Shared and unique responses of plants to multiple individual stresses and stress combinations: Physiological and molecular mechanisms

Frontiers in Plant Science

Volumn 6, Issue September, 2015, Pages

  Pandey, Prachi ^a   Ramegowda, Venkategowda ^b,c   Senthil Kumar, Muthappa ^a  

^a NATIONAL INSTITUTE OF PLANT GENOME RESEARCH   (India)

^b UNIVERSITY OF AGRICULTURAL SCIENCES   (India)

^c UNIVERSITY OF ARKANSAS   (United States)

Author keywords

Concurrent stress; Drought; Heat; Pathogen infection; Tailored response; Unique adaptation mechanisms

Indexed keywords

EID: 84942843638     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00723     Document Type: Review

References (101)

1. Achuo, E. A., Prinsen, E., and Hofte, M. (2006). Influence of drought, salt stress and abscisic acid on the resistance of tomato to Botrytis cinérea and Oidium neolycopersici. Plant Pathol. 55, 178-186. doi: 10.1111/j.1365-3059.2006.01340.x
2. Adie, B. A. T., Pérez-Pérez, J., Pérez-Pérez, M. M., Godoy, M., Sánchez-Serrano, J.-J., Schmelz, E. A., et al. (2007). ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and the activation of defenses in Arabidopsis. Plant Cell 19, 1665-1681. doi: 10.1105/tpc.106.048041
3. Ahmed, I. M., Cao, F., Zhang, M., Chen, X., Zhang, G., and Wu, F. (2013). Difference in yield and physiological features in response to drought and salinity combined stress during anthesis in Tibetan wild and cultivated barleys. PLoS ONE 8:e77869. doi: 10.1371/journal.pone.0077869
4. Alves, A. A. C., and Setter, T. L. (2004). Response of cassava leaf area expansion to water deficit: cell proliferation, cell expansion and delayed development. Ann. Bot. 94,605-613. doi: 10.1093/aob/mch179
5. Amtmann, A., Troufflard, S., and Armengaud, P. (2008). The effect of potassium nutrition on pest and disease resistance in plants. Physiol. Plant. 133, 682-691. doi: 10.1111/j.1399-3054.2008.01075.x
6. Aprile, A., Havlickova, L., Panna, R., Mare, C., Borrelli, G. M., Marone, D., et al. (2013). Different stress responsive strategies to drought and heat in two durum wheat cultivars with contrasting water use efficiency. BMC Genomics 14:821. doi: 10.1186/1471-2164-14-821
7. Asselbergh, B., Achuo, A. E., Hofte, M., and van Gijsegem, F. (2008). Abscisic acid deficiency leads to rapid activation of tomato defence responses upon infection with Erwinia chrysanthemi. Mol. Plant Pathol. 9, 11-24. doi: 10.1111/j.1364-3703.2007.00437.x
8. Atkinson, N. J., Lilley, C. J., and Urwin, P. E. (2013). Identification of genes involved in the response to simultaneouss biotic and abiotic stress. Plant Physiol. 162, 2028-2041. doi: 10.1104/pp.113.222372
9. Atkinson, N. J., and Urwin, P. E. (2012). The interaction of plant biotic and abiotic stresses: from genes to the field. J. Exp. Bot. 63, 3523-3544. doi: 10.1093/jxb/ers100
10. Audenaert, K., De Meyer, G. B., and Hofte, M. M. (2002). Abscisic acid determines basal susceptibility of tomato to Botrytis cinerea and suppresses salicylic acid-dependent signaling mechanisms. Plant Physiol. 128, 491-501. doi: 10.1104/pp.010605
11. Awasthi, R., Kaushal, N., Vadez, V., Turner, N. C., Jens, B., Siddique, K. H. M., et al. (2014). Individual and combined effects of transient drought and heat stress on carbon assimilation and seed filling in chickpea. Funct. Plant Biol. 41, 1148-1167. doi: 10.1071/FP13340
12. Bale, J. S., Masters, G. J., Hodkinson, I. D., Awmack, C. T., Bezemer, M., Brown, V. K., et al. (2002). Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Global Change Biol. 8, 1-16. doi: 10.1046/j.1365-2486.2002.00451.x
13. Beattie, G. A. (2011). Water relations in the interaction of foliar bacterial pathogens with plants. Ann. Rev. Phytopathol. 49, 533-555. doi: 10.1146/annurev-phyto-073009-114436
14. Bos, H. J., Tijani-Eniola, H., and Struikl, P. C. (2000). Morphological analysis of leaf growth of maize: responses to temperature and light intensity. NJAS WageningenJ. LifeSci. 48,181-198. doi: 10.1016/S1573-5214(00)80013-5
15. Bostock, R. M., Pye, M. F., and Roubtsova, T. V. (2014). Predisposition in plant disease: exploiting the nexus in abiotic and biotic stress perception and response. Annu. Rev. Phytopathol. 52, 517-549. doi: 10.1146/annurev-phyto-081211-172902
16. Boyer, J. S. (1995). Biochemical and biophysical aspects of water deficits and the predisposition to disease. Annu. Rev. Phytopathol. 33, 251-274. doi: 10.1146/annurev.py.33.090195.001343
17. Bryla, D. R., Bouma, T. J., Hartmond, U., and Eissenstat, D. M. (2001). Influence of temperature and soil drying on respiration of individual roots in citrus: integrating greenhouse observations into a predictive model for the field. Plant Cell Environ. 24,781-790. doi: 10.1046/j.1365-3040.2001.00723.x
18. Chinnusamy, V., Schumaker, K., and Zhu, J. K. (2004). Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J. Exp. Bot. 55, 225-236. doi: 10.1093/jxb/erh005
19. Choi, H. K., Iandolino, A., da Silva, F. G., and Cook, D. R. (2013). Water deficit modulates the response of Vitis vinifera to the Pierce's disease pathogen Xylella fastidiosa. Mol. Plant Microbe Interact. 26, 643-657. doi: 10.1094/MPMI-09-12-0217-R
20. Choi, H. W., and Hwang, B. K. (2012). The pepper extracellular peroxidase CaPO2 is required for salt, drought and oxidative stress tolerance as well as resistance to fungal pathogens. Planta 235, 1369-1382. doi: 10.1007/s00425-011-1580-z
21. Conde, A., and Chaves, M. M. (2011). Membrane transport, sensing and signaling in plant adaptation to environmental stress. Plant Cell Physiol. 52, 1583-1602. doi: 10.1093/pcp/pcr107
22. Duniway, J. M. (1977). Predisposing effect of water stress on severity of Phytophthora root rot in safflower. Phytopathology 67, 884-889. doi: 10.1094/Phyto-67-884
23. Fonseca, S., Chico, J. M., and Solano, R. (2009). The jasmonate pathway: the ligand, the receptor and the core signalling module. Curr. Opin. Plant Biol. 12, 539-547. doi: 10.1016/j.pbi.2009.07.013
24. Galon, Y., Finkler, A., and Fromm, H. (2010). Calcium-regulated transcription in plants. Mol. Plant 3, 653-669 doi: 10.1093/mp/ssq019
25. Goel, A. K., Lundberg, D., Torres, M. A., Matthews, R., Akimoto-Tomiyama, C., Farmer, L., et al. (2008). The Pseudomonas syringae type III effector HopAM1 enhances virulence on water-stressed plants. Mol. Plant Microb. Int. 21,361-370. doi: 10.1094/MPMI-21-3-0361
26. Grigorova, B., Vassileva, V., Klimchuk, D., Vaseva, I., Demirevska, K., and Feller, U. (2012). Drought, high temperature, and their combination affect ultrastructure of chloroplasts and mitochondria in wheat (Triticum aestivum L.) leaves. J. PlantInteract. 7,204-213. doi: 10.1080/17429145.2011.654134
27. Iriti, M., Vannini, C., Carravieri, S., Genga, A., Bracale, M., and Faoro, F. (2007). "The rice Osmyb4 gene modulates the resistance to tomato mosaic virus in transformed tomato plants improving the quality traits of fruits," in Abs XIII Int Congresson Molecular Plant-Microbe Interactions(Sorrento), 282.
28. Jiang, Y., and Huang, B. (2001). Physiological responses to heat stress alone or in combination with drought: a comparison between tall fescue and perennial ryegrass. Hort Science 36, 682-686. Available online at: http://hortsci.ashspublications.org/content/36/4/682.short
29. Johnson, S. M., Lim, F.-L., Finkler, A., Fromm, H., Slabas, A. R., and Knight, M. R. (2014). Transcriptomic analysis of Sorghum bicolor responding to combined heat and drought stress. BMC Genomics 15:456. doi:10.1186/1471-2164-15-456
30. Kim, B. M., Suehiro, N., Natsuaki, T., Inukai, T., and Masuta, C. (2010). The P3 protein of turnip mosaic virus can alone induce hypersensitive response-like cell death in Arabidopsis thaliana carrying TuNI. Mol. Plant Microbe Interact. 23,144-115. doi: 10.1094/MPMI-23-2-0144
31. Kim, Y., Park, S., Gilmour, S. J., and Thomashow, M. F. (2013). Roles of CAMTA transcription factors and salicylic acid in configuring the low-temperature transcriptome and freezing tolerance of Arabidopsis. Plant J. 75, 364-376. doi: 10.1111/tpj.12205
32. Király, L., Hafez, Y. M., Fodor, J., and Király, Z. (2008). Suppression of tobacco mosaic virus-induced hypersensitive-type necrotization in tobacco at high temperature is associated with down regulation of NADPH oxidase and superoxide and stimulation of dehydroascorbate reductase. J. Gen. Virol. 89, 799-808. doi: 10.1099/vir.0.83328-0
33. Kissoudis, C., van de Wiel, C., Visser, R. G. F., and van der Linden, G. (2014). Enhancing crop resilience to combined abiotic and biotic stress through the dissection of physiological and molecular cross talk. Front. Plant Sci. 5:207. doi: 10.3389/fpls.2014.00207
34. Knight, H., and Knight, M. R. (2001). Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci. 6, 262-267. doi: 10.1016/S1360-1385(01)01946-X
35. Koga, H., Dohi, K., and Mori, M. (2004). Abscisic acid and low temperatures suppress the whole plant-specific resistance reaction of rice plants to the infection of Magnaporthe grisea. Physiol. Mol. Plant Pathol. 65, 3-9. doi: 10.1016/j.pmpp.2004.11.002
36. Krell, A., Funck, D., Plettner, I., John, U., and Dieckmann, G. (2007). Regulation of proline metabolism under salt stress in the psychrophilic diatom Fragilariopsis cylindrus (Bacillariophyceae). J. Phycol. 43, 753-762. doi: 10.1111/j.1529-8817.2007.00366.x
37. Kuwabara, C., and Imai, R. (2009). Molecular basis of disease resistance acquired through cold acclimation in overwintering plants. J. Plant Biol. 52, 19-26. doi: 10.1007/s12374-008-9006-6
38. Li, A., Wang, X., Leseberg, C. H., Jia, J., and Mao, L. (2008). Biotic and abiotic stress responses through calcium-dependent protein kinase (CDPK) signaling in wheat (Triticum aestivum L.). Plant Signal. Behav. 3, 654-656. doi: 10.4161/psb.3.9.5757
39. Li, X., Yang, Y., Sun, X., Lin, H., Chen, J., Ren, J., et al. (2014). Comparative physiological and proteomic analyses of poplar(Populusyunnanensis) plantlets exposed to high temperature and drought. PLoS ONE 9:e107605. doi: 10.1371/journal.pone.0107605
40. Luck, J., Spackman, M., Freeman, A., Trebicki, P., Griffiths, W., Finlay, K., et al. (2011). Climate change and diseases of food crops. Plant Pathol. 60, 113-121. doi: 10.1111/j.1365-3059.2010.02414.x
41. Luomala, E. M., Laitinen, K., Sutinen, S., Kellomáki, S., and Vapaavuori, E. (2005). Stomatal density, anatomy and nutrient concentrations of Scots pine needles are affected by elevated CO2 and temperature. Plant Cell Environ. 38, 733-749. doi: 10.1111/j.1365-3040.2005.01319.x
42. MacDonald, J. D. (1982). Effect of salinity stress on the development of Phytophthora root rot of chrysanthemum Chrysanthemum morifolium cultivar Paragon. Phytopathology 72, 214-219. doi: 10.1094/Phyto-72-214
43. MacDonald, J. D. (1991). Heat stress enhances Phytophthora root rot severity in container-grown chrysanthemums. J. Am. Soc. Hortic. Sci. 116, 36-41.
44. Madgwick, J. W., West, J. S., White, R. P., Semenov, M. A., Townsend, J. A., Turner, J. A., et al. (2011). Impacts of climate change on wheat anthesis and fusarium ear blight in the UK. Eur. J. Plant Pathol. 130, 117-131. doi: 10.1007/s10658-010-9739-1
45. Mahalingam, R. (ed.). (2015). "Consideration of combined stress: a crucial paradigm for improving multiple stress tolerance in plants," in Combined Stresses in Plants (Cham: Springer International Publishing), 1-25.
46. Mattson, W. J., and Haack, R. A. (1987). The role of drought in outbreaks of plant-eating insects. Bioscience 37, 110-118. doi: 10.2307/1310365
47. Mayek-Perez, N., Garcia-Espinosa, R., Lopez-Castaneda, C., Acosta-Gallegos, J. A., and Simpson, J. (2002). Water relations, histopathology and growth of common bean (Phaseolus vulgaris L.) during pathogenesis of Macrophomina phaseolina under drought stress. Physiol. Mol. Plant Pathol. 60, 185-195. doi: 10.1006/pmpp.2001.0388
48. Melotto, M., Underwood, W., Koczan, J., Nomura, K., and He, S. Y. (2006). Plant stomata function in innate immunity against bacterial invasion. Cell 126, 969-980. doi: 10.1016/j.cell.2006.06.054
49. Mengiste, T., Chen, X., Salmeron, J., and Dietrich, R. (2003). The BOTRYTIS SUSCEPTIBLE1 Gene encodes an R2R3MYB transcription factor protein that is required for biotic and abiotic stress responses in Arabidopsis. Plant Cell 15, 2551-2565. doi: 10.1105/tpc.014167
50. Mittler, R. (2006). Abiotic stress, the field environment and stress combination. Trends Plant Sci. 11, 15-19. doi: 10.1016/j.tplants.2005.11.002
51. Mittler, R., and Blumwald, E. (2010). Genetic engineering for modern agriculture: challenges and perspectives. Ann. Rev. Plant Biol. 61, 443-462. doi: 10.1146/annurev-arplant-042809-112116
52. Mohr, P. G., and Cahill, D. M. (2003). Abscisic acid influences the susceptibility of Arabidopsis thaliana to Pseudomonas syringae pv. tomato and Peronospora parasitica. Funct. Plant Biol. 30, 461-469. doi: 10.1071/FP02231
53. Moller, I. M., Jensen, P. E., and Hansson, A. (2007). Oxidative modifications to cellular components in plants. Annu. Rev. Plant Biol. 58, 459-481. doi: 10.1146/annurev.arplant.58.032806.103946
54. Moury, B., Selassie, K. G., Marchoux, G., Daubéze, A., and Palloix, A. (1998). High temperature effects on hypersensitive resistance to Tomato Spotted wilt Tospovirus (TSWV) in pepper (Capsicum chinense Jacq.). Eur. J. Plant Pathol. 104, 489-498. doi: 10.1023/A:1008618022144
55. Munns, R. (2002). Comparative physiology of salt and water stress. Plant Cell Environ. 25, 239-250. doi: 10.1046/j.0016-8025.2001.00808.x
56. Narsai, R., Wang, C., Chen, J., Wu, J., Shou, H., and Whelan, J. (2013). Antagonistic, overlapping and distinct responses to biotic stress in rice (Oryza sativa) and interactions with abiotic stress. BMC Genomics 14:93. doi: 10.1186/1471-2164-14-93
57. Nicol, J. M., Turner, S. J., Coyne, D. L., den Nijs, L., Hockland, S., and Tahna-Maafi, Z. (2011). "Current nematode threats to world agriculture," in Genomics and Molecular Genetics of Plant-Nematode Interactions, eds J. Jones, G. Gheysen, and C. Fenoll (London: Springer), 21-44. doi: 10.1007/978-94-007-0434-3_2
58. Pandey, P., Sinha, R., Mysore, K. S., and Senthil-Kumar, M. (2015). "Impact of concurrent drought stress and pathogen infection on plants," in Combined Stresses in Plants, ed R. Mahalingam (Cham: Springer International Publishing), 203-222.
59. Pitzschke, A., Schikora, A., and Hirt, H. (2009). MAPK cascade signalling networks in plant defence. Curr. Opin. Plant Biol. 12, 421-426. doi: 10.1016/j.pbi.2009.06.008
60. Plieth, C., Hansen, U., Knight, H., and Knight, M. R. (1999). Temperature sensing byplants: the primary characteristics of signal perception and calcium response. Plant J. 18,491-497. doi: 10.1046/j.1365-313X.1999.00471.x
61. Poorter, H., Niinemets, U., Poorter, L., Wright, I. J., and Villar, R. (2009). Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytol. 182,565-588. doi: 10.1111/j.1469-8137.2009.02830.x
62. Pradhan, G. P., Prasad, P. V. V., Fritz, A. K., Kirkham, M. B., and Gill, B. S. (2012). Effects of drought and high temperature stress on synthetic hexaploid wheat. Funct. Plant Biol. 39,190-198. doi: 10.1071/FP11245
63. Prasad, P. V. V., Boote, K. J., and Allen, L. H. (2006). Adverse high temperature effects on pollen viability, seed-set, seed yield and harvest index of grain-sorghum [Sorghum bicolor (L.) Moench] are more severe at elevated carbon dioxide due to higher tissue temperatures. Agric. For. Meteorol. 139, 237-251. doi: 10.1016/j.agrformet.2006.07.003
64. Prasad, P. V. V., Pisipati, S. R., Momcilovic, I., and Ristic, Z. (2011). Independent and combined effects of high temperature and drought stress during grain filling on plant yield and chloroplast EF-Tu expression in spring wheat. J. Agron. CropSci. 197,430-441. doi: 10.1111/j.1439-037X.2011.00477.x
65. Prasad, P. V. V., Staggenborg, S., and Ristic, Z. (2008). "Impacts ofdrought and/or heat stress on physiological, developmental, growth, and yield processes of crop plants" in Response of Crops to Limited Water: Understanding and Modeling Water Stress Effects on Plant Growth Processes: Advances in Agricultural Systems Modeling Series 1, eds L. R. Ahuja, V. R. Reddy, S. A. Saseendran, and Q. Yu (Madison, WI: ASA-CSSA-SSSA), 301-356.
66. Prasch, C. M., and Sonnewald, U. (2013). Simultaneous application of heat, drought, and virus to Arabidopsis plants reveals significant shifts in signaling networks. Plant Physiol. 162, 1849-1866. doi: 10.1104/pp.113.221044
67. Ramegowda, V., and Senthil-kumar, M. (2015). The interactive effects of simultaneous biotic and abiotic stresses on plants: mechanistic understanding from drought and pathogen combination. J. Plant Physiol. 176, 47-54. doi: 10.1016/j.jplph.2014.11.008
68. Ramegowda, V., Senthil-Kumar, M., Ishiga, Y., Kaundal, A., Udayakumar, M., and Mysore, K. S. (2013). Drought stress acclimation imparts tolerance to Sclerotinia sclerotiorum and Pseudomonas syringae in Nicotiana benthamiana. Int. J. Mol. Sci. 14,9497-9513. doi: 10.3390/ijms14059497
69. Rampino, P., Mita, G., Fasano, P., Maria, G., Aprile, A., Dalessandro, G., et al. (2012). Plant physiology and biochemistry novel durum wheat genes up-regulated in responseto a combination of heat and drought stress. Plant Physiol. Biochem. 56, 72-78. doi: 10.1016/j.plaphy.2012.04.006
70. Rejeb, I., Pastor, V., and Mauch-Mani, B. (2014). Plant responses to simultaneous biotic and abiotic stress: molecular mechanisms. Plants 3, 458-475. doi: 10.3390/plants3040458
71. Reusche, M., Thole, K., Janz, D., Truskina, J., Rindfleisch, S., Drübert, C., et al. (2012). Verticillium infection triggers VASCULAR-RELATED NAC DOMAIN7-dependent de novo xylem formation and enhances drought tolerance in Arabidopsis. Plant Cell. 24, 3823-3837. doi: 10.1105/tpc.112.103374
72. Rivero, R. M., Mestre, T. C., Mittler, R., Rubio, F., Garcia-Sanchez, F., and Martinez, V. (2014). The combined effect of salinity and heat reveals a specific physiological, biochemical and molecular response in tomato plants. Plant Cell Environ. 37, 1059-1073. doi: 10.1111/pce.12199
73. Rizhsky, L., Liang, H., and Mittler, R. (2002). The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiol. 130, 1143-1151. doi: 10.1104/pp.006858
74. Rizhsky, L., Liang, H., Shuman, J., Shulaev, V., Davletova, S., and Mittler, R. (2004). When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol. 134, 1683-1696. doi: 10.1104/pp.103.033431
75. Rollins, J. A., Habte, E., Templer, S. E., Colby, T., Schmidt, J., and Von Korff, M. (2013). Leaf proteome alterations in the context of physiological and morphological responses to drought and heat stress in barley (Hordeum vulgare L.). J. Exp. Bot. 64, 3201-3212. doi: 10.1093/jxb/ert158
76. Sainz, M., Díaz, P., Monza, J., and Borsani, O. (2010). Heat stress results in loss of chloroplast Cu/Zn superoxide dismutase and increased damage to photosystem II in combined drought-heat stressed Lotus japonicus. Physiol. Plant. 140, 46-56. doi: 10.1111/j.1399-3054.2010.01383.x
77. Salvucci, M. E., and Crafts-Brandner, S. J. (2004). Inhibition of photosynthesis by heat stress: the activation state ofRubisco as a limiting factor in photosynthesis. Physiol. Plant. 120,179-186. doi: 10.1111/j.0031-9317.2004.0173.x
78. Sarowar, S., Nam, E., Jin, Y., Han, S., Deok, K., Kook, B., et al. (2005). Over expression of a pepper ascorbate peroxidase-like 1 gene in tobacco plants enhances tolerance to oxidative stress and pathogens. Plant Sci. 169, 55-63. doi: 10.1016/j.plantsci.2005.02.025
79. Savin, R., and Nicolas, M. (1996). Effects of short periods of drought and high temperature on grain growth and starch accumulation of two malting barley cultivars. Aust. J. Plant Physiol. 23,201. doi: 10.1071/PP9960201
80. Sawinski, K., Mersmann, S., Robatzek, S., and Bohmer, M. (2013). Guarding the green: pathways to stomatal immunity. Mol Plant Microb Int. 26, 626-632. doi: 10.1094/MPMI-12-12-0288-CR
81. Schoeneweiss, D. F. (1975). Predisposition, stress, and plant disease. Annu. Rev. Phytopathol. 13, 193-211. doi: 10.1146/annurev.py.13.090175.001205
82. Sewelam, N., Oshima, Y., Mitsuda, N., and Ohme-Takagi, M. (2014). A step towards understanding plant responses to multiple environmental stresses: a genome-wide study. Plant Cell Environ. 37, 2024-2035. doi: 10.1111/pce.12274
83. Sharma, R. C., Duveiller, E., and Ortiz-Ferrara, G. (2007). Progress and challenge towards reducing wheat spot blotch threat in the Eastern Gangetic Plains of South Asia: is climate change already taking its toll? Field Crop Res. 103, 109-118. doi: 10.1016/j.fcr.2007.05.004
84. Smekalova, V., Doskocilova, A., Komis, G., and Samaj, J. (2014). Cross talk between secondary messengers, hormones and MAPK modules during abiotic stress signaling in plants. Biotechnol. Adv. 32, 2-11. doi: 10.1016/j.biotechadv.2013.07.009
85. Stermer, B. A., and Hammerschmidt, R. (1987). Association of heat-shock induced resistance to disease with increased accumulation of insoluble extensin and ethylene synthesis. Physiol. Mol. Plant Pathol. 31, 453-461. doi: 10.1016/0885-5765(87)90057-9
86. Suzuki, N., Koussevitzky, S., Mittler, R.O. N., and Miller, G.A.D. (2012).ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ. 35, 259-270. doi: 10.1111/j.1365-3040.2011.02336.x
87. Suzuki, N., Rivero, R.M., Shulaev, V., Blumwald, E., and Mittler, R. (2014).Tansley review Abiotic and biotic stress combinations. New Phytol. 203, 32-43. doi: 10.1111/nph.12797
88. Szucs, A., Jáger, K., Jurca, M. E., Fábián, A., Bottka, S., Zvara, Á., et al. (2010). Histological and microarray analysis of the direct effect of water shortage alone or combined with heat on early grain development in wheat (Triticum aestivum). Physiol. Plant. 140, 174-188. doi: 10.1111/j.1399-3054.2010.01394.x
89. Ton, J., Flors, V., and Mauch-Mani, B. (2009). The multifaceted role of ABA in disease resistance. Trends Plant Sci. 14, 310-317. doi: 10.1016/j.tplants.2009.03.006
90. Ton, J., and Mauch-Mani, B. (2004). Gamma-amino-butyric acid-induced resistance against necrotrophic pathogens is based on ABA-dependent priming for callose. Plant J. 38, 119-130. doi: 10.1111/j.1365-313X.2004.02028.x
91. Tuteja, N. (2007). Abscisic acid and abiotic stress signaling. Plant Signal. Behav. 2, 135-138. doi: 10.4161/psb.2.3.4156
92. Verslues, P. E., and Sharma, S. (2010). Proline metabolism and its implications for plant-environment interaction. Arabidopsis Book 8, e0140. doi: 10.1199/tab.0140
93. Vile, D., Pervent, M., Belluau, M., Vasseur, F., Bresson, J., Muller, B., et al. (2012). Arabidopsis growth under prolonged high temperature and water deficit: independent or interactive effects? Plant Cell Environ. 35, 702-718. doi: 10.1111/j.1365-3040.2011.02445.x
94. Walley, J. W., and Dehesh, K. (2010). Molecular mechanisms regulating rapid stress signaling networks in Arabidopsis. J. Integr. Plant Biol. 52, 354-359. doi: 10.1111/j.1744-7909.2010.00940.x
95. Wang, Y., Bao, Z. L., Zhu, Y., and Hua, J. (2009). Analysis of temperature modulation of plant defense against biotrophic microbes. Mol. Plant Microb. Int. 22, 498-506. doi: 10.1094/MPMI-22-5-0498
96. Wiese, J., Kranz, T., and Schubert, S. (2004). Induction of pathogen resistance in barley by abiotic stress. Plant Biol. 6,529-536. doi: 10.1055/s-2004-821176
97. Wong, H. L., and Shimamoto, K. (2009). Sending ROS on a bullet train. Sci. Signal. 2:60. doi: 10.1126/scisignal.290pe60
98. Xiong, L., and Yang, Y. (2003). Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid - inducible mitogen-activated protein kinase. Plant Cell 15, 745-759. doi: 10.1105/tpc.008714
99. Yang, X., Wen, X., Gong, H., Lu, Q., Yang, Z., Tang, Y., et al. (2007). Genetic engineering of the biosynthesis of glycinebetaine enhances thermo tolerance of photosystem II in tobacco plants. Planta 225, 719-733. doi: 10.1007/s00425-006-0380-3
100. Zhang, G., Chen, M., Li, L., Xu, Z., Chen, X., Guo, J., et al. (2009). Over expression of the soybean GmERF3 gene, an AP2/ERF type transcription factor for increased tolerances to salt, drought, and diseases in transgenic tobacco. J. Exp. Bot. 60,3781-3796. doi: 10.1093/jxb/erp214
101. Zhao, J. Q., Li, S., Jiang, T. F., Liu, Z., Zhang, W., Jian, G., et al. (2012). Chilling stress: the key predisposing factor for causing Alternaria alternata infection and leading to cotton (Gossypium hirsutum L.) leaf senescence. PLoS ONE 7: e36126. doi: 10.1371/journal.pone.0036126