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Drought priming-induced heat tolerance: Metabolic pathways and molecular mechanisms
CHAPTER 9
Drought priming-induced heat tolerance: Metabolic pathways and molecular mechanisms Xiaxiang Zhanga,b, Bingru Huangb a
College of Agro-grassland Science, Nanjing Agricultural University, Nanjing, People’s Republic of China Department of Plant Biology and Pathology, Rutgers University, New Brunswick, NJ, United States
b
9.1 Introduction Heat stress is a detrimental abiotic stress limiting plant growth and sustainable agriculture worldwide.1 With global climate change, the Earth’s surface temperature is expected to increase considerably in the coming years and climate models have predicted a potentiality for heat waves to become more severe and occur more frequently.2,3 Elevated temperature can accentuate the negative impact of heat damages in various physiological and metabolic processes, including carbon metabolism, nitrogen metabolism, nutrient uptake, water uptake, and hormone metabolism.1,4 Identifying approaches for improving heat tolerance is critically important for maintaining plant productivity in warm climatic regions. Priming, by preexposure of plants to an eliciting factor, such as chemicals, biotic, or abiotic stress, could trigger the “stress memory” of plants and enhance plant tolerance to future stresses.5,6 Among abiotic stress factors, drought priming-induced drought or heat tolerance and heat priming-induced heat tolerance have been studied in various plant species, such as wheat (Triticum aestivum), barley (Hordeum vulgare), and Arabidopsis (Arabidopsis thaliana).7 Recently, it has been proven that pretreatment by drought is a positive and effective strategy for improving plant tolerance to future stresses.5,8 Primed plants display faster and stronger activation of various defense responses at morphological, physiological, biochemical, and molecular levels.5 To counter the effects of heat stress, plants respond to changes by reprogramming their transcriptome, proteome, and metabolome during drought priming and adapt to future periods of heat stress. The development of acquired heat tolerance by drought priming has been associated with changes in various physiological and metabolic processes, as well as molecular factors. In this chapter, recent advances on the effects of drought priming-induced heat tolerance and the underlying mechanisms are discussed.
Priming-Mediated Stress and Cross-Stress Tolerance in Crop Plants https://doi.org/10.1016/B978-0-12-817892-8.00009-X
© 2020 Elsevier Inc. All rights reserved.
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9.2 Regulation of photosynthesis through drought priming for acquired heat tolerance Photosynthesis is the fundamental process for plant growth and is highly sensitive to high temperature.9 Plants may close their stomata to avoid excessive transpirational water loss, which reduces CO2 uptake and lowers the photosynthetic rate of leaves in response to heat stress.10 Heat stress also affects photosynthesis by inhibiting carbon fixation and assimilation, as well as light reactions and electron transport.11 Drought priming-enhanced heat tolerance has been associated with the alleviation of heat inhibition in photosynthesis in various plant species. Wang et al. found that drought priming could alleviate photo-inhibition in spring wheat flag leaves caused by heat stress episodes during grain filling and that the higher net photosynthetic rate of flag leaves coincided with the lower nonphotochemical quenching rates in drought-primed plants.12 Wheat plants pretreated with moderate drought priming (leaf water potential reached ca. 0.9 MPa) at the fifth-leaf stage for 11 days possessed higher leaf water potential, chlorophyll content, and consequently a higher photosynthetic rate when exposed to postanthesis heat stress.13 Recent proteomic evidence has shown that the main regulatory mechanisms behind drought-enhanced heat tolerance of winter wheat include improvement of photosynthesis through regulated expression of proteins involved in the light reactions, Calvin cycle, and photorespiration, therefore increasing grain yield.10 These reports suggest that drought priming can enhance protection of photosynthetic machinery when plants are exposed to a later stress event. Chlorophyll fluorescence has been used as an efficient and noninvasive diagnostic tool for evaluating the susceptibility of plant photosynthetic processes to stress and it provides valuable information regarding the structure and function of the photosynthetic apparatus.14 The ratio of variable fluorescence (Fv) to the maximum fluorescence (Fm) (Fv/Fm) reflects the maximal efficiency of photosystem II (PSII) photochemistry and can be used as a guide for screening heat tolerant cultivars.15,16 When cedar (Cedrus brevifolia) seedlings were exposed to heat stress at 45°C for 5 h, Fv/Fm was significantly reduced in the nonprimed plants, whereas that of the drought-primed plants remained unaffected, and the droughtprimed seedlings exhibited a higher tolerance to heat stress than the nonprimed seedlings at 60 days after re-watering.17 Drought-primed tall fescue (Festuca arundinacea) also maintained higher Fv/Fm compared to that of the nonprimed plants when exposed to a subsequent period of heat stress.18 It is suggested that drought priming decreased the sensitivity of PSII to heat stress, thus enabling plant photosynthetic machinery to maintain function.
9.3 Regulation of antioxidant protection through drought priming for acquired heat tolerance Reactive oxygen species (ROS, e.g., O2% , H2O2, OH, 1O2), accumulate when plants are subjected to abiotic stresses.19 Low concentrations of ROS can act as essential secondary messengers for cell metabolism, while high concentrations of ROS can cause lipid
Drought priming-induced heat tolerance: metabolic pathways and molecular mechanisms
peroxidation, protein denaturalization, pigment breakdown, carbohydrate oxidation, and DNA damage, eventually leading to programmed cell death.20,21 ROS types and levels, as well as the efficiency of ROS-scavenging systems, are considered to be key elements in evaluating plant tolerance to single or multiple stresses.21 Plants have evolved a complex enzymatic and nonenzymatic ROS scavenging and detoxification system. The major ROS-scavenging enzymes include superoxide dismutase (SOD), ascorbate peroxidase (APX), catalase (CAT), glutathione peroxidase (GPX), peroxiredoxin (PrxR), and glutathione reductase (GR). The nonenzymatic antioxidants include ascorbic acid (ASA), reduced glutathione (GSH), carotenoids, and flavonoids.22 Drought priming may activate antioxidant defense mechanisms to protect plants from subsequent events of heat stress. Peng et al. demonstrated that after pretreatment with drought, the activities of antioxidant enzymes (SOD, APX, and CAT) were not significantly different between the drought-primed and nonprimed plants before heat stress, while significantly higher activities of SOD, POD, and APX were noted in the drought-primed plants under heat stress.23 SOD and POD activities were also enhanced in the drought-primed wheat plants exposed to heat stress, while the contents of malondialdehyde (MDA) and H2O2, indicators of the oxidation level in plant leaves were notably lower in the drought-primed plants compared to the nonprimed ones.10 Drought pretreatment in growth medium with 20% moisture for 3 days induced the activities of SOD, APX, CAT, and GR in tomato (Solanum lycopersicum) as well as the transcript levels of the genes encoding these antioxidants under drought stress (in growth medium with 15% moisture for 3 days).24 Single or double drought priming by withholding watering for 5–7 days before anthesis led to higher APX activity, lower MDA content, and resulted in higher wheat grain yield under drought stress during grain filling.25 There was also an enhancement of ASA and GSH content in heat, waterlogging, and cold priming treatments, although no similar findings have been made for drought primingenhanced heat tolerance.8,24,26
9.4 Metabolic reprogramming associated with drought primingenhanced heat tolerance Heat stress affects the stability of various proteins and limits the efficiency of enzymatic reactions, interrupting both primary and secondary metabolism.27–29 When plants are exposed to drought, metabolic reprogramming occurs, involving changes in various metabolites that may function in enhancing or inducing plant heat tolerance,30,31 such as primary (i.e., carbohydrates, organic and amino acids, sugars, lipids, and hormones) and secondary metabolites (i.e., flavonoids and phenolics).32,33
9.4.1 Hormones The interactions between plants and the environment are mediated by plant hormones, which have been demonstrated to play pivotal roles in the tolerance of plants to heat
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stress, and are being applied increasingly to manipulate plant growth and yield.34,35 Among them, abscisic acid (ABA) is a key signaling molecule in activating plant responses to water deficit and heat stress.36 Under mild drought conditions, when soil drying begins, the accumulation of ABA modulates guard cell ion transport and promotes stomatal closure, thus reducing transpirational water loss.37,38 ABA also acts as a stress signaling hormone by inducing the accumulation of various proteins involved in stress protection.39 The role of ABA in acquired thermotolerance has been indicated in several studies using ABA-deficient or ABA-insensitive mutants, and overexpression of genes encoding ABA synthesis enzymes, or those involved in ABA signaling pathways increased heat tolerance in various plant species.40–44 Wang et al. found that drought priming wheat for 5–7 days (with SRWC decreased to 30%–40%) significantly increased ABA concentration in leaves under heat stress compared to the nonprimed plants.12 The authors concluded that having a high concentration of ABA in reproductive organs during grain filling stages under stress conditions may enhance sink strength and facilitate remobilization of the stored assimilate to grains, thus contributing to increased grain yield. Additionally, endogenous accumulation of ABA has been observed to promote root growth, which also may explain the enhancement of heat tolerance.45 Jiang and Huang46 found that heat stress reduced root dry biomass and that root dry biomass was 100% higher in drought primed plants than in nonprimed plants in the 20–40 cm soil layer. Under high temperature conditions, deep root development has been associated with higher leaf transpiration rates, serving as a mechanism by which plants maintain cooler canopies at high temperatures.47 The biosynthesis of jasmonic acid (JA) and salicylic acid (SA) has been found to occur during heat or cold priming and results in improved heat or cold tolerance, respectively.8,48,49 There is also evidence that other plant hormones, such as ethylene (ET), cytokinins, and auxins, are predominately associated with the stimulation of cell division and control of plant growth and development under heat stress.35,39 However, the mechanisms by which these hormones participate in the acquisition of tolerance to various stresses is largely unknown and needs further investigation.
9.4.2 Osmoregulants and stress protective metabolites Various metabolites participate in the adaptive mechanisms in plants exposed to high temperature stress and function in osmotic adjustment and stress tolerance.50 The accumulation of proline, glycine betaine, and soluble sugars contributes to maintaining osmotic balance and membrane stability under drought and heat stresses.32,51 Engineering plants for increased biosynthesis of osmolytes such as mannitol, proline, and glycine betaine has been proven to have a positive effect on abiotic stress tolerance through oxidative detoxification and production of protective xanthophyll pigments.51,52 Glycine betaine can act as both an antioxidant and metabolic signal that maintains redox
Drought priming-induced heat tolerance: metabolic pathways and molecular mechanisms
homeostasis and regulates the expression of genes involved in stress response.8 Cold or heat priming induced accumulation of endogenous osmo-protectants was found to contribute to the increased subsequent cold, drought, and salt tolerance.8 With two 14-day cycles of soil drying (soil volumetric water content decreased to 5%), drought-primed Kentucky bluegrass (Poa pratensis) plants had 23% higher level of proline at 7 days of heat stress and 21% and 44% higher soluble carbohydrate content at 14 and 21 days of heat stress than the nonprimed plants, respectively. The accumulation of soluble carbohydrate and proline content in drought-primed plants contributed to higher osmotic adjustment and resulted in higher turf quality.46 A deepened knowledge of how the synthesis of compatible solutes is activated could definitely help to manipulate plant stress tolerance and provide guidance for molecular breeding for stress tolerant plants.
9.4.3 Fatty acid and lipid metabolism Fatty acids are major and essential constituents of cellular membranes, affecting membrane integrity and fluidity, and serving as energy reserves for various metabolic processes.53,54 Fatty acid unsaturation index is positively correlated with heat tolerance since the saturation level of fatty acids influences membrane fluidity.55 The research on Kentucky bluegrass showed that, compared to the well water control, plants pretreated by 12 days drought priming accumulated higher total fatty acids. The content of linolenic acid (C18:3) were significantly higher and the content of palmitic acid (C16:0) was significantly lower in the primed plants than in the nonprimed plants at 15 days of heat stress (35°C/30°C).23 The accumulation of linolenic acids and the higher unsaturation degree of fatty acids also play vital roles in acquiring drought, heat, and cold tolerance.55–57 It appears that a higher unsaturation level of fatty acids by drought priming would be beneficial for maintaining membrane fluidity, and leads to the enhanced tolerance of plants to later stresses. Lipids are esters of glycerol and fatty acids and are the main composition of many structural compounds including fats, waxes, phospholipids, and glycolipids.58 Phospholipids are one major component of plant plasma membranes, which are the interface between plant cell and the environment.59 Phospholipids acts not only as structural but also as signaling molecule for transducing information across the membrane bilayer, while glycolipid are the most abundant lipids in chloroplasts, regulating thylakoid membrane stability and integrity for photosynthetic electron transport.18,60 Through lipidomics, Zhang et al. found that drought priming (8 days withholding of irrigation) increased the content of 36:6 lipid molecular species of both phospholipids and glycolipids, which helped to maintain higher unsaturation levels comparing to the nonprimed plants.18 In addition, the accumulation of signaling lipids (phosphatidic acid, lysophospholipids) by drought priming could activate the downstream pathways and protect the plants from heat damages. Previous studies also proved that cold acclimation induced
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changes of lipid classes and molecular species were associated with the maintenance of thermodynamic properties and physiological functions of plasma membrane, thus contributing to the increased freezing tolerance.61 Our understanding of lipid metabolic reprogramming for drought priming induced heat tolerance in plants remains incomplete. Although it has been proven that the composition and the unsaturation index of fatty acids and lipids played a significant role in drought priming-induced heat tolerance, the biochemical and molecular mechanisms for specific lipids responsive to drought priming for improving heat tolerance remain largely unknown and deserve further investigation.
9.5 Molecular responses to drought priming for acquired heat tolerance Plant stress response and tolerance to drought and heat stress involve various changes at the molecular level, including transcription factors (TFs), protein kinases and phosphatases, and downstream genes.62–64 Stress signal perception and transduction are critical for metabolic and gene-expression reprogramming under stress conditions.65 Abiotic stress can cause increases in the cytosolic free calcium concentration in plants, and activate the mitogen-activated protein kinase (MAPK) and the Ca2+-dependent protein kinase (CDPK) gene families.66,67 Overexpression of MPK5 increased salt and oxidative stress tolerance in plants by repressing ROS accumulation under high salinity and inhibited pathogens by influencing SA-mediated and JA/ET-mediated defense responses.68 In rice, CPK9 plays a positive role in drought, osmotic, and dehydration stress responses by improving osmotic adjustment and stomatal movement, and regulating expression of stress-associated genes.69 The central roles of CDPKs and MPKs acting as downstream of second messengers participating in biotic priming has been proved.67,70 However, their function in drought priming-induced heat tolerance is not clear yet. TFs have important roles in the perception of stress signals and regulating expression of many stress-responsive genes by interacting with cis-acting elements present in their promoter regions.62 Thus, TFs are good candidates for genetic engineering for stresstolerant plant breeding.71 The dehydration-responsive element (DRE), which contains the core sequence A/GCCGAC, and ABA-responsive elements (ABREs contains the sequence ACGTGGC) are cis-acting elements involved in the expression of genes in response to various abiotic stresses.43,72 The roles of DREB and ABRE-binding protein (AREB) have been proven in cold acclimation.48,73 Traditional genetic and molecular analyses have identified C-repeat/DREB binding factors (CBFs) as key TFs that function in cold acclimation.74 In the process of drought priming-induced heat response, the genes induced by drought pretreatment may be activated faster in the primed plants under heat stress. DREBs and AREBs can be activated by drought and exogenous ABA treatment, which may play important roles in drought priming-enhanced heat tolerance.1,75
Drought priming-induced heat tolerance: metabolic pathways and molecular mechanisms
Heat stress causes plant proteins to dysfunction; therefore, maintaining proteins in their functional conformations and preventing the aggregation of nonnative proteins are particularly important for plant survival under high temperature stress.1,76 As molecular chaperones, heat shock proteins (HSPs) play essential functions in protecting plants against heat stress, as they are responsible for protein folding, translocation, and stabilization, and can assist in protein refolding under stress conditions.77 In wheat, proteomic analysis showed that increased abundances of HSP70 and HOP (HSP70-HSP90 organizing protein) were evident in leaves pretreated with drought under heat stress.10 The increase in the expression of HSPs is transcriptionally regulated mostly by heat shock factors (HSFs), and it has been demonstrated that HSFs are involved in heat and cold priming.8,78–80 Moreover, HsfAs could directly enhance the expression of other TFs, like MBF1c (multiprotein bridging factor 1c), which is a transcriptional co-activator mediating transcriptional activation by bridging an activator to a TATA-box binding protein, and they are required for thermotolerance.81,82 HSFs might also take part in drought priming-enhanced heat tolerance, but the involvement of HSFs as key transcriptional factors in cross-stress tolerance remains to be established. The molecular basis of drought priming-induced heat tolerance remains largely unclear and further studies are essential to elucidate the underlying molecular mechanisms.
9.6 Stress memory and epigenetic changes involved in drought priming-induced heat tolerance Plant stress memory has been associated with epigenetic changes, especially in long-term or trans-generational memories.5 The epigenetic changes involve modification of DNA methylation, histone modification, and chromatin remodeling. Such changes are inherited through mitotic cell divisions and can be transmitted to the next generation in some cases.83 They have been recognized as important adaptation strategies and as a mechanistic basis for stress memory, enabling plants to respond faster and more efficiently to recurring stress or even to prepare their offspring for potential future climate changes.84 In recent years, scientists have developed approaches and tools for estimating and quantifying epigenetic variations with respect to their impacts on plant responses to environmental stresses.85 DNA methylation and alterations in chromatin dynamics can be induced by drought or temperature treatments and these changes at the level of drought-inducible genes are associated with altered expression of transcriptional responses.86 Trimethylation of histone H3 at the position of lysine 4 (H3K4me3) is a prominent histone mark known to be connected with promoters and early-transcribed regions of active genes, and functions in promoting gene transcription.87 Changes in H3K4me3 in response to preexposure to drought have been reported for delaying dehydrin-induced gene expression.88 Furthermore, some epigenetic processes are controlled by fluxes of certain hormones, such as ABA, which are in turn influenced by drought and heat stress, resulting in plant
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adaptation.89,90 However, no research has been conducted regarding epigenetic changes related to drought priming-enhanced heat tolerance, in efforts to decipher how epigenetic machinery responds to environmental stresses so that epigenetic modifications may be used in breeding new crop cultivars that are more resilient to a future changing climate.85
9.7 Conclusions and future research perspectives Various physiological, metabolic, and molecular factors are involved in drought priminginduced subsequent heat tolerance, including the induction of stress signaling perception and transduction components, such as CDPKs and MPKs, transcriptional factors (DREB, AREB, HSFs), HSPs, and stress responsive genes. The improved photosynthesis, balanced ROS homeostasis, and metabolic reprogramming occurring during drought priming may also contribute to priming-enhanced heat tolerance. Applying the basic knowledge of drought priming to practice may lead to improvement of sustainable agriculture globally in the future. Although priming has proven to be an effective way to promote plant stress tolerance, the mechanisms behind drought priming-induced heat tolerance remain largely unclear, especially at the molecular level, and merit further investigation.
Acknowledgments The authors would like to acknowledge the Natural Science Foundation of Jiangsu Province, China (BK20180521), the China Postdoctoral Science Foundation (2017M611840), the Fundamental Research Funds for the Central Universities (KYCY201701), and Rutgers Center of Turfgrass Science.
References 1. Mittler R, Finka A, Goloubinoff P. How do plants feel the heat? Trends Biochem Sci 2012;37(3):118–25. 2. Semenov MA, Shewry PR. Modelling predicts that heat stress, not drought, will increase vulnerability of wheat in Europe. Sci Rep 2011;1:66. 3. IPCC. Climate change 2007—The physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate changeCambridge: Cambridge University Press; 2007. 4. Allakhverdiev SI, Kreslavski VD, Klimov VV, Los DA, Carpentier R, Mohanty P. Heat stress: an overview of molecular responses in photosynthesis. Photosynth Res 2008;98(1–3):541–50. 5. Bruce TJA, Matthes MC, Napier JA, Pickett JA. Stressful “memories” of plants: evidence and possible mechanisms. Plant Sci 2007;173(6):603–8. 6. Pastor V, Luna E, Mauch-Mani B, Ton J, Flors V. Primed plants do not forget. Environ Exp Bot 2013;94:46–56. 7. Wang X, Liu F, Jiang D. Priming: a promising strategy for crop production in response to future climate. J Integr Agric 2017;16(12):2709–16. 8. Hossain MA, Li ZG, Hoque TS, Burritt DJ, Fujita M, Munne-Bosch S. Heat or cold priming-induced cross-tolerance to abiotic stresses in plants: key regulators and possible mechanisms. Protoplasma 2018;255(1):399–412.
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9. Gururani Mayank A, Venkatesh J, Tran LSP. Regulation of photosynthesis during abiotic stress-induced photoinhibition. Mol Plant 2015;8(9):1304–20. 10. Zhang X, Wang X, Zhong J, et al. Drought priming induces thermo-tolerance to post-anthesis hightemperature in offspring of winter wheat. Environ Exp Bot 2016;127:26–36. 11. Jedmowski C, Ashoub A, Momtaz O, Br€ uggemann W. Impact of drought, heat, and their combination on chlorophyll fluorescence and yield of wild barley (Hordeum spontaneum). J Bot 2015;2015:9. 12. Wang X, Vignjevic M, Liu F, Jacobsen S, Jiang D, Wollenweber B. Drought priming at vegetative growth stages improves tolerance to drought and heat stresses occurring during grain filling in spring wheat. Plant Growth Regul 2015;75(3):677–87. 13. Liu S, Li X, Larsen DH, Zhu X, Song F, Liu F. Drought priming at vegetative growth stage enhances nitrogen-use efficiency under post-anthesis drought and heat stress in wheat. J Agron Crop Sci 2017;203 (1):29–40. 14. Stirbet A, Laza´r D, Kromdijk J, Govindjee. Chlorophyll a fluorescence induction: can just a one-second measurement be used to quantify abiotic stress responses? Photosynthetica 2018;56(1):86–104. 15. Xu Y, Wang J, Bonos S, Meyer W, Huang B. Candidate genes and molecular markers correlated to physiological traits for heat tolerance in fine fescue cultivars. Int J Mol Sci 2018;19(1):116. 16. Haque MS, Kjaer KH, Rosenqvist E, Sharma DK, Ottosen CO. Heat stress and recovery of photosystem II efficiency in wheat (Triticum aestivum L.) cultivars acclimated to different growth temperatures. Environ Exp Bot 2014;99:1–8. 17. Ladjal M, Epron D, Ducrey M. Effects of drought preconditioning on thermotolerance of photosystem II and susceptibility of photosynthesis to heat stress in cedar seedlings. Tree Physiol 2000;20(18):1235–41. 18. Zhang X, Xu Y, Huang B. Lipidomic reprogramming associated with drought stress priming-enhanced heat tolerance in tall fescue (Festuca arundinacea). Plant Cell Environ 2019;42:947–58. 19. Choudhury FK, Rivero RM, Blumwald E, Mittler R. Reactive oxygen species, abiotic stress and stress combination. Plant J 2017;90(5):856–67. 20. Suzuki N, Koussevitzky S, Mittler RON, Miller GAD. ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ 2012;35(2):259–70. 21. de Pinto MC, Locato V, Paradiso A, De Gara L. Role of redox homeostasis in thermo-tolerance under a climate change scenario. Ann Bot 2015;116(4):487–96. 22. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F. Reactive oxygen gene network of plants. Trends Plant Sci 2004;9(10):490–8. 23. Peng Y, Xu C, Xu L, Huang B. Improved heat tolerance through drought preconditioning associated with changes in lipid composition, antioxidant enzymes, and protein expression in Kentucky bluegrass. Crop Sci 2012;52:807–17. 24. Zhou J, Xia XJ, Zhou Y-H, Shi K, Chen Z, Yu JQ. RBOH1-dependent H2O2 production and subsequent activation of MPK1/2 play an important role in acclimation-induced cross-tolerance in tomato. J Exp Bot 2014;65(2):595–607. 25. Wang X, Vignjevic M, Jiang D, Jacobsen S, Wollenweber B. Improved tolerance to drought stress after anthesis due to priming before anthesis in wheat (Triticum aestivum L.) var. Vinjett. J Exp Bot 2014;65 (22):6441–56. 26. Wang X, Huang M, Zhou Q, et al. Physiological and proteomic mechanisms of waterlogging priming improves tolerance to waterlogging stress in wheat (Triticum aestivum L.). Environ Exp Bot 2016;132:175–82. 27. Bita C, Gerats T. Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci 2013;4:273. 28. Ruelland E, Zachowski A. How plants sense temperature. Environ Exp Bot 2010;69(3):225–32. 29. Rivero RM, Mestre TC, Mittler R, Rubio F, Garcia-Sanchez F, Martinez V. The combined effect of salinity and heat reveals a specific physiological, biochemical and molecular response in tomato plants. Plant Cell Environ 2014;37(5):1059–73. 30. Obata T, Witt S, Lisec J, et al. Metabolite profiles of maize leaves in drought, heat, and combined stress field trials reveal the relationship between metabolism and grain yield. Plant Physiol 2015;169 (4):2665–83.
157
158
Priming-mediated stress and cross-stress tolerance in crop plants
31. Tripathi P, Rabara RC, Reese RN, et al. A toolbox of genes, proteins, metabolites and promoters for improving drought tolerance in soybean includes the metabolite coumestrol and stomatal development genes. BMC Genomics 2016;17(1):102. 32. Zandalinas SI, Mittler R, Balfagon D, Arbona V, Gomez-Cadenas A. Plant adaptations to the combination of drought and high temperatures. Physiol Plant 2018;162(1):2–12. 33. Mouradov A, Spangenberg G. Flavonoids: a metabolic network mediating plants adaptation to their real estate. Front Plant Sci 2014;5:620. 34. Zhou W, Leul M. Uniconazole-induced tolerance of rape plants to heat stress in relation to changes in hormonal levels, enzyme activities and lipid peroxidation. Plant Growth Regul 1999;27(2):99–104. 35. Dobra J, Motyka V, Dobrev P, et al. Comparison of hormonal responses to heat, drought and combined stress in tobacco plants with elevated proline content. J Plant Physiol 2010;167(16):1360–70. 36. Kollist H, Zandalinas SI, Sengupta S, Nuhkat M, Kangasj€arvi J, Mittler R. Rapid responses to abiotic stress: priming the landscape for the signal transduction network. Trends Plant Sci 2019;24(1):25–37. 37. Li J, Wang XQ, Watson MB, Assmann SM. Regulation of abscisic acid-induced stomatal closure and anion channels by guard cell AAPK kinase. Science 2000;287(5451):300. 38. Osakabe Y, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS. ABA control of plant macroelement membrane transport systems in response to water deficit and high salinity. New Phytol 2014;202(1):35–49. 39. Wani SH, Kumar V, Shriram V, Sah SK. Phytohormones and their metabolic engineering for abiotic stress tolerance in crop plants. Crop J 2016;4(3):162–76. 40. Larkindale J, Hall JD, Knight MR, Vierling E. Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol 2005;138(2):882–97. 41. Xian L, Sun P, Hu S, Wu J, Liu JH. Molecular cloning and characterization of CrNCED1, a gene encoding 9-cis-epoxycarotenoid dioxygenase in Citrus reshni, with functions in tolerance to multiple abiotic stresses. Planta 2014;239(1):61–77. 42. Wu JR, Wang LC, Lin YR, Weng CP, Yeh CH, Wu SJ. The Arabidopsis heat-intolerant 5 (hit5)/ enhanced response to aba 1 (era1) mutant reveals the crucial role of protein farnesylation in plant responses to heat stress. New Phytol 2017;213(3):1181–93. 43. Kidokoro S, Watanabe K, Ohori T, et al. Soybean DREB1/CBF-type transcription factors function in heat and drought as well as cold stress-responsive gene expression. Plant J 2015;81(3):505–18. 44. Urano K, Maruyama K, Jikumaru Y, Kamiya Y, Yamaguchi-Shinozaki K, Shinozaki K. Analysis of plant hormone profiles in response to moderate dehydration stress. Plant J 2017;90(1):17–36. 45. Kuromori T, Seo M, Shinozaki K. ABA transport and plant water stress responses. Trends Plant Sci 2018;23(6):513–22. 46. Jiang Y, Huang B. Osmotic adjustment and root growth associated with drought preconditioningenhanced heat tolerance in Kentucky bluegrass. Crop Sci 2001;41(4):1168–73. 47. Pinto RS, Reynolds MP. Common genetic basis for canopy temperature depression under heat and drought stress associated with optimized root distribution in bread wheat. Theor Appl Genet 2015;128(4):575–85. 48. Xin C, Wang X, Cai J, et al. Changes of transcriptome and proteome are associated with the enhanced post-anthesis high temperature tolerance induced by pre-anthesis heat priming in wheat. Plant Growth Regul 2016;79(2):135–45. 49. Li Q, Lei S, Du K, et al. RNA-seq based transcriptomic analysis uncovers α-linolenic acid and jasmonic acid biosynthesis pathways respond to cold acclimation in Camellia japonica. Sci Rep 2016;6:36463. 50. Wahid A. Physiological implications of metabolite biosynthesis for net assimilation and heat-stress tolerance of sugarcane (Saccharum officinarum) sprouts. J Plant Res 2007;120(2):219–28. 51. Conde A, Chaves MM, Geros H. Membrane transport, sensing and signaling in plant adaptation to environmental stress. Plant Cell Physiol 2011;52(9):1583–602. 52. Chen THH, Murata N. Glycinebetaine protects plants against abiotic stress: mechanisms and biotechnological applications. Plant Cell Environ 2011;34(1):1–20. 53. Upchurch RG. Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress. Biotechnol Lett 2008;30(6):967–77. 54. Lim GH, Singhal R, Kachroo A, Kachroo P. Fatty acid- and lipid-mediated signaling in plant defense. Annu Rev Phytopathol 2017;55(1):505–36.
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55. Wang J, Juliani HR, Jespersen D, Huang B. Differential profiles of membrane proteins, fatty acids, and sterols associated with genetic variations in heat tolerance for a perennial grass species, hard fescue (Festuca trachyphylla). Environ Exp Bot 2017;140:65–75. 56. Xu L, Han L, Huang B. Membrane fatty acid composition and saturation levels associated with leaf dehydration tolerance and post-drought rehydration in Kentucky bluegrass. Crop Sci 2011;51(1):273–81. 57. Zhang C, Tian S. Peach fruit acquired tolerance to low temperature stress by accumulation of linolenic acid and N-acylphosphatidylethanolamine in plasma membrane. Food Chem 2010;120(3):864–72. 58. Singh SC, Sinha RP, H€ader DP. Role of lipids and fatty acids in stress tolerance in cyanobacteria. Acta Protozool 2012;41:297–308. 59. Ruelland E, Kravets V, Derevyanchuk M, Martinec J, Zachowski A, Pokotylo I. Role of phospholipid signalling in plant environmental responses. Environ Exp Bot 2015;114:129–43. 60. Hou Q, Ufer G, Bartels D. Lipid signalling in plant responses to abiotic stress. Plant Cell Environ 2016;39 (5):1029–48. 61. Takahashi D, Imai H, Kawamura Y, Uemura M. Lipid profiles of detergent resistant fractions of the plasma membrane in oat and rye in association with cold acclimation and freezing tolerance. Cryobiology 2016;72(2):123–34. 62. Guo M, Liu JH, Ma X, Luo DX, Gong ZH, Lu MH. The plant heat stress transcription factors (HSFs): structure, regulation, and function in response to abiotic stresses. Front Plant Sci 2016;7:114. 63. Yoshida T, Mogami J, Yamaguchi-Shinozaki K. ABA-dependent and ABA-independent signaling in response to osmotic stress in plants. Curr Opin Plant Biol 2014;21:133–9. 64. Prasch CM, Sonnewald U. Signaling events in plants: stress factors in combination change the picture. Environ Exp Bot 2015;114:4–14. 65. Zhu JK. Abiotic stress signaling and responses in plants. Cell 2016;167(2):313–24. 66. Kurusu T, Kuchitsu K, Tada Y. Plant signaling networks involving Ca2+ and Rboh/Nox-mediated ROS production under salinity stress. Front Plant Sci 2015;6:427. 67. Smekalova´ V, Doskocilova´ A, Komis G, Sˇamaj J. Crosstalk between secondary messengers, hormones and MAPK modules during abiotic stress signalling in plants. Biotechnol Adv 2014;32(1):2–11. 68. Zhang D, Jiang S, Pan J, et al. The overexpression of a maize mitogen-activated protein kinase gene (ZmMPK5) confers salt stress tolerance and induces defence responses in tobacco. Plant Biol 2014;16 (3):558–70. 69. Wei S, Hu W, Deng X, et al. A rice calcium-dependent protein kinase OsCPK9 positively regulates drought stress tolerance and spikelet fertility. BMC Plant Biol 2014;14(1):133. 70. Hake K, Romeis T. Protein kinase-mediated signalling in priming: immune signal initiation, propagation, and establishment of long-term pathogen resistance in plants. Plant Cell Environ 2019;42:904–17. 71. Wang H, Wang H, Shao H, Tang X. Recent advances in utilizing transcription factors to improve plant abiotic stress tolerance by transgenic technology. Front Plant Sci 2016;7:67. 72. Yoshida T, Fujita Y, Maruyama K, et al. Four Arabidopsis AREB/ABF transcription factors function predominantly in gene expression downstream of SnRK2 kinases in abscisic acid signalling in response to osmotic stress. Plant Cell Environ 2015;38(1):35–49. 73. Zuther E, Lee YP, Erban A, Kopka J, Hincha DK. Natural variation in freezing tolerance and cold acclimation response in Arabidopsis thaliana and related species. In: Iwaya-Inoue M, Sakurai M, Uemura M, editors. Survival strategies in extreme cold and desiccation: Adaptation mechanisms and their applications. Singapore: Springer Singapore; 2018. p. 81–98. 74. Shi Y, Ding Y, Yang S. Molecular regulation of CBF signaling in cold acclimation. Trends Plant Sci 2018;23(7):623–37. 75. Shinozaki K, Yamaguchi-Shinozaki K. Gene networks involved in drought stress response and tolerance. J Exp Bot 2007;58(2):221–7. 76. Wang W, Vinocur B, Shoseyov O, Altman A. Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 2004;9(5):244–52. 77. Saidi Y, Finka A, Goloubinoff P. Heat perception and signalling in plants: a tortuous path to thermotolerance. New Phytol 2011;190(3):556–65. 78. Liu G, Chai F, Wang Y, et al. Genome-wide identification and classification of HSF family in grape, and their transcriptional analysis under heat acclimation and heat stress. Hortic Plant J 2018;4(4):133–43.
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Priming-mediated stress and cross-stress tolerance in crop plants
79. Olate E, Jimenez-Go´mez JM, Holuigue L, Salinas J. NPR1 mediates a novel regulatory pathway in cold acclimation by interacting with HSFA1 factors. Nat Plants 2018;4(10):811–23. 80. L€amke J, Brzezinka K, Altmann S, B€aurle I. A hit-and-run heat shock factor governs sustained histone methylation and transcriptional stress memory. EMBO J 2016;35(2):162–75. 81. Suzuki N, Sejima H, Tam R, Schlauch K, Mittler R. Identification of the MBF1 heat-response regulon of Arabidopsis thaliana. Plant J 2011;66(5):844–51. 82. Takemaru KI, Li FQ, Ueda H, Hirose S. Multiprotein bridging factor 1 (MBF1) is an evolutionarily conserved transcriptional coactivator that connects a regulatory factor and TATA element-binding protein. Proc Natl Acad Sci 1997;94(14):7251–6. 83. Kinoshita T, Seki M. Epigenetic memory for stress response and adaptation in plants. Plant Cell Physiol 2014;55(11):1859–63. 84. L€amke J, B€aurle I. Epigenetic and chromatin-based mechanisms in environmental stress adaptation and stress memory in plants. Genome Biol 2017;18(1):124. 85. Gallusci P, Dai Z, Genard M, et al. Epigenetics for plant improvement: current knowledge and modeling avenues. Trends Plant Sci 2017;22(7):610–23. 86. Crisp PA, Ganguly D, Eichten SR, Borevitz JO, Pogson BJ. Reconsidering plant memory: intersections between stress recovery, RNA turnover, and epigenetics. Sci Adv 2016;2(2):e1501340. 87. Lauberth Shannon M, Nakayama T, Wu X, et al. H3K4me3 interactions with TAF3 regulate preinitiation complex assembly and selective gene activation. Cell 2013;152(5):1021–36. 88. Ding Y, Fromm M, Avramova Z. Multiple exposures to drought ‘train’ transcriptional responses in Arabidopsis. Nat Commun 2012;3:740. 89. Sahu PP, Pandey G, Sharma N, Puranik S, Muthamilarasan M, Prasad M. Epigenetic mechanisms of plant stress responses and adaptation. Plant Cell Rep 2013;32(8):1151–9. 90. Chinnusamy V, Gong Z, Zhu JK. Abscisic acid-mediated epigenetic processes in plant development and stress responses. J Integr Plant Biol 2008;50(10):1187–95.
Drought priming-induced heat tolerance: Metabolic pathways and molecular mechanisms Xiaxiang Zhanga,b, Bingru Huangb a
College of Agro-grassland Science, Nanjing Agricultural University, Nanjing, People’s Republic of China Department of Plant Biology and Pathology, Rutgers University, New Brunswick, NJ, United States
b
9.1 Introduction Heat stress is a detrimental abiotic stress limiting plant growth and sustainable agriculture worldwide.1 With global climate change, the Earth’s surface temperature is expected to increase considerably in the coming years and climate models have predicted a potentiality for heat waves to become more severe and occur more frequently.2,3 Elevated temperature can accentuate the negative impact of heat damages in various physiological and metabolic processes, including carbon metabolism, nitrogen metabolism, nutrient uptake, water uptake, and hormone metabolism.1,4 Identifying approaches for improving heat tolerance is critically important for maintaining plant productivity in warm climatic regions. Priming, by preexposure of plants to an eliciting factor, such as chemicals, biotic, or abiotic stress, could trigger the “stress memory” of plants and enhance plant tolerance to future stresses.5,6 Among abiotic stress factors, drought priming-induced drought or heat tolerance and heat priming-induced heat tolerance have been studied in various plant species, such as wheat (Triticum aestivum), barley (Hordeum vulgare), and Arabidopsis (Arabidopsis thaliana).7 Recently, it has been proven that pretreatment by drought is a positive and effective strategy for improving plant tolerance to future stresses.5,8 Primed plants display faster and stronger activation of various defense responses at morphological, physiological, biochemical, and molecular levels.5 To counter the effects of heat stress, plants respond to changes by reprogramming their transcriptome, proteome, and metabolome during drought priming and adapt to future periods of heat stress. The development of acquired heat tolerance by drought priming has been associated with changes in various physiological and metabolic processes, as well as molecular factors. In this chapter, recent advances on the effects of drought priming-induced heat tolerance and the underlying mechanisms are discussed.
Priming-Mediated Stress and Cross-Stress Tolerance in Crop Plants https://doi.org/10.1016/B978-0-12-817892-8.00009-X
© 2020 Elsevier Inc. All rights reserved.
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9.2 Regulation of photosynthesis through drought priming for acquired heat tolerance Photosynthesis is the fundamental process for plant growth and is highly sensitive to high temperature.9 Plants may close their stomata to avoid excessive transpirational water loss, which reduces CO2 uptake and lowers the photosynthetic rate of leaves in response to heat stress.10 Heat stress also affects photosynthesis by inhibiting carbon fixation and assimilation, as well as light reactions and electron transport.11 Drought priming-enhanced heat tolerance has been associated with the alleviation of heat inhibition in photosynthesis in various plant species. Wang et al. found that drought priming could alleviate photo-inhibition in spring wheat flag leaves caused by heat stress episodes during grain filling and that the higher net photosynthetic rate of flag leaves coincided with the lower nonphotochemical quenching rates in drought-primed plants.12 Wheat plants pretreated with moderate drought priming (leaf water potential reached ca. 0.9 MPa) at the fifth-leaf stage for 11 days possessed higher leaf water potential, chlorophyll content, and consequently a higher photosynthetic rate when exposed to postanthesis heat stress.13 Recent proteomic evidence has shown that the main regulatory mechanisms behind drought-enhanced heat tolerance of winter wheat include improvement of photosynthesis through regulated expression of proteins involved in the light reactions, Calvin cycle, and photorespiration, therefore increasing grain yield.10 These reports suggest that drought priming can enhance protection of photosynthetic machinery when plants are exposed to a later stress event. Chlorophyll fluorescence has been used as an efficient and noninvasive diagnostic tool for evaluating the susceptibility of plant photosynthetic processes to stress and it provides valuable information regarding the structure and function of the photosynthetic apparatus.14 The ratio of variable fluorescence (Fv) to the maximum fluorescence (Fm) (Fv/Fm) reflects the maximal efficiency of photosystem II (PSII) photochemistry and can be used as a guide for screening heat tolerant cultivars.15,16 When cedar (Cedrus brevifolia) seedlings were exposed to heat stress at 45°C for 5 h, Fv/Fm was significantly reduced in the nonprimed plants, whereas that of the drought-primed plants remained unaffected, and the droughtprimed seedlings exhibited a higher tolerance to heat stress than the nonprimed seedlings at 60 days after re-watering.17 Drought-primed tall fescue (Festuca arundinacea) also maintained higher Fv/Fm compared to that of the nonprimed plants when exposed to a subsequent period of heat stress.18 It is suggested that drought priming decreased the sensitivity of PSII to heat stress, thus enabling plant photosynthetic machinery to maintain function.
9.3 Regulation of antioxidant protection through drought priming for acquired heat tolerance Reactive oxygen species (ROS, e.g., O2% , H2O2, OH, 1O2), accumulate when plants are subjected to abiotic stresses.19 Low concentrations of ROS can act as essential secondary messengers for cell metabolism, while high concentrations of ROS can cause lipid
Drought priming-induced heat tolerance: metabolic pathways and molecular mechanisms
peroxidation, protein denaturalization, pigment breakdown, carbohydrate oxidation, and DNA damage, eventually leading to programmed cell death.20,21 ROS types and levels, as well as the efficiency of ROS-scavenging systems, are considered to be key elements in evaluating plant tolerance to single or multiple stresses.21 Plants have evolved a complex enzymatic and nonenzymatic ROS scavenging and detoxification system. The major ROS-scavenging enzymes include superoxide dismutase (SOD), ascorbate peroxidase (APX), catalase (CAT), glutathione peroxidase (GPX), peroxiredoxin (PrxR), and glutathione reductase (GR). The nonenzymatic antioxidants include ascorbic acid (ASA), reduced glutathione (GSH), carotenoids, and flavonoids.22 Drought priming may activate antioxidant defense mechanisms to protect plants from subsequent events of heat stress. Peng et al. demonstrated that after pretreatment with drought, the activities of antioxidant enzymes (SOD, APX, and CAT) were not significantly different between the drought-primed and nonprimed plants before heat stress, while significantly higher activities of SOD, POD, and APX were noted in the drought-primed plants under heat stress.23 SOD and POD activities were also enhanced in the drought-primed wheat plants exposed to heat stress, while the contents of malondialdehyde (MDA) and H2O2, indicators of the oxidation level in plant leaves were notably lower in the drought-primed plants compared to the nonprimed ones.10 Drought pretreatment in growth medium with 20% moisture for 3 days induced the activities of SOD, APX, CAT, and GR in tomato (Solanum lycopersicum) as well as the transcript levels of the genes encoding these antioxidants under drought stress (in growth medium with 15% moisture for 3 days).24 Single or double drought priming by withholding watering for 5–7 days before anthesis led to higher APX activity, lower MDA content, and resulted in higher wheat grain yield under drought stress during grain filling.25 There was also an enhancement of ASA and GSH content in heat, waterlogging, and cold priming treatments, although no similar findings have been made for drought primingenhanced heat tolerance.8,24,26
9.4 Metabolic reprogramming associated with drought primingenhanced heat tolerance Heat stress affects the stability of various proteins and limits the efficiency of enzymatic reactions, interrupting both primary and secondary metabolism.27–29 When plants are exposed to drought, metabolic reprogramming occurs, involving changes in various metabolites that may function in enhancing or inducing plant heat tolerance,30,31 such as primary (i.e., carbohydrates, organic and amino acids, sugars, lipids, and hormones) and secondary metabolites (i.e., flavonoids and phenolics).32,33
9.4.1 Hormones The interactions between plants and the environment are mediated by plant hormones, which have been demonstrated to play pivotal roles in the tolerance of plants to heat
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stress, and are being applied increasingly to manipulate plant growth and yield.34,35 Among them, abscisic acid (ABA) is a key signaling molecule in activating plant responses to water deficit and heat stress.36 Under mild drought conditions, when soil drying begins, the accumulation of ABA modulates guard cell ion transport and promotes stomatal closure, thus reducing transpirational water loss.37,38 ABA also acts as a stress signaling hormone by inducing the accumulation of various proteins involved in stress protection.39 The role of ABA in acquired thermotolerance has been indicated in several studies using ABA-deficient or ABA-insensitive mutants, and overexpression of genes encoding ABA synthesis enzymes, or those involved in ABA signaling pathways increased heat tolerance in various plant species.40–44 Wang et al. found that drought priming wheat for 5–7 days (with SRWC decreased to 30%–40%) significantly increased ABA concentration in leaves under heat stress compared to the nonprimed plants.12 The authors concluded that having a high concentration of ABA in reproductive organs during grain filling stages under stress conditions may enhance sink strength and facilitate remobilization of the stored assimilate to grains, thus contributing to increased grain yield. Additionally, endogenous accumulation of ABA has been observed to promote root growth, which also may explain the enhancement of heat tolerance.45 Jiang and Huang46 found that heat stress reduced root dry biomass and that root dry biomass was 100% higher in drought primed plants than in nonprimed plants in the 20–40 cm soil layer. Under high temperature conditions, deep root development has been associated with higher leaf transpiration rates, serving as a mechanism by which plants maintain cooler canopies at high temperatures.47 The biosynthesis of jasmonic acid (JA) and salicylic acid (SA) has been found to occur during heat or cold priming and results in improved heat or cold tolerance, respectively.8,48,49 There is also evidence that other plant hormones, such as ethylene (ET), cytokinins, and auxins, are predominately associated with the stimulation of cell division and control of plant growth and development under heat stress.35,39 However, the mechanisms by which these hormones participate in the acquisition of tolerance to various stresses is largely unknown and needs further investigation.
9.4.2 Osmoregulants and stress protective metabolites Various metabolites participate in the adaptive mechanisms in plants exposed to high temperature stress and function in osmotic adjustment and stress tolerance.50 The accumulation of proline, glycine betaine, and soluble sugars contributes to maintaining osmotic balance and membrane stability under drought and heat stresses.32,51 Engineering plants for increased biosynthesis of osmolytes such as mannitol, proline, and glycine betaine has been proven to have a positive effect on abiotic stress tolerance through oxidative detoxification and production of protective xanthophyll pigments.51,52 Glycine betaine can act as both an antioxidant and metabolic signal that maintains redox
Drought priming-induced heat tolerance: metabolic pathways and molecular mechanisms
homeostasis and regulates the expression of genes involved in stress response.8 Cold or heat priming induced accumulation of endogenous osmo-protectants was found to contribute to the increased subsequent cold, drought, and salt tolerance.8 With two 14-day cycles of soil drying (soil volumetric water content decreased to 5%), drought-primed Kentucky bluegrass (Poa pratensis) plants had 23% higher level of proline at 7 days of heat stress and 21% and 44% higher soluble carbohydrate content at 14 and 21 days of heat stress than the nonprimed plants, respectively. The accumulation of soluble carbohydrate and proline content in drought-primed plants contributed to higher osmotic adjustment and resulted in higher turf quality.46 A deepened knowledge of how the synthesis of compatible solutes is activated could definitely help to manipulate plant stress tolerance and provide guidance for molecular breeding for stress tolerant plants.
9.4.3 Fatty acid and lipid metabolism Fatty acids are major and essential constituents of cellular membranes, affecting membrane integrity and fluidity, and serving as energy reserves for various metabolic processes.53,54 Fatty acid unsaturation index is positively correlated with heat tolerance since the saturation level of fatty acids influences membrane fluidity.55 The research on Kentucky bluegrass showed that, compared to the well water control, plants pretreated by 12 days drought priming accumulated higher total fatty acids. The content of linolenic acid (C18:3) were significantly higher and the content of palmitic acid (C16:0) was significantly lower in the primed plants than in the nonprimed plants at 15 days of heat stress (35°C/30°C).23 The accumulation of linolenic acids and the higher unsaturation degree of fatty acids also play vital roles in acquiring drought, heat, and cold tolerance.55–57 It appears that a higher unsaturation level of fatty acids by drought priming would be beneficial for maintaining membrane fluidity, and leads to the enhanced tolerance of plants to later stresses. Lipids are esters of glycerol and fatty acids and are the main composition of many structural compounds including fats, waxes, phospholipids, and glycolipids.58 Phospholipids are one major component of plant plasma membranes, which are the interface between plant cell and the environment.59 Phospholipids acts not only as structural but also as signaling molecule for transducing information across the membrane bilayer, while glycolipid are the most abundant lipids in chloroplasts, regulating thylakoid membrane stability and integrity for photosynthetic electron transport.18,60 Through lipidomics, Zhang et al. found that drought priming (8 days withholding of irrigation) increased the content of 36:6 lipid molecular species of both phospholipids and glycolipids, which helped to maintain higher unsaturation levels comparing to the nonprimed plants.18 In addition, the accumulation of signaling lipids (phosphatidic acid, lysophospholipids) by drought priming could activate the downstream pathways and protect the plants from heat damages. Previous studies also proved that cold acclimation induced
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changes of lipid classes and molecular species were associated with the maintenance of thermodynamic properties and physiological functions of plasma membrane, thus contributing to the increased freezing tolerance.61 Our understanding of lipid metabolic reprogramming for drought priming induced heat tolerance in plants remains incomplete. Although it has been proven that the composition and the unsaturation index of fatty acids and lipids played a significant role in drought priming-induced heat tolerance, the biochemical and molecular mechanisms for specific lipids responsive to drought priming for improving heat tolerance remain largely unknown and deserve further investigation.
9.5 Molecular responses to drought priming for acquired heat tolerance Plant stress response and tolerance to drought and heat stress involve various changes at the molecular level, including transcription factors (TFs), protein kinases and phosphatases, and downstream genes.62–64 Stress signal perception and transduction are critical for metabolic and gene-expression reprogramming under stress conditions.65 Abiotic stress can cause increases in the cytosolic free calcium concentration in plants, and activate the mitogen-activated protein kinase (MAPK) and the Ca2+-dependent protein kinase (CDPK) gene families.66,67 Overexpression of MPK5 increased salt and oxidative stress tolerance in plants by repressing ROS accumulation under high salinity and inhibited pathogens by influencing SA-mediated and JA/ET-mediated defense responses.68 In rice, CPK9 plays a positive role in drought, osmotic, and dehydration stress responses by improving osmotic adjustment and stomatal movement, and regulating expression of stress-associated genes.69 The central roles of CDPKs and MPKs acting as downstream of second messengers participating in biotic priming has been proved.67,70 However, their function in drought priming-induced heat tolerance is not clear yet. TFs have important roles in the perception of stress signals and regulating expression of many stress-responsive genes by interacting with cis-acting elements present in their promoter regions.62 Thus, TFs are good candidates for genetic engineering for stresstolerant plant breeding.71 The dehydration-responsive element (DRE), which contains the core sequence A/GCCGAC, and ABA-responsive elements (ABREs contains the sequence ACGTGGC) are cis-acting elements involved in the expression of genes in response to various abiotic stresses.43,72 The roles of DREB and ABRE-binding protein (AREB) have been proven in cold acclimation.48,73 Traditional genetic and molecular analyses have identified C-repeat/DREB binding factors (CBFs) as key TFs that function in cold acclimation.74 In the process of drought priming-induced heat response, the genes induced by drought pretreatment may be activated faster in the primed plants under heat stress. DREBs and AREBs can be activated by drought and exogenous ABA treatment, which may play important roles in drought priming-enhanced heat tolerance.1,75
Drought priming-induced heat tolerance: metabolic pathways and molecular mechanisms
Heat stress causes plant proteins to dysfunction; therefore, maintaining proteins in their functional conformations and preventing the aggregation of nonnative proteins are particularly important for plant survival under high temperature stress.1,76 As molecular chaperones, heat shock proteins (HSPs) play essential functions in protecting plants against heat stress, as they are responsible for protein folding, translocation, and stabilization, and can assist in protein refolding under stress conditions.77 In wheat, proteomic analysis showed that increased abundances of HSP70 and HOP (HSP70-HSP90 organizing protein) were evident in leaves pretreated with drought under heat stress.10 The increase in the expression of HSPs is transcriptionally regulated mostly by heat shock factors (HSFs), and it has been demonstrated that HSFs are involved in heat and cold priming.8,78–80 Moreover, HsfAs could directly enhance the expression of other TFs, like MBF1c (multiprotein bridging factor 1c), which is a transcriptional co-activator mediating transcriptional activation by bridging an activator to a TATA-box binding protein, and they are required for thermotolerance.81,82 HSFs might also take part in drought priming-enhanced heat tolerance, but the involvement of HSFs as key transcriptional factors in cross-stress tolerance remains to be established. The molecular basis of drought priming-induced heat tolerance remains largely unclear and further studies are essential to elucidate the underlying molecular mechanisms.
9.6 Stress memory and epigenetic changes involved in drought priming-induced heat tolerance Plant stress memory has been associated with epigenetic changes, especially in long-term or trans-generational memories.5 The epigenetic changes involve modification of DNA methylation, histone modification, and chromatin remodeling. Such changes are inherited through mitotic cell divisions and can be transmitted to the next generation in some cases.83 They have been recognized as important adaptation strategies and as a mechanistic basis for stress memory, enabling plants to respond faster and more efficiently to recurring stress or even to prepare their offspring for potential future climate changes.84 In recent years, scientists have developed approaches and tools for estimating and quantifying epigenetic variations with respect to their impacts on plant responses to environmental stresses.85 DNA methylation and alterations in chromatin dynamics can be induced by drought or temperature treatments and these changes at the level of drought-inducible genes are associated with altered expression of transcriptional responses.86 Trimethylation of histone H3 at the position of lysine 4 (H3K4me3) is a prominent histone mark known to be connected with promoters and early-transcribed regions of active genes, and functions in promoting gene transcription.87 Changes in H3K4me3 in response to preexposure to drought have been reported for delaying dehydrin-induced gene expression.88 Furthermore, some epigenetic processes are controlled by fluxes of certain hormones, such as ABA, which are in turn influenced by drought and heat stress, resulting in plant
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adaptation.89,90 However, no research has been conducted regarding epigenetic changes related to drought priming-enhanced heat tolerance, in efforts to decipher how epigenetic machinery responds to environmental stresses so that epigenetic modifications may be used in breeding new crop cultivars that are more resilient to a future changing climate.85
9.7 Conclusions and future research perspectives Various physiological, metabolic, and molecular factors are involved in drought priminginduced subsequent heat tolerance, including the induction of stress signaling perception and transduction components, such as CDPKs and MPKs, transcriptional factors (DREB, AREB, HSFs), HSPs, and stress responsive genes. The improved photosynthesis, balanced ROS homeostasis, and metabolic reprogramming occurring during drought priming may also contribute to priming-enhanced heat tolerance. Applying the basic knowledge of drought priming to practice may lead to improvement of sustainable agriculture globally in the future. Although priming has proven to be an effective way to promote plant stress tolerance, the mechanisms behind drought priming-induced heat tolerance remain largely unclear, especially at the molecular level, and merit further investigation.
Acknowledgments The authors would like to acknowledge the Natural Science Foundation of Jiangsu Province, China (BK20180521), the China Postdoctoral Science Foundation (2017M611840), the Fundamental Research Funds for the Central Universities (KYCY201701), and Rutgers Center of Turfgrass Science.
References 1. Mittler R, Finka A, Goloubinoff P. How do plants feel the heat? Trends Biochem Sci 2012;37(3):118–25. 2. Semenov MA, Shewry PR. Modelling predicts that heat stress, not drought, will increase vulnerability of wheat in Europe. Sci Rep 2011;1:66. 3. IPCC. Climate change 2007—The physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate changeCambridge: Cambridge University Press; 2007. 4. Allakhverdiev SI, Kreslavski VD, Klimov VV, Los DA, Carpentier R, Mohanty P. Heat stress: an overview of molecular responses in photosynthesis. Photosynth Res 2008;98(1–3):541–50. 5. Bruce TJA, Matthes MC, Napier JA, Pickett JA. Stressful “memories” of plants: evidence and possible mechanisms. Plant Sci 2007;173(6):603–8. 6. Pastor V, Luna E, Mauch-Mani B, Ton J, Flors V. Primed plants do not forget. Environ Exp Bot 2013;94:46–56. 7. Wang X, Liu F, Jiang D. Priming: a promising strategy for crop production in response to future climate. J Integr Agric 2017;16(12):2709–16. 8. Hossain MA, Li ZG, Hoque TS, Burritt DJ, Fujita M, Munne-Bosch S. Heat or cold priming-induced cross-tolerance to abiotic stresses in plants: key regulators and possible mechanisms. Protoplasma 2018;255(1):399–412.
Drought priming-induced heat tolerance: metabolic pathways and molecular mechanisms
9. Gururani Mayank A, Venkatesh J, Tran LSP. Regulation of photosynthesis during abiotic stress-induced photoinhibition. Mol Plant 2015;8(9):1304–20. 10. Zhang X, Wang X, Zhong J, et al. Drought priming induces thermo-tolerance to post-anthesis hightemperature in offspring of winter wheat. Environ Exp Bot 2016;127:26–36. 11. Jedmowski C, Ashoub A, Momtaz O, Br€ uggemann W. Impact of drought, heat, and their combination on chlorophyll fluorescence and yield of wild barley (Hordeum spontaneum). J Bot 2015;2015:9. 12. Wang X, Vignjevic M, Liu F, Jacobsen S, Jiang D, Wollenweber B. Drought priming at vegetative growth stages improves tolerance to drought and heat stresses occurring during grain filling in spring wheat. Plant Growth Regul 2015;75(3):677–87. 13. Liu S, Li X, Larsen DH, Zhu X, Song F, Liu F. Drought priming at vegetative growth stage enhances nitrogen-use efficiency under post-anthesis drought and heat stress in wheat. J Agron Crop Sci 2017;203 (1):29–40. 14. Stirbet A, Laza´r D, Kromdijk J, Govindjee. Chlorophyll a fluorescence induction: can just a one-second measurement be used to quantify abiotic stress responses? Photosynthetica 2018;56(1):86–104. 15. Xu Y, Wang J, Bonos S, Meyer W, Huang B. Candidate genes and molecular markers correlated to physiological traits for heat tolerance in fine fescue cultivars. Int J Mol Sci 2018;19(1):116. 16. Haque MS, Kjaer KH, Rosenqvist E, Sharma DK, Ottosen CO. Heat stress and recovery of photosystem II efficiency in wheat (Triticum aestivum L.) cultivars acclimated to different growth temperatures. Environ Exp Bot 2014;99:1–8. 17. Ladjal M, Epron D, Ducrey M. Effects of drought preconditioning on thermotolerance of photosystem II and susceptibility of photosynthesis to heat stress in cedar seedlings. Tree Physiol 2000;20(18):1235–41. 18. Zhang X, Xu Y, Huang B. Lipidomic reprogramming associated with drought stress priming-enhanced heat tolerance in tall fescue (Festuca arundinacea). Plant Cell Environ 2019;42:947–58. 19. Choudhury FK, Rivero RM, Blumwald E, Mittler R. Reactive oxygen species, abiotic stress and stress combination. Plant J 2017;90(5):856–67. 20. Suzuki N, Koussevitzky S, Mittler RON, Miller GAD. ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ 2012;35(2):259–70. 21. de Pinto MC, Locato V, Paradiso A, De Gara L. Role of redox homeostasis in thermo-tolerance under a climate change scenario. Ann Bot 2015;116(4):487–96. 22. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F. Reactive oxygen gene network of plants. Trends Plant Sci 2004;9(10):490–8. 23. Peng Y, Xu C, Xu L, Huang B. Improved heat tolerance through drought preconditioning associated with changes in lipid composition, antioxidant enzymes, and protein expression in Kentucky bluegrass. Crop Sci 2012;52:807–17. 24. Zhou J, Xia XJ, Zhou Y-H, Shi K, Chen Z, Yu JQ. RBOH1-dependent H2O2 production and subsequent activation of MPK1/2 play an important role in acclimation-induced cross-tolerance in tomato. J Exp Bot 2014;65(2):595–607. 25. Wang X, Vignjevic M, Jiang D, Jacobsen S, Wollenweber B. Improved tolerance to drought stress after anthesis due to priming before anthesis in wheat (Triticum aestivum L.) var. Vinjett. J Exp Bot 2014;65 (22):6441–56. 26. Wang X, Huang M, Zhou Q, et al. Physiological and proteomic mechanisms of waterlogging priming improves tolerance to waterlogging stress in wheat (Triticum aestivum L.). Environ Exp Bot 2016;132:175–82. 27. Bita C, Gerats T. Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci 2013;4:273. 28. Ruelland E, Zachowski A. How plants sense temperature. Environ Exp Bot 2010;69(3):225–32. 29. Rivero RM, Mestre TC, Mittler R, Rubio F, Garcia-Sanchez F, Martinez V. The combined effect of salinity and heat reveals a specific physiological, biochemical and molecular response in tomato plants. Plant Cell Environ 2014;37(5):1059–73. 30. Obata T, Witt S, Lisec J, et al. Metabolite profiles of maize leaves in drought, heat, and combined stress field trials reveal the relationship between metabolism and grain yield. Plant Physiol 2015;169 (4):2665–83.
157
158
Priming-mediated stress and cross-stress tolerance in crop plants
31. Tripathi P, Rabara RC, Reese RN, et al. A toolbox of genes, proteins, metabolites and promoters for improving drought tolerance in soybean includes the metabolite coumestrol and stomatal development genes. BMC Genomics 2016;17(1):102. 32. Zandalinas SI, Mittler R, Balfagon D, Arbona V, Gomez-Cadenas A. Plant adaptations to the combination of drought and high temperatures. Physiol Plant 2018;162(1):2–12. 33. Mouradov A, Spangenberg G. Flavonoids: a metabolic network mediating plants adaptation to their real estate. Front Plant Sci 2014;5:620. 34. Zhou W, Leul M. Uniconazole-induced tolerance of rape plants to heat stress in relation to changes in hormonal levels, enzyme activities and lipid peroxidation. Plant Growth Regul 1999;27(2):99–104. 35. Dobra J, Motyka V, Dobrev P, et al. Comparison of hormonal responses to heat, drought and combined stress in tobacco plants with elevated proline content. J Plant Physiol 2010;167(16):1360–70. 36. Kollist H, Zandalinas SI, Sengupta S, Nuhkat M, Kangasj€arvi J, Mittler R. Rapid responses to abiotic stress: priming the landscape for the signal transduction network. Trends Plant Sci 2019;24(1):25–37. 37. Li J, Wang XQ, Watson MB, Assmann SM. Regulation of abscisic acid-induced stomatal closure and anion channels by guard cell AAPK kinase. Science 2000;287(5451):300. 38. Osakabe Y, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS. ABA control of plant macroelement membrane transport systems in response to water deficit and high salinity. New Phytol 2014;202(1):35–49. 39. Wani SH, Kumar V, Shriram V, Sah SK. Phytohormones and their metabolic engineering for abiotic stress tolerance in crop plants. Crop J 2016;4(3):162–76. 40. Larkindale J, Hall JD, Knight MR, Vierling E. Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol 2005;138(2):882–97. 41. Xian L, Sun P, Hu S, Wu J, Liu JH. Molecular cloning and characterization of CrNCED1, a gene encoding 9-cis-epoxycarotenoid dioxygenase in Citrus reshni, with functions in tolerance to multiple abiotic stresses. Planta 2014;239(1):61–77. 42. Wu JR, Wang LC, Lin YR, Weng CP, Yeh CH, Wu SJ. The Arabidopsis heat-intolerant 5 (hit5)/ enhanced response to aba 1 (era1) mutant reveals the crucial role of protein farnesylation in plant responses to heat stress. New Phytol 2017;213(3):1181–93. 43. Kidokoro S, Watanabe K, Ohori T, et al. Soybean DREB1/CBF-type transcription factors function in heat and drought as well as cold stress-responsive gene expression. Plant J 2015;81(3):505–18. 44. Urano K, Maruyama K, Jikumaru Y, Kamiya Y, Yamaguchi-Shinozaki K, Shinozaki K. Analysis of plant hormone profiles in response to moderate dehydration stress. Plant J 2017;90(1):17–36. 45. Kuromori T, Seo M, Shinozaki K. ABA transport and plant water stress responses. Trends Plant Sci 2018;23(6):513–22. 46. Jiang Y, Huang B. Osmotic adjustment and root growth associated with drought preconditioningenhanced heat tolerance in Kentucky bluegrass. Crop Sci 2001;41(4):1168–73. 47. Pinto RS, Reynolds MP. Common genetic basis for canopy temperature depression under heat and drought stress associated with optimized root distribution in bread wheat. Theor Appl Genet 2015;128(4):575–85. 48. Xin C, Wang X, Cai J, et al. Changes of transcriptome and proteome are associated with the enhanced post-anthesis high temperature tolerance induced by pre-anthesis heat priming in wheat. Plant Growth Regul 2016;79(2):135–45. 49. Li Q, Lei S, Du K, et al. RNA-seq based transcriptomic analysis uncovers α-linolenic acid and jasmonic acid biosynthesis pathways respond to cold acclimation in Camellia japonica. Sci Rep 2016;6:36463. 50. Wahid A. Physiological implications of metabolite biosynthesis for net assimilation and heat-stress tolerance of sugarcane (Saccharum officinarum) sprouts. J Plant Res 2007;120(2):219–28. 51. Conde A, Chaves MM, Geros H. Membrane transport, sensing and signaling in plant adaptation to environmental stress. Plant Cell Physiol 2011;52(9):1583–602. 52. Chen THH, Murata N. Glycinebetaine protects plants against abiotic stress: mechanisms and biotechnological applications. Plant Cell Environ 2011;34(1):1–20. 53. Upchurch RG. Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress. Biotechnol Lett 2008;30(6):967–77. 54. Lim GH, Singhal R, Kachroo A, Kachroo P. Fatty acid- and lipid-mediated signaling in plant defense. Annu Rev Phytopathol 2017;55(1):505–36.
Drought priming-induced heat tolerance: metabolic pathways and molecular mechanisms
55. Wang J, Juliani HR, Jespersen D, Huang B. Differential profiles of membrane proteins, fatty acids, and sterols associated with genetic variations in heat tolerance for a perennial grass species, hard fescue (Festuca trachyphylla). Environ Exp Bot 2017;140:65–75. 56. Xu L, Han L, Huang B. Membrane fatty acid composition and saturation levels associated with leaf dehydration tolerance and post-drought rehydration in Kentucky bluegrass. Crop Sci 2011;51(1):273–81. 57. Zhang C, Tian S. Peach fruit acquired tolerance to low temperature stress by accumulation of linolenic acid and N-acylphosphatidylethanolamine in plasma membrane. Food Chem 2010;120(3):864–72. 58. Singh SC, Sinha RP, H€ader DP. Role of lipids and fatty acids in stress tolerance in cyanobacteria. Acta Protozool 2012;41:297–308. 59. Ruelland E, Kravets V, Derevyanchuk M, Martinec J, Zachowski A, Pokotylo I. Role of phospholipid signalling in plant environmental responses. Environ Exp Bot 2015;114:129–43. 60. Hou Q, Ufer G, Bartels D. Lipid signalling in plant responses to abiotic stress. Plant Cell Environ 2016;39 (5):1029–48. 61. Takahashi D, Imai H, Kawamura Y, Uemura M. Lipid profiles of detergent resistant fractions of the plasma membrane in oat and rye in association with cold acclimation and freezing tolerance. Cryobiology 2016;72(2):123–34. 62. Guo M, Liu JH, Ma X, Luo DX, Gong ZH, Lu MH. The plant heat stress transcription factors (HSFs): structure, regulation, and function in response to abiotic stresses. Front Plant Sci 2016;7:114. 63. Yoshida T, Mogami J, Yamaguchi-Shinozaki K. ABA-dependent and ABA-independent signaling in response to osmotic stress in plants. Curr Opin Plant Biol 2014;21:133–9. 64. Prasch CM, Sonnewald U. Signaling events in plants: stress factors in combination change the picture. Environ Exp Bot 2015;114:4–14. 65. Zhu JK. Abiotic stress signaling and responses in plants. Cell 2016;167(2):313–24. 66. Kurusu T, Kuchitsu K, Tada Y. Plant signaling networks involving Ca2+ and Rboh/Nox-mediated ROS production under salinity stress. Front Plant Sci 2015;6:427. 67. Smekalova´ V, Doskocilova´ A, Komis G, Sˇamaj J. Crosstalk between secondary messengers, hormones and MAPK modules during abiotic stress signalling in plants. Biotechnol Adv 2014;32(1):2–11. 68. Zhang D, Jiang S, Pan J, et al. The overexpression of a maize mitogen-activated protein kinase gene (ZmMPK5) confers salt stress tolerance and induces defence responses in tobacco. Plant Biol 2014;16 (3):558–70. 69. Wei S, Hu W, Deng X, et al. A rice calcium-dependent protein kinase OsCPK9 positively regulates drought stress tolerance and spikelet fertility. BMC Plant Biol 2014;14(1):133. 70. Hake K, Romeis T. Protein kinase-mediated signalling in priming: immune signal initiation, propagation, and establishment of long-term pathogen resistance in plants. Plant Cell Environ 2019;42:904–17. 71. Wang H, Wang H, Shao H, Tang X. Recent advances in utilizing transcription factors to improve plant abiotic stress tolerance by transgenic technology. Front Plant Sci 2016;7:67. 72. Yoshida T, Fujita Y, Maruyama K, et al. Four Arabidopsis AREB/ABF transcription factors function predominantly in gene expression downstream of SnRK2 kinases in abscisic acid signalling in response to osmotic stress. Plant Cell Environ 2015;38(1):35–49. 73. Zuther E, Lee YP, Erban A, Kopka J, Hincha DK. Natural variation in freezing tolerance and cold acclimation response in Arabidopsis thaliana and related species. In: Iwaya-Inoue M, Sakurai M, Uemura M, editors. Survival strategies in extreme cold and desiccation: Adaptation mechanisms and their applications. Singapore: Springer Singapore; 2018. p. 81–98. 74. Shi Y, Ding Y, Yang S. Molecular regulation of CBF signaling in cold acclimation. Trends Plant Sci 2018;23(7):623–37. 75. Shinozaki K, Yamaguchi-Shinozaki K. Gene networks involved in drought stress response and tolerance. J Exp Bot 2007;58(2):221–7. 76. Wang W, Vinocur B, Shoseyov O, Altman A. Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 2004;9(5):244–52. 77. Saidi Y, Finka A, Goloubinoff P. Heat perception and signalling in plants: a tortuous path to thermotolerance. New Phytol 2011;190(3):556–65. 78. Liu G, Chai F, Wang Y, et al. Genome-wide identification and classification of HSF family in grape, and their transcriptional analysis under heat acclimation and heat stress. Hortic Plant J 2018;4(4):133–43.
159
160
Priming-mediated stress and cross-stress tolerance in crop plants
79. Olate E, Jimenez-Go´mez JM, Holuigue L, Salinas J. NPR1 mediates a novel regulatory pathway in cold acclimation by interacting with HSFA1 factors. Nat Plants 2018;4(10):811–23. 80. L€amke J, Brzezinka K, Altmann S, B€aurle I. A hit-and-run heat shock factor governs sustained histone methylation and transcriptional stress memory. EMBO J 2016;35(2):162–75. 81. Suzuki N, Sejima H, Tam R, Schlauch K, Mittler R. Identification of the MBF1 heat-response regulon of Arabidopsis thaliana. Plant J 2011;66(5):844–51. 82. Takemaru KI, Li FQ, Ueda H, Hirose S. Multiprotein bridging factor 1 (MBF1) is an evolutionarily conserved transcriptional coactivator that connects a regulatory factor and TATA element-binding protein. Proc Natl Acad Sci 1997;94(14):7251–6. 83. Kinoshita T, Seki M. Epigenetic memory for stress response and adaptation in plants. Plant Cell Physiol 2014;55(11):1859–63. 84. L€amke J, B€aurle I. Epigenetic and chromatin-based mechanisms in environmental stress adaptation and stress memory in plants. Genome Biol 2017;18(1):124. 85. Gallusci P, Dai Z, Genard M, et al. Epigenetics for plant improvement: current knowledge and modeling avenues. Trends Plant Sci 2017;22(7):610–23. 86. Crisp PA, Ganguly D, Eichten SR, Borevitz JO, Pogson BJ. Reconsidering plant memory: intersections between stress recovery, RNA turnover, and epigenetics. Sci Adv 2016;2(2):e1501340. 87. Lauberth Shannon M, Nakayama T, Wu X, et al. H3K4me3 interactions with TAF3 regulate preinitiation complex assembly and selective gene activation. Cell 2013;152(5):1021–36. 88. Ding Y, Fromm M, Avramova Z. Multiple exposures to drought ‘train’ transcriptional responses in Arabidopsis. Nat Commun 2012;3:740. 89. Sahu PP, Pandey G, Sharma N, Puranik S, Muthamilarasan M, Prasad M. Epigenetic mechanisms of plant stress responses and adaptation. Plant Cell Rep 2013;32(8):1151–9. 90. Chinnusamy V, Gong Z, Zhu JK. Abscisic acid-mediated epigenetic processes in plant development and stress responses. J Integr Plant Biol 2008;50(10):1187–95.