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Downloaded from https://academic.oup.com/jxb/article/69/11/2753/4999765 by DeepDyve user on 20 July 2022 Journal of Experimental Botany, Vol. 69, No. 11 pp. 2753–2758, 2018 doi:10.1093/jxb/ery157 Special Issue Editorial Received 19 April 2018; Editorial decision ; Accepted Molecular mechanisms controlling plant growth during abiotic stress Mechanisms that protect against abiotic stress are essen- be modified to increase nutrient uptake, while severe nutrient tial for plant survival, yet their activation generally comes at limitation may lead to complete growth arrest. Roots are essen- the expense of growth and productivity, which is particularly tial for water and nutrient uptake, but also serve a variety of serious for agriculture. Recent developments in molecular other functions, such as forming symbioses with other micro- genetics have contributed substantially to our understand- organisms in the rhizosphere, anchoring the plant to the soil, ing of the basis of abiotic stress defense. Progress has also and acting as storage organs. Consequently, roots are essential been made towards understanding how plants control the for optimal plant productivity. Many abiotic stresses are first switch between growth and defense, especially with regard encountered at the root level often leading to changes in root bio- to timing and mechanism. This ongoing research is critical mass and architecture. For example, primary root growth stops for the improvement of crop plants. when Arabidopsis seedlings are transferred to media without phosphate. This growth arrest is the consequence of a signaling Cell proliferation and growth require nutrients, biosynthetic pathway mediated by STOP1, ALMT1 and LPR2 (Balzergue capacity and energy. Restricting any one of these factors will et al., 2017). Strikingly, knockout mutants of these genes lose lead to arrested growth and eventually death. To ensure their the root growth arrest response on phosphate removal, indicat- survival it is therefore necessary for living organisms to antici- ing that root growth arrest is not a result of metabolic limitation. pate changes in the environment that might affect their capacity Importantly, when roots encounter changes in environmen- to grow, and then to mount an effective acclimatory response. tal conditions they will change growth direction in order to This is particularly important in plants, which are typically optimize plant survival. Such directional changes in response immobile and encounter large fluctuations in temperature, light, to stimuli (tropisms) include where roots sense the soil water humidity and nutrient availability in their natural environment content and grow towards water to avoid dry soil by either (see Box 1). Environmental stress causes massive agricultural changing direction or halting growth. Despite water sens- losses (Godfray et al., 2010; Cramer et al., 2011), and improving ing being the subject of very early plant physiology studies, crop tolerance is a major goal of crop improvement programs. until recently the mechanisms of this growth response were However, tolerance can come with trade-offs; for example, it has essentially unknown. Some genes required for hydrotropism, long been known that stress-tolerant plants have lower growth such as MIZ1 and MIZ2/GNOM, have now been identified rates and productivity (reviewed by Chapin, 1991). Therefore, (Kobayashi et al., 2007; Miyazawa et al., 2008), and a role iden- in addition to understanding the basis of tolerance, it is also tified for the action of plant hormones such as auxin, ABA important to understand the trade-offs between tolerance and and cytokinin (Moriwaki et al., 2011; Moriwaki et al., 2012; growth/productivity for effective crop improvement. Saucedo et al., 2012). More recently the site of water perception The impact of abiotic stress on plant performance is and growth control was localized to the root cortex (Dietrich being explored at many different levels, in a great variety of et al., 2017), and progress and perspectives in the active hydro- model and crop species, and includes metabolic/physiological tropism field are reviewed in this issue by Dietrich (2018). responses, molecular signaling pathways, ecophysiology and The review highlights the many outstanding questions that crop breeding studies. In addition, abiotic stress is not a sin- remain regarding the signaling pathways involved in hydro- gle entity but rather comprises all the environmental pertur- tropism, as well as the need for further research in this area. bations that plants may encounter in nature. Consequently, Indeed, it has been suggested that the genes involved in hydro- the literature on abiotic stress responses is vast, and covers tropism could be important targets for crop improvement by very diverse research areas. Here, we focus on a selection of enhancing drought avoidance. A recent demonstration that recent advances made in our understanding of the molecular a robust hydrotropic response leads to better growth under mechanisms that control plant growth during abiotic stress. drought and partial lateral irrigation in different maize culti- vars strongly supports this notion (Eapen et al., 2017). Nutrient and water limitation: the root perspective Growing pains: abiotic stress Nutrient limitation has drastic effects on plant growth and devel- Abiotic stress leads to altered biosynthetic capacity and opment. Under mild nutrient deprivation plant architecture may nutrient acquisition that can inhibit plant growth. This © The Author(s) 2018. Published by Oxford University Press on behalf of the Society for Experimental Biology. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. Downloaded from https://academic.oup.com/jxb/article/69/11/2753/4999765 by DeepDyve user on 20 July 2022 2754 | Special Issue Editorial Box 1. Plant growth during abiotic stress Carbohydrate resources and energy generated by photosynthesis (circular arrows) are allo- cated to growth and reproduction. Nutrient limitation or abiotic stress exposure can limit growth and also lead to over-excitation of the photosynthetic electron transport chain and the production of potentially damaging ROS. Timely perception of stress leads to the modulation of plant growth and the activation of defense and acclimation pathways that can act within specific plant organs, or across the entire plant. Key players in the control of plant growth dur - ing abiotic stress are shown. Chloro, chloroplast; GA, gibberellins; BR, brassinosteroids; SA, salicylic acid; ET, ethylene. phenomenon is documented in many research papers on that may integrate both processes. For example, the molecular model and crop species alike. Consequently, research into mechanisms that control leaf growth under mild drought con- understanding the responses to abiotic stress has moved to ditions link both growth and transcriptional responses to the the forefront over the past decade, leading to the discovery of circadian clock. Specifically, two ETHYLENE RESPONSE several signaling pathways involving a large number of genes, FACTORS (ERFs), ERF2 and ERF8, were found to affect proteins and post-translational modifications. These include leaf growth under drought and well-watered conditions 2+ the MAPK, ABF/bZIP, Ca -CBL-CIPK and CBF/DREB (Dubois et al., 2017). Interestingly, in the same study the spe- signaling pathways, which employ numerous stress-respon- cific up-regulation of three genes encoding growth-repressing sive transcription factors to orchestrate the downstream DELLA proteins was observed during the early drought responses required to mount an effective defense to specific response (Dubois et al., 2017). DELLA proteins have previ- abiotic challenges (Wang et al., 2016; Zhu, 2016). ously been shown to accumulate under nutrient deficiency, low Importantly, these molecular signaling pathways can temperature treatment and in response to salt stress (Achard anticipate the effects of abiotic stress to regulate the balance et al., 2008; Xie et al., 2016). DELLAs promote stress-induc- between growth and acclimation. More recently, efforts into ible anthocyanin biosynthesis through the formation of a understanding how plant growth is regulated under stress con- JAZ–DELLA–MYBL2 complex (Xie et al., 2016) and can ditions has resulted in the identification of candidate genes also promote ROS scavenging to delay cell death (Achard Downloaded from https://academic.oup.com/jxb/article/69/11/2753/4999765 by DeepDyve user on 20 July 2022 Special Issue Editorial | 2755 et al., 2008). Stress-induced anthocyanin accumulation is sig- study has shown that TOR can also phosphorylate the ABA nificantly inhibited in della mutants (Xie et al., 2016), while receptor PYL to prevent activation of the ABA-signaling under salt stress della quadruple mutants produce significantly effector kinase SnRK2 in non-stressed plants (Wang et al., more ROS than the wild type (Achard et al., 2008). DELLA 2018). In turn, under stress conditions, ABA is able to activate proteins therefore promote survival under abiotic stress con- SnRK2, which then phosphorylates a member of the TOR ditions. Interestingly, reduced anthocyanin accumulation in complex RAPTOR, which triggers complex dissociation and response to high light was also observed in the ascorbate-defi- TOR inactivation. This antagonistic signaling loop is an excel- cient mutants vtc2-1 and vtc2-4, yet both vtc mutants experi- lent example of how plants are able make the decision between enced identical levels of photodamage compared to wild type. growth and stress acclimation. Interestingly, both TOR and This suggests that ascorbate is not essential for photoprotec- SnRK1 have been implicated in the regulation of chloroplast tion during high light, but intriguingly is required for the accu- function (Dong et al., 2015; Dobrenel et al., 2016; Nukarinen mulation of rosette biomass under low-light and short-day et al., 2016; Sun et al., 2016; Imamura et al., 2018). conditions (Plumb et al., 2018). Signal transduction pathways mediated by phytohormones can play a critical role in abiotic stress responses (reviewed It all comes down to light: chloroplasts by Verma et al., 2016). For example, ABA plays a key role in at the centre of stress perception and stress responses, while auxin plays a major role in promot- regulation ing plant growth. The interplay between phytohormones is Chloroplasts are one of the powerhouses for plant productiv- therefore an important mechanism for balancing growth and ity, but photosynthesis is highly sensitive to light, CO levels, stress resistance. Brassinosteroids are a class of plant steroid 2 and plant metabolic capacity. Excess light, or limitation in CO hormones that promote growth via the activation of the tran- 2 supply or metabolic capacity, during abiotic stress exposure scription factors BZR1 and BES1. A recent study has shown rapidly leads to over-excitation and reduction of the photo- that drought stress represses the brassinosteroid signaling synthetic electron transport chain. Over-excitation is poten- pathway, and thereby growth, by promoting the degradation tially highly dangerous for the plant because it can lead to the of BES1 via ubiquitination and selective autophagy (Nolan production of ROS such as O and H O that can irreversibly et al., 2017). This example highlights the importance that 2 2 2 damage proteins, membranes and DNA. However, changes in plant hormones can have as major integrators of environ- chloroplast redox status during overexcitation act as a signal mental stress and nutrient status. that leads to the rapid activation of energy-dissipating mech- anisms, changes in chloroplast genome expression, and over the longer term to changes in chloroplast protein compos- Hunger games: nutrient and energy ition and position to allow acclimation. Importantly, chloro- signaling plast stress triggers acclimation at the cellular level as well Over recent years it has become clear that plants integrate as the organellar level, and as the severity of stress increases energy/nutrient status to regulate growth and stress responses can lead to growth inhibition and eventually programmed cell using antagonistic signaling pathways mediated by the evo- death (Laloi and Havaux, 2015). The majority of chloroplast lutionarily conserved protein kinases TOR (TARGET OF proteins are encoded in the nuclear genome. Remodelling of RAPAMYCIN) and SnRK1 (Snf1-RELATED PROTEIN the chloroplast proteome during abiotic stress acclimation KINASE1) (Robaglia et al., 2012; Broeckx et al., 2016; therefore requires signaling from the nucleus to the chloro- Baena-González and Hanson, 2017). The central role of these plast (anterograde signaling), and from the chloroplast to kinases in energy metabolism is underlined by their wide con- the nucleus (retrograde signaling). An overview of chloro- servation in the eukaryotes, from yeast and animals to plants plast proteome remodelling, with a focus on stress-regulated and fungi (Roustan et al., 2016). SnRK1 is activated by low- import of proteins, nuclear control of the chloroplast genome energy conditions, such as those that may occur during stress and protein turnover within the chloroplast is reviewed in this exposure, to trigger catabolism and repress growth. Notably, special issue (Watson et al., 2018). Stress-induced retrograde SnRK1 can be activated by the inhibition of photosynthesis signaling from the chloroplast is also considered from a dif- with the inhibitor DCMU, and can be inhibited by the add- ferent perspective by Crawford et al. (2018). In particular, ition of sugars. SnRK1 directly targets metabolic and regula- these authors discuss how the stress-induced down-regula- tory enzymes in the cytosol, and also affects gene expression tion of photosynthesis and respiration in the mitochondria via the phosphorylation of transcription factors such as can lead to a reduction in the supply of energy available for BZIP63 (Mair et al., 2015; Nukarinen et al., 2016). In con- cellular stress acclimation. They propose a new hypothesis trast, TOR promotes cell growth and proliferation in response for the integration of different organellar retrograde sig- to light, sugars, and growth-promoting hormones through nals in the nucleus to coordinate transcriptional responses the phosphorylation of target proteins (recently reviewed by that regulate the allocation of energy to either growth or Schepetilnikov and Ryabova, 2018). Over the past 10 years a stress acclimation. Notably, and in relation to this hypoth- growing number of TORC client proteins and downstream esis, recent work indicates that chloroplast-generated H O 2 2 effectors have been firmly identified in plants, including the S6 acts as a retrograde signal that is directly transferred from kinase, E2F, and the brassinosteroid pathway. A very recent the chloroplast to the nucleus, avoiding the cytosol, to drive Downloaded from https://academic.oup.com/jxb/article/69/11/2753/4999765 by DeepDyve user on 20 July 2022 2756 | Special Issue Editorial a transcriptional response (Exposito-Rodriguez et al., 2017). species may lead to the rapid development of new strategies Stress can also lead to transcriptional reprogramming within for conferring stress resistance to crop plants without penal- the chloroplast, and the signaling nucleotides guanosine ties. The basis of C24 stress resistance is likely to be complex tetra- and penta-phosphate [or (p)ppGpp] potentially play and multigenic. However, even the overexpression of a single a major role (Field, 2018). Indeed, (p)ppGpp is known to transcription factor gene, such as Heat Shock Transcription accumulate in response to a wide range of different abi- FactorA1b, can lead to penalty-less increases in abiotic stress otic stresses, and both in vitro and in vivo studies show that resistance (Bechtold et al., 2013), and other positive examples (p)ppGpp accumulation inhibits chloroplast transcription utilizing single-gene manipulations are highlighted in Bechtold and affects chloroplast function. These findings and other et al. (2018). Intriguingly, the molecular basis of HSFA1b recent advances in our understanding of (p)ppGpp metabo- stress resistance appears to be in its ability to regulate the lism in plants and algae are reviewed by Field (2018). expression of a large hierarchical network of stress and devel- While light plays an obvious role in the production of pho- opment genes (Albihlal et al., 2018), suggesting the HSFA1b tosynthates and energy, a perhaps less intuitive role is in the could be a master regulator of the switch between growth and regulation of biomass partitioning and plant architecture in abiotic stress defenses. It will also be fascinating to discover response to resource availability, which can occur in a phyto- how such ‘penalty-less’ improvements in stress tolerance are chrome B (PHYB) dependent manner (Arsovski et al., 2018). able to bypass SnRK1/TOR-mediated growth control. The function of phytochromes as regulators of carbon supply, metabolic status and biomass production has been recently proposed (Yang et al., 2016), and together with the PHYB- Future directions and light-dependent development of stomata (Casson and Research into plant responses to environmental stress and Hetherington, 2014) emphasizes the close connection between the application of this knowledge to improve productiv- light perception and photosynthetic metabolism beyond ity under non-optimal growing conditions is becoming ever photosynthetic electron transport. PHYB was also recently more important. Over recent years dramatic progress has shown to act as a temperature sensor in plants. PHYB activ- been made, and the molecular mechanisms for many stress ity decreases with increasing temperature in a light-depend- response pathways revealed. Identification of the cellular ent manner (Legris et al., 2016), to allow the optimization of hubs that integrate these diverse stress acclimation mecha- growth and biomass production under different environmen- nisms, and the regulatory logic behind the plant’s decision- tal conditions. Furthermore, PHYB has been demonstrated making processes, are now emerging themes in the field. Over to uncouple growth and defense pathways through the relief coming years further research in these directions has the of transcriptional repression, thereby providing a direct link potential to lead to a more unified view of plant growth and between light, plant growth and defense signaling pathways abiotic stress resistance that could be applied for the rational (Campos et al., 2016; Cerrudo et al., 2017). improvement of crop plants. The trade-off between growth and defense: Acknowledgements a balancing act? This editorial covers a topic that was part of a stimulating two-day session held at the Society for Experimental Biology meeting in Gothenburg, Sweden In light of the diverse molecular mechanisms that regulate in 2017, and which forms the basis for the reviews and research articles in this growth and abiotic stress acclimation the question arises as special issue. to whether the induction of stress tolerance always leads to Keywords: Abiotic stress, Arabidopsis, ascorbate, chloroplast proteome, growth penalties, or whether we can get something for noth- heat shock transcription factorA1b, (p)ppGpp, phytochrome, plant growth, ing. It is commonly thought that constitutive stress tolerance productivity, retrograde signals. comes at a cost to the organism, and this has been extensively reviewed for disease resistance traits (Heil, 2014; Heil and 1, 2, Baldwin, 2002). Early examples of engineered constitutive abi- Ulrike Bechtold * and Benjamin Field * otic stress tolerances have often led to growth penalties under School of Biological Sciences, University of Essex, benign growth conditions (Kasuga et al., 1999; Haake et al., Colchester CO4 3SQ, UK 2002). Another example is the Physcomitrella patens ppabi1a/b Aix Marseille Univ, CEA, CNRS, UMR7265 BVME, double mutant, where ABA signaling is constitutively active, 13009 Marseille, France which is stress resistant but also shows very severe growth * Correspondence: firstname.lastname@example.org or email@example.com defects (Komatsu et al., 2013). However, there are now many indications that the cost need not always be so high. C24, an Arabidopsis ecotype from the Iberian peninsula, is resistant to ROS, heat and drought stress yet shows similar productivity References to less-tolerant ecotypes. 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Journal of Experimental Botany – Oxford University Press
Published: May 19, 2018
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