Physiological and transcriptional memory in guard cells during repetitive dehydration stress

New Phytologist

Volumn 205, Issue 2, 2015, Pages 596-607

  Virlouvet, Laetitia ^a   Fromm, Michael ^a  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

Abscisic acid (ABA); Arabidopsis thaliana; Dehydration stress; Guard cell (GC); Memory response; SNF1 RELATED PROTEIN KINASE 2 (SnRK2)

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ABSCISIC ACID; ARABIDOPSIS PROTEIN; PROTEIN SERINE THREONINE KINASE; SNF1-RELATED PROTEIN KINASES; WATER;

ARABIDOPSIS; DESICCATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT LEAF; PLANT STOMA; SIGNAL TRANSDUCTION;

ABSCISIC ACID; ARABIDOPSIS; ARABIDOPSIS PROTEINS; DESICCATION; GENE EXPRESSION REGULATION, PLANT; PLANT LEAVES; PLANT STOMATA; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; WATER;

EID: 84919626396     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.13080     Document Type: Article

References (94)

1. Bauer H, Ache P, Lautner S, Fromm J, Hartung W, Al-Rasheid KA, Sonnewald S, Sonnewald U, Kneitz S, Lachmann N et al. 2013. The stomatal response to reduced relative humidity requires guard cell-autonomous ABA synthesis. Current Biology 23: 53-57.
2. Boudsocq M, Barbier-Brygoo H, Lauriere C. 2004. Identification of nine sucrose nonfermenting 1-related protein kinases 2 activated by hyperosmotic and saline stresses in Arabidopsis thaliana. Journal of Biological Chemistry 279: 41758-41766.
3. Brandt B, Brodsky DE, Xue S, Negi J, Iba K, Kangasjarvi J, Ghassemian M, Stephan AB, Hu H, Schroeder JI. 2012. Reconstitution of abscisic acid activation of SLAC1 anion channel by CPK6 and OST1 kinases and branched ABI1 PP2C phosphatase action. Proceedings of the National Academy of Sciences, USA 109: 10593-10598.
4. Bruce TJ, Matthes MC, Napier JA, Pickett JA. 2007. Stressful "memories" of plants: evidence for possible mechanisms. Plant Science 173: 603-608.
5. Byun YJ, Koo MY, Joo HJ, Ha-Lee YM, Lee DH. 2014. Comparative analysis of gene expression under cold acclimation, deacclimation and reacclimation in Arabidopsis. Physiologia Plantarum 152: 256-274.
6. Caesar K, Elgass K, Chen Z, Huppenberger P, Witthoft J, Schleifenbaum F, Blatt MR, Oecking C, Harter K. 2011. A fast brassinolide-regulated response pathway in the plasma membrane of Arabidopsis thaliana. Plant Journal 66: 528-540.
7. Cominelli E, Galbiati M, Vavasseur A, Conti L, Sala T, Vuylsteke M, Leonhardt N, Dellaporta SL, Tonelli C. 2005. A guard-cell-specific MYB transcription factor regulates stomatal movements and plant drought tolerance. Current Biology 15: 1196-1200.
8. Conrath U, Beckers GJ, Flors V, Garcia-Agustin P, Jakab G, Mauch F, Newman MA, Pieterse CM, Poinssot B, Pozo MJ et al. 2006. Priming: getting ready for battle. Molecular Plant-Microbe Interactions 19: 1062-1071.
9. Cornish K, Zeevaart JA. 1986. Abscisic acid accumulation by in situ and isolated guard cells of Pisum sativum L. and Vicia faba L. in relation to water stress. Plant Physiology 81: 1017-1021.
10. Davies WJ, Kozlowski TT. 1977. Variations among woody plants in stomatal conductance and photosynthesis during and after drought. Plant and Soil 46: 435-444.
11. Ding Y, Fromm M, Avramova Z. 2012. Multiple exposures to drought 'train' transcriptional responses in Arabidopsis. Nature Communications 3: 740.
12. Ding Y, Liu N, Virlouvet L, Riethoven JJ, Fromm M, Avramova Z. 2013. Four distinct types of dehydration stress memory genes in Arabidopsis thaliana. BMC Plant Biology 13: 229.
13. Dreyer I, Gomez-Porras JL, Riano-Pachon DM, Hedrich R, Geiger D. 2012. Molecular evolution of slow and quick anion channels (SLACs and QUACs/ALMTs). Frontiers in Plant Science 3: 263.
14. Flexas J, Baron M, Bota J, Ducruet JM, Galle A, Galmes J, Jimenez M, Pou A, Ribas-Carbo M, Sajnani C et al. 2009. Photosynthesis limitations during water stress acclimation and recovery in the drought-adapted Vitis hybrid Richter-110 (V. berlandierix V. rupestris). Journal of Experimental Botany 60: 2361-2377.
15. Fujii H, Chinnusamy V, Rodrigues A, Rubio S, Antoni R, Park SY, Cutler SR, Sheen J, Rodriguez PL, Zhu JK. 2009. In vitro reconstitution of an abscisic acid signalling pathway. Nature 462: 660-664.
16. Fujii H, Verslues PE, Zhu JK. 2007. Identification of two protein kinases required for abscisic acid regulation of seed germination, root growth, and gene expression in Arabidopsis. Plant Cell 19: 485-494.
17. Fujii H, Verslues PE, Zhu JK. 2011. Arabidopsis decuple mutant reveals the importance of SnRK2 kinases in osmotic stress responses in vivo. Proceedings of the National Academy of Sciences, USA 108: 1717-1722.
18. Fujii H, Zhu JK. 2009. Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress. Proceedings of the National Academy of Sciences, USA 106: 8380-8385.
19. Fujita Y, Fujita M, Satoh R, Maruyama K, Parvez MM, Seki M, Hiratsu K, Ohme-Takagi M, Shinozaki K, Yamaguchi-Shinozaki K. 2005. AREB1 Is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell 17: 3470-3488.
20. Fujita Y, Fujita M, Shinozaki K, Yamaguchi-Shinozaki K. 2011. ABA-mediated transcriptional regulation in response to osmotic stress in plants. Journal of Plant Research 124: 509-525.
21. Fujita Y, Nakashima K, Yoshida T, Katagiri T, Kidokoro S, Kanamori N, Umezawa T, Fujita M, Maruyama K, Ishiyama K et al. 2009. Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis. Plant and Cell Physiology 50: 2123-2132.
22. Furihata T, Maruyama K, Fujita Y, Umezawa T, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K. 2006. Abscisic acid-dependent multisite phosphorylation regulates the activity of a transcription activator AREB1. Proceedings of the National Academy of Sciences, USA 103: 1988-1993.
23. Galle A, Feller U. 2007. Changes of photosynthetic traits in beech saplings (Fagus sylvatica) under severe drought stress and during recovery. Physiologia Plantarum 131: 412-421.
24. Galle A, Haldimann P, Feller U. 2007. Photosynthetic performance and water relations in young pubescent oak (Quercus pubescens) trees during drought stress and recovery. New Phytologist 174: 799-810.
25. Galmes J, Medrano H, Flexas J. 2007. Photosynthetic limitations in response to water stress and recovery in Mediterranean plants with different growth forms. New Phytologist 175: 81-93.
26. Geiger D, Scherzer S, Mumm P, Stange A, Marten I, Bauer H, Ache P, Matschi S, Liese A, Al-Rasheid KA et al. 2009. Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair. Proceedings of the National Academy of Sciences, USA 106: 21425-21430.
27. Grzesiak MT, Grzesiak S, Skoczowski A. 2006. Changes of leaf water potential and gas exchange during and after drought in triticale and maize genotypes differing in drought tolerance. Photosynthetica 44: 561-568.
28. Guo FQ, Young J, Crawford NM. 2003. The nitrate transporter AtNRT1.1 (CHL1) functions in stomatal opening and contributes to drought susceptibility in Arabidopsis. Plant Cell 15: 107-117.
29. Harris MJ, Outlaw WH. 1991. Rapid adjustment of guard-cell abscisic acid levels to current leaf-water status. Plant Physiology 95: 171-173.
30. Harris MJ, Outlaw WH, Mertens R, Weiler EW. 1988. Water-stress-induced changes in the abscisic acid content of guard cells and other cells of Vicia faba L. leaves as determined by enzyme-amplified immunoassay. Proceedings of the National Academy of Sciences, USA 85: 2584-2588.
31. Ho CH, Lin SH, Hu HC, Tsay YF. 2009. CHL1 functions as a nitrate sensor in plants. Cell 138: 1184-1194.
32. + channel GORK is involved in regulation of stomatal movements and plant transpiration. Proceedings of the National Academy of Sciences, USA 100: 5549-5554.
33. 2-controlled stomatal movements in guard cells. Nature Cell Biology 12: 87-93.
34. van Hulten M, Pelser M, van Loon LC, Pieterse CM, Ton J. 2006. Costs and benefits of priming for defense in Arabidopsis. Proceedings of the National Academy of Sciences, USA 103: 5602-5607.
35. Ikegami K, Okamoto M, Seo M, Koshiba T. 2009. Activation of abscisic acid biosynthesis in the leaves of Arabidopsis thaliana in response to water deficit. Journal of Plant Research 122: 235-243.
36. Imes D, Mumm P, Bohm J, Al-Rasheid KA, Marten I, Geiger D, Hedrich R. 2013. Open stomata 1 (OST1) kinase controls R-type anion channel QUAC1 in Arabidopsis guard cells. Plant Journal 74: 372-382.
37. Iuchi S, Kobayashi M, Taji T, Naramoto M, Seki M, Kato T, Tabata S, Kakubari Y, Yamaguchi-Shinozaki K, Shinozaki K. 2001. Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant Journal 27: 325-333.
38. Jaskiewicz M, Conrath U, Peterhansel C. 2011. Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response. EMBO Reports 12: 50-55.
39. Joshi-Saha A, Valon C, Leung J. 2011. A brand new START: abscisic acid perception and transduction in the guard cell. Science Signaling 4: re4.
40. Kang JY, Choi HI, Im MY, Kim SY. 2002. Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell 14: 343-357.
41. 2+ signaling. Annual Review of Plant Biology 61: 561-591.
42. Klingler JP, Batelli G, Zhu JK. 2010. ABA receptors: the START of a new paradigm in phytohormone signalling. Journal of Experimental Botany 61: 3199-3210.
43. Koiwai H, Nakaminami K, Seo M, Mitsuhashi W, Toyomasu T, Koshiba T. 2004. Tissue-specific localization of an abscisic acid biosynthetic enzyme, AAO3, in Arabidopsis. Plant Physiology 134: 1697-1707.
44. Kulik A, Wawer I, Krzywinska E, Bucholc M, Dobrowolska G. 2011. SnRK2 protein kinases-key regulators of plant response to abiotic stresses. OMICS: A Journal of Integrative Biology 15: 859-872.
45. Kushiro T, Okamoto M, Nakabayashi K, Yamagishi K, Kitamura S, Asami T, Hirai N, Koshiba T, Kamiya Y, Nambara E. 2004. The Arabidopsis cytochrome P450 CYP707A encodes ABA 8′-hydroxylases: key enzymes in ABA catabolism. EMBO Journal 23: 1647-1656.
46. + current properties in Arabidopsis guard cells. Journal of Biological Chemistry 285: 6265-6274.
47. Lee SC, Lim CW, Lan W, He K, Luan S. 2013. ABA signaling in guard cells entails a dynamic protein-protein interaction relay from the PYL-RCAR family receptors to ion channels. Molecular Plant 6: 528-538.
48. Lee SC, Luan S. 2012. ABA signal transduction at the crossroad of biotic and abiotic stress responses. Plant, Cell & Environment 35: 53-60.
49. Leonhardt N, Kwak JM, Robert N, Waner D, Leonhardt G, Schroeder JI. 2004. Microarray expression analyses of Arabidopsis guard cells and isolation of a recessive abscisic acid hypersensitive protein phosphatase 2C mutant. Plant Cell 16: 596-615.
50. Li WX, Oono Y, Zhu J, He XJ, Wu JM, Iida K, Lu XY, Cui X, Jin H, Zhu JK. 2008. The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell 20: 2238-2251.
51. Liu N, Fromm M, Avramova Z. 2014. H3K27me3 and H3K4me3 chromatin environment at superinduced dehydration stress memory genes of A. thaliana. Molecular Plant 7: 502-513.
52. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408.
53. Loewenstein NJ, Pallardy SG. 2002. Influence of a drying cycle on post-drought xylem sap abscisic acid and stomatal responses in young temperate deciduous angiosperms. New Phytologist 156: 351-361.
54. Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E. 2009. Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324: 1064-1068.
55. Melhorn V, Matsumi K, Koiwai H, Ikegami K, Okamoto M, Nambara E, Bittner F, Koshiba T. 2008. Transient expression of AtNCED3 and AAO3 genes in guard cells causes stomatal closure in Vicia faba. Journal of Plant Research 121: 125-131.
56. Melotto M, Underwood W, He SY. 2008. Role of stomata in plant innate immunity and foliar bacterial diseases. Annual Review of Phytopathology 46: 101-122.
57. Miyashita K, Tanakamaru S, Maitani T, Kimura K. 2005. Recovery responses of photosynthesis, transpiration, and stomatal conductance in kidney bean following drought stress. Environmental and Experimental Botany 53: 205-214.
58. 2+-permeable channels and stomatal closure. PLoS Biology 4: e327.
59. Nakashima K, Yamaguchi-Shinozaki K. 2013. ABA signaling in stress-response and seed development. Plant Cell Reports 32: 959-970.
60. Nambara E, Kawaide H, Kamiya Y, Naito S. 1998. Characterization of an Arabidopsis thaliana mutant that has a defect in ABA accumulation: ABA-dependent and ABA-independent accumulation of free amino acids during dehydration. Plant and Cell Physiology 39: 853-858.
61. Nambara E, Marion-Poll A. 2005. Abscisic acid biosynthesis and catabolism. Annual Review of Plant Biology 56: 165-185.
62. Ni BR, Pallardy SG. 1992. Stomatal and nonstomatal limitations to net photosynthesis in seedlings of woody angiosperms. Plant Physiology 99: 1502-1508.
63. Pandey S, Wang X-Q, Coursol SA, Assmann SM. 2002. Preparation and applications of Arabidopsis thaliana guard cell protoplasts. New Phytologist 153: 517-526.
64. Park SY, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow TF et al. 2009. Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324: 1068-1071.
65. + channel activity in Arabidopsis involves expression of the twin channel subunits KAT1 and KAT2. Journal of Biological Chemistry 276: 3215-3221.
66. R Core Team. 2014. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing [WWW document] URL: http://www.R-project.org
67. Roychoudhury A, Paul S, Basu S. 2013. Cross-talk between abscisic acid-dependent and abscisic acid-independent pathways during abiotic stress. Plant Cell Reports 32: 985-1006.
68. Rusconi F, Simeoni F, Francia P, Cominelli E, Conti L, Riboni M, Simoni L, Martin CR, Tonelli C, Galbiati M. 2013. The Arabidopsis thaliana MYB60 promoter provides a tool for the spatio-temporal control of gene expression in stomatal guard cells. Journal of Experimental Botany 64: 3361-3371.
69. Russo SE, Cannon WL, Elowsky C, Tan S, Davies SJ. 2010. Variation in leaf stomatal traits of 28 tree species in relation to gas exchange along an edaphic gradient in a Bornean rain forest. American Journal of Botany 97: 1109-1120.
70. Sato A, Sato Y, Fukao Y, Fujiwara M, Umezawa T, Shinozaki K, Hibi T, Taniguchi M, Miyake H, Goto DB et al. 2009. Threonine at position 306 of the KAT1 potassium channel is essential for channel activity and is a target site for ABA-activated SnRK2/OST1/SnRK2.6 protein kinase. The Biochemical Journal 424: 439-448.
71. Schachtman DP, Schroeder JI, Lucas WJ, Anderson JA, Gaber RF. 1992. Expression of an inward-rectifying potassium channel by the Arabidopsis KAT1 cDNA. Science 258: 1654-1658.
72. Shinozaki K, Yamaguchi-Shinozaki K. 2007. Gene networks involved in drought stress response and tolerance. Journal of Experimental Botany 58: 221-227.
73. Sirichandra C, Gu D, Hu HC, Davanture M, Lee S, Djaoui M, Valot B, Zivy M, Leung J, Merlot S et al. 2009a. Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase. FEBS Letters 583: 2982-2986.
74. Sirichandra C, Wasilewska A, Vlad F, Valon C, Leung J. 2009b. The guard cell as a single-cell model towards understanding drought tolerance and abscisic acid action. Journal of Experimental Botany 60: 1439-1463.
75. Tan BC, Joseph LM, Deng WT, Liu L, Li QB, Cline K, McCarty DR. 2003. Molecular characterization of the Arabidopsis 9-cis epoxycarotenoid dioxygenase gene family. Plant Journal 35: 44-56.
76. Tardieu F, Parent B, Simonneau T. 2010. Control of leaf growth by abscisic acid: hydraulic or non-hydraulic processes? Plant, Cell & Environment 33: 636-647.
77. To TK, Kim JM. 2014. Epigenetic regulation of gene responsiveness in Arabidopsis. Frontiers in Plant Science 4: 548.
78. Ton J, D'Alessandro M, Jourdie V, Jakab G, Karlen D, Held M, Mauch-Mani B, Turlings TC. 2007. Priming by airborne signals boosts direct and indirect resistance in maize. Plant Journal 49: 16-26.
79. Ton J, Jakab G, Toquin V, Flors V, Iavicoli A, Maeder MN, Metraux JP, Mauch-Mani B. 2005. Dissecting the beta-aminobutyric acid-induced priming phenomenon in Arabidopsis. Plant Cell 17: 987-999.
80. +-ATPase activation in guard cell protoplasts of Arabidopsis thaliana in response to blue light. Plant and Cell Physiology 46: 955-963.
81. Umezawa T, Sugiyama N, Mizoguchi M, Hayashi S, Myouga F, Yamaguchi-Shinozaki K, Ishihama Y, Hirayama T, Shinozaki K. 2009. Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis. Proceedings of the National Academy of Sciences, USA 106: 17588-17593.
82. Vahisalu T, Kollist H, Wang YF, Nishimura N, Chan WY, Valerio G, Lamminmaki A, Brosche M, Moldau H, Desikan R et al. 2008. SLAC1 is required for plant guard cell S-type anion channel function in stomatal signalling. Nature 452: 487-491.
83. Virlouvet L, Jacquemot MP, Gerentes D, Corti H, Bouton S, Gilard F, Valot B, Trouverie J, Tcherkez G, Falque M et al. 2011. The ZmASR1 protein influences branched-chain amino acid biosynthesis and maintains kernel yield in maize under water-limited conditions. Plant Physiology 157: 917-936.
84. Wan XR, Li L. 2006. Regulation of ABA level and water-stress tolerance of Arabidopsis by ectopic expression of a peanut 9-cis-epoxycarotenoid dioxygenase gene. Biochemical and Biophysical Research Communications 347: 1030-1038.
85. Wang RS, Pandey S, Li S, Gookin TE, Zhao Z, Albert R, Assmann SM. 2011. Common and unique elements of the ABA-regulated transcriptome of Arabidopsis guard cells. BMC Genomics 12: 216.
86. Wilkinson S, Davies WJ. 2010. Drought, ozone, ABA and ethylene: new insights from cell to plant to community. Plant, Cell & Environment 33: 510-525.
87. Xie T, Ren R, Zhang YY, Pang Y, Yan C, Gong X, He Y, Li W, Miao D, Hao Q et al. 2012. Molecular mechanism for inhibition of a critical component in the Arabidopsis thaliana abscisic acid signal transduction pathways, SnRK2.6, by protein phosphatase ABI1. Journal of Biological Chemistry 287: 794-802.
88. Xu Z, Zhou G, Shimizu H. 2009. Are plant growth and photosynthesis limited by pre-drought following rewatering in grass? Journal of Experimental Botany 60: 3737-3749.
89. Xu ZY, Kim DH, Hwang I. 2013. ABA homeostasis and signaling involving multiple subcellular compartments and multiple receptors. Plant Cell Reports 32: 807-813.
90. Yamaguchi K, Takahashi Y, Berberich T, Imai A, Takahashi T, Michael AJ, Kusano T. 2007. A protective role for the polyamine spermine against drought stress in Arabidopsis. Biochemical and Biophysical Research Communications 352: 486-490.
91. Yang Y, Costa A, Leonhardt N, Siegel RS, Schroeder JI. 2008. Isolation of a strong Arabidopsis guard cell promoter and its potential as a research tool. Plant Methods 4: 6.
92. Yoshida T, Fujita Y, Sayama H, Kidokoro S, Maruyama K, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K. 2010. AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant Journal 61: 672-685.
93. You J, Zong W, Li X, Ning J, Hu H, Li X, Xiao J, Xiong L. 2013. The SNAC1-targeted gene OsSRO1c modulates stomatal closure and oxidative stress tolerance by regulating hydrogen peroxide in rice. Journal of Experimental Botany 64: 569-583.
94. Yunta C, Martinez-Ripoll M, Zhu JK, Albert A. 2011. The structure of Arabidopsis thaliana OST1 provides insights into the kinase regulation mechanism in response to osmotic stress. Journal of Molecular Biology 414: 135-144.