Signaling events in plants: Stress factors in combination change the picture

Environmental and Experimental Botany

Volumn 114, Issue , 2015, Pages 4-14

  Prasch, Christian M ^a   Sonnewald, Uwe ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Biotic stress; Combined stress; Drought stress; Heat stress; Signaling

Indexed keywords

EID: 84937860376     PISSN: 00988472     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.envexpbot.2014.06.020     Document Type: Article

References (168)

1. Achuo E.A., Prinsen E., Höfte M. Influence of drought, salt stress and abscisic acid on the resistance of tomato to Botrytis cinerea and Oidium neolycopersici. Plant Pathol. 2006, 55:178-186.
2. Ahuja I., de Vos R.C., Bones A.M., Hall R.D. Plant molecular stress responses face climate change. Trends Plant Sci. 2010, 15:664-674.
3. Alexandersson E., Fraysse L., Sjovall-Larsen S., Gustavsson S., Fellert M., Karlsson M., Johanson U., Kjellbom P. Whole gene family expression and drought stress regulation of aquaporins. Plant Mol. Biol. 2005, 59:469-484.
4. Anderson J.P., Badruzsaufari E., Schenk P.M., Manners J.M., Desmond O.J., Ehlert C., Maclean D.J., Ebert P.R., Kazan K. Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell 2004, 16:3460-3479.
5. Andreasson E., Ellis B. Convergence and specificity in the Arabidopsis MAPK nexus. Trends Plant Sci. 2010, 15:106-113.
6. Apel K., Hirt H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 2004, 55:373-399.
7. Aranda M.A., Escaler M., Wang D., Maule A.J. Induction of HSP70 and polyubiquitin expression associated with plant virus replication. Proc. Natl. Acad. Sci. U S A 1996, 93:15289-15293.
8. Asselbergh B., De Vleesschauwer D., Hofte M. Global switches and fine-tuning-ABA modulates plant pathogen defense. Mol. Plant-Microbe Interact.: MPMI 2008, 21:709-719.
9. Atkinson N.J., Lilley C.J., Urwin P.E. Identification of genes involved in the response of Arabidopsis to simultaneous biotic and abiotic stresses. Plant Physiol. 2013, 162:2028-2041.
10. Atkinson N.J., Urwin P.E. The interaction of plant biotic and abiotic stresses: from genes to the field. J. Exp. Bot. 2012, 63:3523-3543.
11. Baena-Gonzalez E., Sheen J. Convergent energy and stress signaling. Trends Plant Sci. 2008, 13:474-482.
12. Baniwal S.K., Bharti K., Chan K.Y., Fauth M., Ganguli A., Kotak S., Mishra S.K., Nover L., Port M., Scharf K.D., Tripp J., Weber C., Zielinski D., von Koskull-Doring P. Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors. J. Biosci. 2004, 29:471-487.
13. Banti V., Mafessoni F., Loreti E., Alpi A., Perata P. The heat-inducible transcription factor HsfA2 enhances anoxia tolerance in Arabidopsis. Plant Physiol. 2010, 152:1471-1483.
14. Barnabas B., Jager K., Feher A. The effect of drought and heat stress on reproductive processes in cereals. Plant Cell Environ. 2008, 31:11-38.
15. Batistic O., Kudla J. Analysis of calcium signaling pathways in plants. Biochim. Biophys. Acta 2012, 1820:1283-1293.
16. Baxter A., Mittler R., Suzuki N. ROS as key players in plant stress signalling. J. Exp. Bot. 2014, 65:1229-1240.
17. Bechtold U., Lawson T., Mejia-Carranza J., Meyer R.C., Brown I.R., Altmann T., Ton J., Mullineaux P.M. Constitutive salicylic acid defences do not compromise seed yield, drought tolerance and water productivity in the Arabidopsis accession C24. Plant Cell Environ. 2010, 33:1959-1973.
18. Berridge M.J., Irvine R.F. Inositol trisphosphate, a novel second messenger in cellular signal transduction. Nature 1984, 312:315-321.
19. Biemelt S., Sonnewald U. Plant-microbe interactions to probe regulation of plant carbon metabolism. J. Plant Physiol. 2006, 163:307-318.
20. Bita C.E., 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.
21. Carter A.H., Chen X.M., Garland-Campbell K., Kidwell K.K. Identifying QTL for high-temperature adult-plant resistance to stripe rust (Puccinia striiformis f. sp. tritici) in the spring wheat (Triticum aestivum L.) cultivar 'Louise'. Theor. Appl. Genet. (Theoretische und angewandte Genetik) 2009, 119:1119-1128.
22. Castiglioni P., Warner D., Bensen R.J., Anstrom D.C., Harrison J., Stoecker M., Abad M., Kumar G., Salvador S., D'Ordine R., Navarro S., Back S., Fernandes M., Targolli J., Dasgupta S., Bonin C., Luethy M.H., Heard J.E. Bacterial RNA chaperones confer abiotic stress tolerance in plants and improved grain yield in maize under water-limited conditions. Plant Physiol. 2008, 147:446-455.
23. Chakraborty U., Tongden C. Evaluation of heat acclimation and salicylic acid treatments as potent inducers of thermotolerance in Cicer arietinum L. Curr. Sci. 2005, 89:384-389.
24. Choi H.I., Park H.J., Park J.H., Kim S., Im M.Y., Seo H.H., Kim Y.W., Hwang I., Kim S.Y. Arabidopsis calcium-dependent protein kinase AtCPK32 interacts with ABF4, a transcriptional regulator of abscisic acid-responsive gene expression, and modulates its activity. Plant Physiol. 2005, 139:1750-1761.
25. Ciais P., Reichstein M., Viovy N., Granier A., Ogee J., Allard V., Aubinet M., Buchmann N., Bernhofer C., Carrara A., Chevallier F., De Noblet N., Friend A.D., Friedlingstein P., Grunwald T., Heinesch B., Keronen P., Knohl A., Krinner G., Loustau D., Manca G., Matteucci G., Miglietta F., Ourcival J.M., Papale D., Pilegaard K., Rambal S., Seufert G., Soussana J.F., Sanz M.J., Schulze E.D., Vesala T., Valentini R. Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 2005, 437:529-533.
26. Cramer G.R., Urano K., Delrot S., Pezzotti M., Shinozaki K. Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biol. 2011, 11:163.
27. Cutler S.R., Rodriguez P.L., Finkelstein R.R., Abrams S.R. Abscisic acid: emergence of a core signaling network. Annu. Rev. Plant Biol. 2010, 61:651-679.
28. Danquah A., de Zelicourt A., Colcombet J., Hirt H. The role of ABA and MAPK signaling pathways in plant abiotic stress responses. Biotechnol. Adv. 2014, 32:40-52.
29. Daszkowska-Golec A., Szarejko I. Open or close the gate-stomata action under the control of phytohormones in drought stress conditions. Front. Plant Sci. 2013, 4:138.
30. De Geyter N., Gholami A., Goormachtig S., Goossens A. Transcriptional machineries in jasmonate-elicited plant secondary metabolism. Trends Plant Sci. 2012, 17:349-359.
31. De Vos M., Van Oosten V.R., Van Poecke R.M., Van Pelt J.A., Pozo M.J., Mueller M.J., Buchala A.J., Metraux J.P., Van Loon L.C., Dicke M., Pieterse C.M. Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol. Plant-Microbe Interact.: MPMI 2005, 18:923-937.
32. Dropkin V.H. Necrotic reaction of tomatoes and other hosts resistant to Meloidogyne: reversal by temperature. Phytopathology 1969, 59:1632-1637.
33. Elmore J.M., Lin Z.J., Coaker G. Plant NB-LRR signaling: upstreams and downstreams. Curr. Opin. Plant Biol. 2011, 14:365-371.
34. Finka A., Cuendet A.F., Maathuis F.J., Saidi Y., Goloubinoff P. Plasma membrane cyclic nucleotide gated calcium channels control land plant thermal sensing and acquired thermotolerance. Plant Cell 2012, 24:3333-3348.
35. Finkelstein R.R., Gampala S.S., Rock C.D. Abscisic acid signaling in seeds and seedlings. Plant Cell 2002, 14:S15-S45. Suppl.
36. Fragniere C., Serrano M., Abou-Mansour E., Metraux J.P., L'Haridon F. Salicylic acid and its location in response to biotic and abiotic stress. FEBS Lett. 2011, 585:1847-1852.
37. Fujii H., et al. In vitro reconstitution of an abscisic acid signalling pathway. Nature 2009, 462:660-664.
38. Fujita M., Fujita Y., Noutoshi Y., Takahashi F., Narusaka Y., Yamaguchi-Shinozaki K., Shinozaki K. Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr. Opin. Plant Biol. 2006, 9:436-442.
39. Gadjev I., Vanderauwera S., Gechev T.S., Laloi C., Minkov I.N., Shulaev V., Apel K., Inze D., Mittler R., Van Breusegem F. Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol. 2006, 141:436-445.
40. Geiger D., Scherzer S., Mumm P., Stange A., Marten I., Bauer H., Ache P., Matschi S., Liese A., Al-Rasheid K.A., Romeis T., Hedrich R. Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair. Proc. Natl. Acad. Sci. U S A 2009, 106:21425-21430.
41. Grigorova B., Vaseva I., Demirevska K., Feller U. Combined drought and heat stress in wheat: changes in some heat shock proteins. Biol. Plant. 2011, 55:105-111.
42. Gupta D., Tuteja N. Chaperones and foldases in endoplasmic reticulum stress signaling in plants. Plant Signal Behav. 2011, 6:232-236.
43. Hafren A., Hofius D., Ronnholm G., Sonnewald U., Makinen K. HSP70 and its cochaperone CPIP promote potyvirus infection in Nicotiana benthamiana by regulating viral coat protein functions. Plant Cell 2010, 22:523-535.
44. Hammond-Kosack K.E., Jones J.D.G. Response to plant pathogens. Biochemistry and Molecular Biology of Plants 2000, 1102-1157. American Society of Plant Physiologists, Rockville, MD. B. Buchannan, W. Gruissem, R. Jones (Eds.).
45. Hancock R.D., Morris W.L., Ducreux L.J., Morris J.A., Usman M., Verrall S.R., Fuller J., Simpson C.G., Zhang R., Hedley P.E., Taylor M.A. Physiological, biochemical and molecular responses of the potato (Solanum tuberosum L.) plant to moderately elevated temperature. Plant Cell Environ. 2014, 37:439-450.
46. Hayat S., Hayat Q., Alyemeni M.N., Wani A.S., Pichtel J., Ahmad A. Role of proline under changing environments: a review. Plant Signal Behav. 2012, 7:1456-1466.
47. Hey S.J., Byrne E., Halford N.G. The interface between metabolic and stress signalling. Ann. Bot. 2010, 105:197-203.
48. Hewezi T., Leger M., Gentzbittel L. A comprehensive analysis of the combined effects of high light and high temperature stresses on gene expression in sunflower. Ann. Bot. 2008, 102:127-140.
49. Hirayama T., Shinozaki K. Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant J.: Cell Mol. Biol. 2010, 61:1041-1052.
50. Horvath I., Glatz A., Nakamoto H., Mishkind M.L., Munnik T., Saidi Y., Goloubinoff P., Harwood J.L., Vigh L. Heat shock response in photosynthetic organisms: membrane and lipid connections. Prog. Lipid Res. 2012, 51:208-220.
51. Howell S.H. Endoplasmic reticulum stress responses in plants. Annu. Rev. Plant Biol. 2013, 64:477-499.
52. Huang G.T., Ma S.L., Bai L.P., Zhang L., Ma H., Jia P., Liu J., Zhong M., Guo Z.F. Signal transduction during cold, salt, and drought stresses in plants. Mol. Biol. Rep. 2012, 39:969-987.
53. Huang T.L., Huang H.J. ROS and CDPK-like kinase-mediated activation of MAP kinase in rice roots exposed to lead. Chemosphere 2008, 71:1377-1385.
54. Hubbard K.E., Nishimura N., Hitomi K., Getzoff E.D., Schroeder J.I. Early abscisic acid signal transduction mechanisms: newly discovered components and newly emerging questions. Genes Dev. 2010, 24:1695-1708.
55. Iba K. Acclimative response to temperature stress in higher plants: approaches of gene engineering for temperature tolerance. Annu. Rev. Plant Biol. 2002, 53:225-245.
56. Jan A.T., Singhal P., Mohd Q., Haq R. Plant abiotic stress: deciphering remedial strategies for emerging problem. J. Plant Interact. 2013, 8:97-108.
57. Jelenska J., van Hal J.A., Greenberg J.T. Pseudomonas syringae hijacks plant stress chaperone machinery for virulence. Proc. Natl. Acad. Sci. U S A 2010, 107:13177-13182.
58. Jiang Y., Liang G., Yang S., Yu D. Arabidopsis WRKY57 functions as a node of convergence for jasmonic acid- and auxin-mediated signaling in jasmonic acid-induced leaf senescence. Plant Cell 2014, 26:230-245.
59. Jiang Y., Liang G., Yu D. Activated expression of WRKY57 confers drought tolerance in Arabidopsis. Mol. Plant 2012, 5:1375-1388.
60. Jones R.W., Jackson A.O., Morris T.J. Defective-interfering RNAs and elevated temperatures inhibit replication of tomato bushy stunt virus in inoculated protoplasts. Virology 1990, 176:539-545.
61. Joshi-Saha A., Valon C., Leung J. A brand new START: abscisic acid perception and transduction in the guard cell. Sci. Signal. 2011, 4. re4.
62. Kant P., Gordon M., Kant S., Zolla G., Davydov O., Heimer Y.M., Chalifa-Caspi V., Shaked R., Barak S. Functional-genomics-based identification of genes that regulate Arabidopsis responses to multiple abiotic stresses. Plant Cell Environ. 2008, 31:697-714.
63. Kilian J., Whitehead D., Horak J., Wanke D., Weinl S., Batistic O., D'Angelo C., Bornberg-Bauer E., Kudla J., Harter K. The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J.: Cell Mol. Biol. 2007, 50:347-363.
64. Kim T.H., Bohmer M., Hu H., Nishimura N., Schroeder J.I. Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annu. Rev. Plant Biol. 2010, 61:561-591.
65. Kim T.H., Hauser F., Ha T., Xue S., Bohmer M., Nishimura N., Munemasa S., Hubbard K., Peine N., Lee B.H., Lee S., Robert N., Parker J.E., Schroeder J.I. Chemical genetics reveals negative regulation of abscisic acid signaling by a plant immune response pathway. Curr. Biol.: CB 2011, 21:990-997.
66. Kiraly L., Hafez Y.M., Fodor J., Kiraly Z. Suppression of tobacco mosaic virus-induced hypersensitive-type necrotization in tobacco at high temperature is associated with downregulation of NADPH oxidase and superoxide and stimulation of dehydroascorbate reductase. J. Gen. Virol. 2008, 89:799-808.
67. Kissoudis C., van de Wiel C., Visser R.G.F., van der Linden G. Enhancing crop resilience to combined abiotic and biotic stress through the dissection of physiological and molecular crosstalk. Front. Plant Sci. 2014, 5:207.
68. Krasensky J., Jonak C. Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J. Exp. Bot. 2012, 63:1593-1608.
69. Kreps J.A., Wu Y., Chang H.S., Zhu T., Wang X., Harper J.F. Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol. 2002, 130:2129-2141.
70. Kumar M., Busch W., Birke H., Kemmerling B., Nurnberger T., Schoffl F. Heat shock factors HsfB1 and HsfB2b are involved in the regulation of Pdf1.2 expression and pathogen resistance in Arabidopsis. Mol. Plant 2009, 2:152-165.
71. Kumar S.V., Wigge P.A. H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 2010, 140:136-147.
72. Larkindale J., Knight M.R. Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol. 2002, 128:682-695.
73. Lawlor D.W. Genetic engineering to improve plant performance under drought: physiological evaluation of achievements, limitations, and possibilities. J. Exp. Bot. 2013, 64:83-108.
74. Lastdrager J., Hanson J., Smeekens S. Sugar signals and the control of plant growth and development. J. Exp. Bot. 2014, 65:799-807.
75. Lecourieux D., Ranjeva R., Pugin A. Calcium in plant defence-signalling pathways. New Phytol. 2006, 171:249-269.
76. Lee S.C., Lan W., Buchanan B.B., Luan S. A protein kinase-phosphatase pair interacts with an ion channel to regulate ABA signaling in plant guard cells. Proc. Natl. Acad. Sci. U S A 2009, 106:21419-21424.
77. Liu H.T., Gao F., Li G.L., Han J.L., Liu D.L., Sun D.Y., Zhou R.G. The calmodulin-binding protein kinase 3 is part of heatshocksignal transduction in Arabidopsis thaliana. Plant J. 2008, 55:760-773.
78. Ma Y., Szostkiewicz I., Korte A., Moes D., Yang Y., Christmann A., Grill E. Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 2009, 324:1064-1068.
79. Licausi F., Ohme-Takagi M., Perata P. APETALA2/Ethylene Responsive Factor (AP2/ERF) transcription factors: mediators of stress responses and developmental programs. New Phytol. 2013, 199:639-649.
80. Lindemose S., O'Shea C., Jensen M.K., Skriver K. Structure, function and networks of transcription factors involved in abiotic stress responses. Int. J. Mol. Sci. 2013, 14:5842-5878.
81. Liu H.C., Charng Y.Y. Common and distinct functions of Arabidopsis class A1 and A2 heat shock factors in diverse abiotic stress responses and development. Plant Physiol. 2013, 163:276-290.
82. Lobell D.B., Schlenker W., Costa-Roberts J. Climate trends and global crop production since 1980. Science 2011, 333:616-620.
83. Marti M.C., Stancombe M.A., Webb A.A. Cell- and stimulus type-specific intracellular free Ca2+ signals in Arabidopsis. Plant Physiol. 2013, 163:625-634.
84. Mazzucotelli E., Mastrangelo A.M., Crosatti C., Guerra D., Stanca A.M., Cattivelli L. Abiotic stress response in plants: when post-transcriptional and post-translational regulations control transcription. Plant Sci. 2008, 174:420-431.
85. Meijer H.J., Munnik T. Phospholipid-based signaling in plants. Annu. Rev. Plant Biol. 2003, 54:265-306.
86. Miller G., Mittler R. Could heat shock transcription factors function as hydrogen peroxide sensors in plants?. Ann. Bot. 2006, 98:279-288.
87. Mir R.R., Zaman-Allah M., Sreenivasulu N., Trethowan R., Varshney R.K. Integrated genomics, physiology and breeding approaches for improving drought tolerance in crops. Theor. Appl. Genet. (Theoretische und angewandte Genetik) 2012, 125:625-645.
88. Mittal D., Madhyastha D.A., Grover A. Gene expression analysis in response to low and high temperature and oxidative stresses in rice: combination of stresses evokes different transcriptional changes as against stresses applied individually. Plant Sci. 2012, 197:102-113.
89. Mittler R. Abiotic stress, the field environment and stress combination. Trends Plant Sci. 2006, 11:15-19.
90. Mittler R., Blumwald E. Genetic engineering for modern agriculture: challenges and perspectives. Annu. Rev. Plant Biol. 2010, 61:443-462.
91. Mittler R., Finka A., Goloubinoff P. How do plants feel the heat?. Trends Biochem. Sci. 2012, 37:118-125.
92. Miyazono K., Miyakawa T., Sawano Y., Kubota K., Kang H.J., Asano A., Miyauchi Y., Takahashi M., Zhi Y., Fujita Y., Yoshida T., Kodaira K.S., Yamaguchi-Shinozaki K., Tanokura M. Structural basis of abscisic acid signalling. Nature 2009, 462:609-614.
93. Mustilli A.C., Merlot S., Vavasseur A., Fenzi F., Giraudat J. Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell 2002, 14:3089-3099.
94. Mohr P.G., Cahill D.M. Abscisic acid influences the susceptibility of Arabidopsis thaliana to Pseudomonas syringae pv. tomato and Peronospora parasitica. Funct. Plant Biol. 2003, 30:461-469.
95. Montillet J.L., Hirt H. New checkpoints in stomatal defense. Trends Plant Sci. 2013, 18:295-297.
96. Moury B., Selassie K.G., Marchoux G., Daubèze A., Palloix A. High temperature effects on hypersensitive resistance to Tomato Spotted wilt Tospovirus (TSWV) in pepper (Capsicum chinense Jacq.). Eur. J. Plant Pathol. 1998, 104:489-498.
97. Munne-Bosch S., Muller M. Hormonal cross-talk in plant development and stress responses. Front. Plant Sci. 2013, 4:529.
98. Munnik T., Testerink C. Plant phospholipid signaling: in a nutshell. J. Lipid Res. 2009, 50(Suppl):S260-S265.
99. Navarro C., Abelenda J.A., Cruz-Oro E., Cuellar C.A., Tamaki S., Silva J., Shimamoto K., Prat S. Control of flowering and storage organ formation in potato by FLOWERING LOCUS T. Nature 2011, 478:119-122.
100. Negi J., Matsuda O., Nagasawa T., Oba Y., Takahashi H., Kawai-Yamada M., Uchimiya H., Hashimoto M., Iba K. CO2 regulator SLAC1 and its homologues are essential for anion homeostasis in plant cells. Nature 2008, 452:483-486.
101. Nishizawa A., Yabuta Y., Yoshida E., Maruta T., Yoshimura K., Shigeoka S. Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. Plant J.: Cell Mol. Biol. 2006, 48:535-547.
102. Noctor G., Arisi A.C., Jouanin L., Foyer C.H. Manipulation of glutathione and amino acid biosynthesis in the chloroplast. Plant Physiol. 1998, 118:471-482.
103. Noel L.D., Cagna G., Stuttmann J., Wirthmuller L., Betsuyaku S., Witte C.P., Bhat R., Pochon N., Colby T., Parker J.E. Interaction between SGT1 and cytosolic/nuclear HSC70 chaperones regulates Arabidopsis immune responses. Plant Cell 2007, 19:4061-4076.
104. Nover L., Bharti K., Doring P., Mishra S.K., Ganguli A., Scharf K.D. Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need?. Cell Stress Chaperones 2001, 6:177-189.
105. Pan Z., Zhao Y., Zheng Y., Liu J., Jiang X., Guo Y. A high-throughput method for screening Arabidopsis mutants with disordered abiotic stress-induced calcium signal. J. Genet. Genomics=Yi chuan xue bao 2012, 39:225-235.
106. Pandey S., Nelson D.C., Assmann S.M. Two novel GPCR-type;1; G proteins are abscisic acid receptors in Arabidopsis. Cell 2009, 136:136-148.
107. Park S.Y., Fung P., Nishimura N., Jensen D.R., Fujii H., Zhao Y., Lumba S., Santiago J., Rodrigues A., Chow T.F., Alfred S.E., Bonetta D., Finkelstein R., Provart N.J., Desveaux D., Rodriguez P.L., McCourt P., Zhu J.K., Schroeder J.I., Volkman B.F., Cutler S.R. Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 2009, 324:1068-1071.
108. Prasch C.M., Sonnewald U. Simultaneous application of heat, drought, and virus to Arabidopsis plants reveals significant shifts in signaling networks. Plant Physiol. 2013, 162:1849-1866.
109. Qu A.L., Ding Y.F., Jiang Q., Zhu C. Molecular mechanisms of the plant heat stress response. Biochem. Biophys. Res. Commun. 2013, 432:203-207.
110. Raghavendra A.S., Gonugunta V.K., Christmann A., Grill E. ABA perception and signalling. Trends Plant Sci. 2010, 15:395-401.
111. Ramakrishna A., Ravishankar G.A. Influence of abiotic stress signals on secondary metabolites in plants. Plant Signal Behav. 2011, 6:1720-1731.
112. Rasmussen S., Barah P., Suarez-Rodriguez M.C., Bressendorff S., Friis P., Costantino P., Bones A.M., Nielsen H.B., Mundy J. Transcriptome responses to combinations of stresses in Arabidopsis. Plant Physiol. 2013, 161:1783-1794.
113. Reddy A.S., Ali G.S., Celesnik H., Day I.S. Coping with stresses: roles of calcium- and calcium/calmodulin-regulated gene expression. Plant Cell 2011, 23:2010-2032.
114. Reguera M., Peleg Z., Blumwald E. Targeting metabolic pathways for genetic engineering abiotic stress-tolerance in crops. Biochim. Biophys. Acta 2012, 1819:186-194.
115. Rivas-San Vicente M., Plasencia J. Salicylic acid beyond defence: its role in plant growth and development. J. Exp. Bot. 2011, 62:3321-3338.
116. Rivero R.M., Mestre T.C., 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):1059-1073.
117. Rizhsky L., Liang H., Mittler R. The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiol. 2002, 130:1143-1151.
118. Rizhsky L., Liang H., Shuman J., Shulaev V., Davletova S., Mittler R. When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol. 2004, 134:1683-1696.
119. Rodriguez M.C., Petersen M., Mundy J. Mitogen-activated protein kinase signaling in plants. Annu. Rev. Plant Biol. 2010, 61:621-649.
120. Saidi Y., Finka A., Muriset M., Bromberg Z., Weiss Y.G., Maathuis F.J., Goloubinoff P. The heat shock response in moss plants is regulated by specific calcium-permeable channels in the plasma membrane. Plant Cell 2009, 21:2829-2843.
121. Sakuma Y., Maruyama K., Osakabe Y., Qin F., Seki M., Shinozaki K., Yamaguchi-Shinozaki K. Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell 2006, 18:1292-1309.
122. Sangwan V., Orvar B.L., Beyerly J., Hirt H., Dhindsa R.S. Opposite changes in membrane fluidity mimic cold and heat stress activation of distinct plant MAP kinase pathways. Plant J.: Cell Mol. Biol. 2002, 31:629-638.
123. Santiago J., Rodrigues A., Saez A., Rubio S., Antoni R., Dupeux F., Park S.Y., Marquez J.A., Cutler S.R., Rodriguez P.L. Modulation of drought resistance by the abscisic acid receptor PYL5 through inhibition of clade A PP2Cs. Plant J.: Cell Mol. Biol. 2009, 60:575-588.
124. Santino A., Taurino M., De Domenico S., Bonsegna S., Poltronieri P., Pastor V., Flors V. Jasmonate signaling in plant development and defense response to multiple (a)biotic stresses. Plant Cell Rep. 2013, 32:1085-1098.
125. Sato A., Sato Y., Fukao Y., Fujiwara M., Umezawa T., Shinozaki K., Hibi T., Taniguchi M., Miyake H., Goto D.B., Uozumi N. 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. Biochem. J. 2009, 424:439-448.
126. Scharf K.D., Berberich T., Ebersberger I., Nover L. The plant heat stress transcription factor (Hsf) family: structure, function and evolution. Biochim. Biophys. Acta 2012, 1819:104-119.
127. Schramm F., Larkindale J., Kiehlmann E., Ganguli A., Englich G., Vierling E., von Koskull-Doring P. A cascade of transcription factor DREB2A and heat stress transcription factor HsfA3 regulates the heat stress response of Arabidopsis. Plant J.: Cell Mol. Biol. 2008, 53:264-274.
128. Seki M., Ishida J., Narusaka M., Fujita M., Nanjo T., Umezawa T., Kamiya A., Nakajima M., Enju A., Sakurai T., Satou M., Akiyama K., Yamaguchi-Shinozaki K., Carninci P., Kawai J., Hayashizaki Y., Shinozaki K. Monitoring the expression pattern of around 7,000 Arabidopsis genes under ABA treatments using a full-length cDNA microarray. Funct. Integr. Genomics 2002, 2:282-291.
129. Senaratna T., Touchell D., Bunn E., Dixon K. Acetyl salicylic acid (Aspirin) and salicylic acid induce multiple stress tolerance in bean and tomato plants. Plant Growth Regulation 2000, 30:157-161.
130. Seo P.J., Kim M.J., Song J.S., Kim Y.S., Kim H.J., Park C.M. Proteolytic processing of an Arabidopsis membrane-bound NAC transcription factor is triggered by cold-induced changes in membrane fluidity. Biochem. J. 2010, 427:359-367.
131. Sewelam N., Oshima Y., Mitsuda N., Ohme-Takagi M. A step towards understanding plant responses to multiple environmental stresses: a genome-wide study. Plant Cell Environ. 2014, 10.1111/pce.12274.
132. Shaik R., Ramakrishna W. Genes and co-expression modules common to drought and bacterial stress responses in Arabidopsis and rice. PloS One 2013, 8:e77261.
133. Shang Y., Yan L., Liu Z.Q., Cao Z., Mei C., Xin Q., Wu F.Q., Wang X.F., Du S.Y., Jiang T., Zhang X.F., Zhao R., Sun H.L., Liu R., Yu Y.T., Zhang D.P. The Mg-chelatase H subunit of Arabidopsis antagonizes a group of WRKY transcription repressors to relieve ABA-responsive genes of inhibition. Plant Cell 2010, 22:1909-1935.
134. Sharma R., De Vleesschauwer D., Sharma M.K., Ronald P.C. Recent advances in dissecting stress-regulatory crosstalk in rice. Mol. Plant 2013, 6:250-260.
135. Shen Y.Y., Wang X.F., Wu F.Q., Du S.Y., Cao Z., Shang Y., Wang X.L., Peng C.C., Yu X.C., Zhu S.Y., Fan R.C., Xu Y.H., Zhang D.P. The Mg-chelatase H subunit is an abscisic acid receptor. Nature 2006, 443:823-826.
136. Siegel R.S., Xue S., Murata Y., Yang Y., Nishimura N., Wang A., Schroeder J.I. Calcium elevation-dependent and attenuated resting calcium-dependent abscisic acid induction of stomatal closure and abscisic acid-induced enhancement of calcium sensitivities of S-type anion and inward-rectifying K channels in Arabidopsis guard cells. Plant J.: Cell Mol. Biol. 2009, 59:207-220.
137. Shinozaki K., Yamaguchi-Shinozaki K. Gene networks involved in drought stress response and tolerance. J. Exp. Bot. 2007, 58:221-227.
138. Smith A.M., Stitt M. Coordination of carbon supply and plant growth. Plant Cell Environ. 2007, 30:1126-1149.
139. Sreenivasulu N., Harshavardhan V.T., Govind G., Seiler C., Kohli A. Contrapuntal role of ABA: does it mediate stress tolerance or plant growth retardation under long-term drought stress?. Gene 2012, 506:265-273.
140. Sreenivasulu N., Sopory S.K., Kavi Kishor P.B. Deciphering the regulatory mechanisms of abiotic stress tolerance in plants by genomic approaches. Gene 2007, 388:1-13.
141. Sugio A., Dreos R., Aparicio F., Maule A.J. The cytosolic protein response as a subcomponent of the wider heat shock response in Arabidopsis. Plant Cell 2009, 21:642-654.
142. Sunkar R., Chinnusamy V., Zhu J., Zhu J.K. Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci. 2007, 12:301-309.
143. Suzuki N., Rivero R.M., Shulaev V., Blumwald E., Mittler R. Abiotic and biotic stress combinations. New Phytol. 2014.
144. Suzuki N., Rizhsky L., Liang H., Shuman J., Shulaev V., Mittler R. Enhanced tolerance to environmental stress in transgenic plants expressing the transcriptional coactivator multiprotein bridging factor 1c. Plant Physiol. 2005, 139:1313-1322.
145. Suzuki N., Sejima H., Tam R., Schlauch K., Mittler R. Identification of the MBF1 heat-response regulon of Arabidopsis thaliana. Plant J.: Cell Mol. Biol. 2011, 66:844-851.
146. Swindell W.R. The association among gene expression responses to nine abiotic stress treatments in Arabidopsis thaliana. Genetics 2006, 174:1811-1824.
147. Tian D., Traw M.B., Chen J.Q., Kreitman M., Bergelson J. Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 2003, 423:74-77.
148. Tran L.S., Nakashima K., Sakuma Y., Simpson S.D., Fujita Y., Maruyama K., Fujita M., Seki M., Shinozaki K., Yamaguchi-Shinozaki K. Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell 2004, 16:2481-2498.
149. Umezawa T., Sugiyama N., Mizoguchi M., Hayashi S., Myouga F., Yamaguchi-Shinozaki K., Ishihama Y., Hirayama T., Shinozaki K. Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis. Proc. Natl. Acad. Sci. U S A 2009, 106:17588-17593.
150. Vacca R.A., de Pinto M.C., Valenti D., Passarella S., Marra E., De Gara L. Production of reactive oxygen species, alteration of cytosolic ascorbate peroxidase, and impairment of mitochondrial metabolism are early events in heat shock-induced programmed cell death in tobacco Bright-Yellow 2 cells. Plant Physiol. 2004, 134:1100-1112.
151. Vlad F., Rubio S., Rodrigues A., Sirichandra C., Belin C., Robert N., Leung J., Rodriguez P.L., Lauriere C., Merlot S. Protein phosphatases 2C regulate the activation of the Snf1-related kinase OST1 by abscisic acid in Arabidopsis. Plant Cell 2009, 21:3170-3184.
152. von Koskull-Doring P., Scharf K.D., Nover L. The diversity of plant heat stress transcription factors. Trends Plant Sci. 2007, 12:452-457.
153. 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, 9:244-252.
154. Wang Y., Bao Z., Zhu Y., Hua J. Analysis of temperature modulation of plant defense against biotrophic microbes. Mol. Plant-Microbe Interact.: MPMI 2009, 22:498-506.
155. Whitham S.A., Quan S., Chang H.S., Cooper B., Estes B., Zhu T., Wang X., Hou Y.M. Diverse RNA viruses elicit the expression of common sets of genes in susceptible Arabidopsis thaliana plants. Plant J.: Cell Mol. Biol. 2003, 33:271-283.
156. Wilkinson S., Davies W.J. Drought, ozone, ABA and ethylene: new insights from cell to plant to community. Plant Cell Environ. 2010, 33:510-525.
157. Xiong L., Schumaker K.S., Zhu J.K. Cell signaling during cold, drought, and salt stress. Plant Cell 2002, 14(Suppl):S165-S183.
158. Xu P., Chen F., Mannas J.P., Feldman T., Sumner L.W., Roossinck M.J. Virus infection improves drought tolerance. New Phytol. 2008, 180:911-921.
159. Yasuda M., Ishikawa A., Jikumaru Y., Seki M., Umezawa T., Asami T., Maruyama-Nakashita A., Kudo T., Shinozaki K., Yoshida S., Nakashita H. Antagonistic interaction between systemic acquired resistance and the abscisic acid-mediated abiotic stress response in Arabidopsis. Plant Cell 2008, 20:1678-1692.
160. Yoshida T., Sakuma Y., Todaka D., Maruyama K., Qin F., Mizoi J., Kidokoro S., Fujita Y., Shinozaki K., Yamaguchi-Shinozaki K. Functional analysis of an Arabidopsis heat-shock transcription factor HsfA3 in the transcriptional cascade downstream of the DREB2A stress-regulatory system. Biochem. Biophys. Res. Commun. 2008, 368:515-521.
161. Wang G.P., Hui Z., Li F., Zhao M.R., Zhang J., Wang W. Improvement of heat and drought photosynthetic tolerance in wheat by overaccumulation of glycinebetaine. Plant Biotechnol. Rep. 2010, 4:213-222.
162. Wang W., Vinocur B., Altman A. Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 2003, 218:1-14.
163. 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, 9:244-252.
164. Zhang T., Liu Y., Yang T., Zhang L., Xu S., Xue L., An L. Diverse signals converge at MAPK cascades in plant. Plant Physiol. Biochem.:PPB/Soc. Fr. Physiol. Veg. 2006, 44:274-283.
165. Zhang W., Zhou R.G., Gao Y.J., Zheng S.Z., Xu P., Zhang S.Q., Sun D.Y. Molecular and genetic evidence for the key role of AtCaM3 in heat-shock signal transduction in Arabidopsis. Plant Physiol. 2009, 149:1773-1784.
166. Zhang Y., Zhu H., Zhang Q., Li M., Yan M., Wang R., Wang L., Welti R., Zhang W., Wang X. Phospholipase dalpha1 and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis. Plant Cell 2009, 21:2357-2377.
167. Zheng S.Z., Liu Y.L., Li B., Shang Z.L., Zhou R.G., Sun D.Y. Phosphoinositide-specific phospholipase C9 is involved in the thermotolerance of Arabidopsis. Plant J. 2012, 69:689-700.
168. Zhu Y., Qian W., Hua J. Temperature modulates plant defense responses through NB-LRR proteins. PLoS Pathog. 2010, 6:e1000844.