also gets transported directly from the Golgi to the vacuole. By generating yeast mutants with impaired retromer (vps35Ɗ) or sorting nexin (snx4Ɗ) function, Suzuki and Emr were able to show that retrograde transport of Atg27 from the vacuole to the Golgi occurs in two steps: First, Atg27 is incorporated into a vacuole-to-endosome transport vesicle formed by the attachment of dimers of Snx4 and Snx41/42 via their PHOX homology (PX) and Bin/Amphiphysin/Rvs (BAR) domains on the vacuole membrane; second, a classical retromer-mediated transport of Atg27 from the endosome to the Golgi occurs. A direct interaction between Atg27 and Snx4 was demonstrated by coimmunoprecipitation, with R224, S227, F231, and I236 being determined as the responsible residues in the C-tail of Atg27. Thus, as with the retrograde transport of mannosyl 6-phosphate receptors from maturing endosomes in mammalian cells (for a discussion, see Robinson, 2018), it is once again the sorting nexins that have been demonstrated to be the crucial coat proteins for vesicle transport. In another landmark article, Zhu et al. (2017) followed the degradation of the Lys transporter Ypq1. This degradation is initiated upon Lys withdrawal from the growth medium and causes a type E3 ubiquitin ligase, RSP5, to be recruited to the surface of the yeast vacuole. After being ubiquitinated, Ypq1 is sorted into a microvesicle and released into the vacuole lumen. Based on multiple genetic approaches, Zhu et al. (2017) concluded that the ESCRT (endosomal sorting complexes required for transport) complexes required for this internalization process are located directly on the vacuole membrane, in addition to those on endosomes as previously described (Henne et al., 2011). At present, it is unclear how evolutionary conserved the Snx4 retrieval and vacuole-based ESCRT internalization mechanisms are, but we feel that they are unlikely to be restricted to yeast. Might they operate in plants? Unfortunately, Atg27 (YJL178C) has no homologs in the green lineage (Michaeli et al., 2016), while homologs of Snx41p (YDR425W) and Snx42p (YDL113C) may exist in green algae but not in plants. However, the situation with Snx4p (YJL036W) is different. BLAST searches reveal that the known BAR-domain SNX proteins of plants are distantly related to both Vps5p (YOR069W) and Snx4p, and therefore might have the capacity to perform recycling of tonoplast proteins. Two considerations must be taken into account. On the one hand, SNX1 (At5g06140) and SNX2 (At5g58440 and At5g07120) proteins mainly localize to the TGN (Stierhof et al., 2013); thus, their involvement at the tonoplast is not directly evident. On the other hand, one cannot exclude a potential short-lived SNX1/SNX2 tonoplast association and a rapid vesicle release that remains unnoticed in localization studies. Notably, Snx4 is also not obviously localized to the yeast vacuolar membrane (Suzuki and Emr, 2018). In support of a potential SNX1/SNX2 involvement is the fact that PI3P, the lipid targeted by the PX domain of SNX proteins, has been detected at the tonoplast (Simon et al., 2014). Moreover, SNX1 and SNX2 have been shown form homo- and heterodimers in vivo. Therefore, the absence of plant Snx41/42 homologs and the fact that the three Arabidopsis non-BAR-domain SNXs might not participate in membrane tubulation (for review, see Heucken and Ivanov, 2018) suggest that there might be no requirement for additional partners as in the case of Snx4p. However, before this can be addressed experimentally, we will first need to identify retrograde cargo proteins in plants. Except for ESCRT complex 0, which is absent in plants, all of the other ESCRT complexes have been identified and functionally characterized in relation to the vacuolar degradation of ubiquitinated plant plasma membrane proteins (Nagel et al., 2017). However, and as in other eukaryotes, the ESCRT complexes in plants are located on endosomal membranes. To our knowledge, there is no publication showing the presence of ESCRT proteins at the tonoplast or that ubiquitination of specific proteins occurs at this location. For the moment, it would seem that this particular mechanism for tonoplast protein turnover is peculiar to yeast. LITERATURE CITED Brillada C , Rojas-Pierce M ( 2017 ) Vacuolar traffivcking and biogenesis: a maturation in the field . Curr Opin Plant Biol 40 : 77 – 81 Google Scholar Crossref Search ADS PubMed WorldCat Carter C , Pan S, Zouhar J, Avila EL, Girke T, Raikhel NV ( 2004 ) The vegetative vacuole proteome of Arabidopsis thaliana reveals predicted and unexpected proteins . Plant Cell 16 : 3285 – 3303 Google Scholar Crossref Search ADS PubMed WorldCat Feeney M , Kittelmann M, Menassa R, Hawes C, Frigerio L ( 2018 ) Protein storage vacuoles originate by remodelling of preexisting vacuoles in Arabidopsis thaliana . Plant Physiol 177 : 241 – 254 Google Scholar Crossref Search ADS PubMed WorldCat Han SW , Alonso JM, Rojas-Pierce M ( 2015 ) Regulator of bulb biogenesis 1 (RBB1) is involved in vacuole bulb formation in Arabidopsis . PLoS One 10 : e0125621 Google Scholar Crossref Search ADS PubMed WorldCat Henne WM , Buchkovich NJ, Emr SD ( 2011 ) The ESCRT Pathway . Dev Cell 21 : 77 – 91 Google Scholar Crossref Search ADS PubMed WorldCat Heucken N , Ivanov R ( 2018 ) The retromer, sorting nexins and the plant endomembrane protein trafficking . J Cell Sci 131 : jcs203695 Google Scholar Crossref Search ADS PubMed WorldCat Michaeli S , Galili G, Genschik P, Fernie AR, Avin-Wittenberg T ( 2016 ) Autophagy in plants: What’s new on the menu? Trends Plant Sci 21 : 134 – 144 Google Scholar Crossref Search ADS PubMed WorldCat Maîtrejean M , Vitale A ( 2012 ) How are tonoplast proteins degraded? 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Plant J 77 : 322 – 337 Google Scholar Crossref Search ADS PubMed WorldCat Stierhof YD , Viotti C, Scheuring D, Sturm S, Robinson DG ( 2013 ) Sorting nexins 1 and 2a locate mainly to the TGN . Protoplasma 250 : 235 – 240 Google Scholar Crossref Search ADS PubMed WorldCat Suzuki SW , Emr SD ( 2018 ) Membrane protein recycling from the vacuole/lysosome membrane . J Cell Biol pii : jcb.201709162 Google Scholar OpenURL Placeholder Text WorldCat Viotti C , Krüger F, Krebs M, Neubert C, Fink F, Lupanga U, Scheuring D, Boutté Y, Frescattada-Rosa M, Wolfenstetter S, et al. ( 2013 ) The endoplasmic reticulum is the main membrane source for biogenesis of the lytic vacuole in Arabidopsis . Plant Cell 25 : 3434 – 3449 Google Scholar Crossref Search ADS PubMed WorldCat Zhu L , Jorgensen J, Li M, Chuang Y-S, Emr SD ( 2017 ) ESCRTs function directly on the lysosome membrane to downregulate ubiquitinated lysosomal membrane proteins . eLife 6 : e26403 Google Scholar Crossref Search ADS PubMed WorldCat Author notes 1 Address correspondence to [email protected]. www.plantphysiol.org/cgi/doi/10.1104/pp.18.00322 © 2018 American Society of Plant Biologists. All Rights Reserved. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model)
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