Abstract
Plants respond to multiple simultaneous stresses in a complex manner that is different to that for individual stresses, and not merely additive. This is particularly true for concurrent biotic and abiotic stresses, which may normally elicit conflicting response mechanisms. To tailor the stress response to the exact set of environmental conditions encountered, plants employ an interacting network of signalling pathways involving hormones, transcription factors and downstream response elements. This may have the effect of increasing tolerance to one stress at the expense of another, in order to focus on the most potentially damaging stress. As responses to simultaneous biotic and abiotic stresses are non-linear, it is crucial to understand the mechanisms involved in order to develop stress-tolerant crop plants. Any such plants should then be tested under a wide range of concurrent stresses. This is increasingly important in the face of climatological change, which will alter the range of pests and pathogens, as well as exacerbating the effects of many existing abiotic stresses. This chapter examines the mechanisms by which plants respond to simultaneous biotic and abiotic stresses, highlighting the effects on agriculture, and in particular rice.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abbasi F, Onodera H, Toki S, Tanaka H, Komatsu S. OsCDPK13, a calcium-dependent protein kinase gene from rice, is induced by cold and gibberellin in rice leaf sheath. Plant Mol Biol. 2004;55(4):541–52.
Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K. Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell Online. 2003;15(1):63–78.
AbuQamar S, Luo H, Laluk K, Mickelbart MV, Mengiste T. Crosstalk between biotic and abiotic stress responses in tomato is mediated by the AIM1 transcription factor. Plant J. 2009;58(2):347–60.
Amtmann A, Troufflard S, Armengaud P. The effect of potassium nutrition on pest and disease resistance in plants. Physiol Plant. 2008;133(4):682–91.
Anderson JP, Badruzsaufari E, Schenk PM, Manners JM, Desmond OJ, Ehlert C, et al. Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell Online. 2004;16(12):3460–79.
Asano T, Hayashi N, Kobayashi M, Aoki N, Miyao A, Mitsuhara I, et al. A rice calcium-dependent protein kinase OsCPK12 oppositely modulates salt-stress tolerance and blast disease resistance. Plant J. 2012;69(1):26–36.
Asselbergh B, Curvers K, França SC, Audenaert K, Vuylsteke M, Van Breusegem F, et al. Resistance to Botrytis cinerea in sitiens, an abscisic acid-deficient tomato mutant, involves timely production of hydrogen peroxide and cell wall modifications in the epidermis. Plant Physiol. 2007;144(4):1863–77.
Asselbergh B, De Vleesschauwer D, Höfte M. Global switches and fine-tuning-ABA modulates plant pathogen defense. Mol Plant-Microbe Interact. 2008a;21(6):709–19.
Asselbergh B, Achuo AE, Höfte M, Van Gijsegem F. Abscisic acid deficiency leads to rapid activation of tomato defence responses upon infection with Erwinia chrysanthemi. Mol Plant Pathol. 2008b;9(1):11–24.
Atkinson NJ, Urwin PE. The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot. 2012;63(10):3523–43.
Atkinson NJ, Lilley CJ, Urwin PE. Identification of genes involved in the response of Arabidopsis to simultaneous biotic and abiotic stresses. Plant Physiol. 2013;162(4):2028–41.
Audebert A, Coyne D, Dingkuhn M, Plowright R. The influence of cyst nematodes (Heterodera sacchari) and drought on water relations and growth of upland rice in Côte d’Ivoire. Plant Soil. 2000;220(1–2):235–42.
Audenaert K, De Meyer GB, Höfte MM. Abscisic acid determines basal susceptibility of tomato to Botrytis cinerea and suppresses salicylic acid-dependent signaling mechanisms. Plant Physiol. 2002;128(2):491–501.
Baena-González E, Sheen J. Convergent energy and stress signaling. Trends Plant Sci. 2008;13(9):474–82.
Balass M, Cohen Y, Bar-Joseph M. Temperature-dependent resistance to downy mildew in muskmelon: structural responses. Physiol Mol Plant Pathol. 1993;43(1):11–20.
Balderas-Hernández VE, Alvarado-Rodríguez M, Fraire-Velázquez S. Conserved versatile master regulators in signalling pathways in response to stress in plants. AoB Plants. 2013;5:plt033.
Bechtold U, Albihlal WS, Lawson T, Fryer MJ, Sparrow PA, Richard F, et al. Arabidopsis HEAT SHOCK TRANSCRIPTION FACTORA1b overexpression enhances water productivity, resistance to drought, and infection. J Exp Bot. 2013;64(11):3467–81.
Bergelson J, Purrington CB. Surveying patterns in the cost of resistance in plants. Am Nat. 1996;148:536–58.
Blande JD, Holopainen JK, Niinemets Ü. Plant volatiles in polluted atmospheres: stress responses and signal degradation. Plant Cell Environ. 2014:37:1892–904.
Bourbon H-M. Comparative genomics supports a deep evolutionary origin for the large, four-module transcriptional mediator complex. Nucleic Acids Res. 2008;36(12):3993–4008.
Bray EA. Genes commonly regulated by water-deficit stress in Arabidopsis thaliana. J Exp Bot. 2004;55(407):2331–41.
Bruce TJA, Wadhams LJ, Woodcock CM. Insect host location: a volatile situation. Trends Plant Sci. 2005;10(6):269–74.
Cao Y, Song F, Goodman RM, Zheng Z. Molecular characterization of four rice genes encoding ethylene-responsive transcriptional factors and their expressions in response to biotic and abiotic stress. J Plant Physiol. 2006;163(11):1167–78.
Casteel CL, Segal LM, Niziolek OK, Berenbaum MR, Delucia EH. Elevated carbon dioxide increases salicylic acid in Glycine max. Environ Entomol. 2012;41(6):1435–42.
Chakraborty S. Potential impact of climate change on plant-pathogen interactions. Australas Plant Pathol. 2005;34(4):443–8.
Chen X-f, Gu Z-m, Liu F, Ma B-j, Zhang H-S. Molecular analysis of rice CIPKs involved in both biotic and abiotic stress responses. Rice Sci. 2011;18(1):1–9.
Choi H-K, Iandolino A, da Silva FG, Cook DR. Water deficit modulates the response of Vitis vinifera to the Pierce’s disease pathogen Xylella fastidiosa. Mol Plant Microbe Interact. 2013;26(6):643–57.
Cockfield S, Potter D. Interaction of euonymus scale (Homoptera: Diaspididae) feeding damage and severe water stress on leaf abscission and growth of Euonymus fortunei. Oecologia. 1986;71(1):41–6.
Copolovici L, Kännaste A, Remmel T, Niinemets Ü. Volatile organic compound emissions from Alnus glutinosa under interacting drought and herbivory stresses. Environ Exp Bot. 2014;100:55–63.
De Torres-Zabala M, Truman W, Bennett MH, Lafforgue G, Mansfield JW, Rodriguez Egea P, et al. Pseudomonas syringae pv. tomato hijacks the Arabidopsis abscisic acid signalling pathway to cause disease. EMBO J. 2007;26(5):1434–43.
Denancé N, Sánchez-Vallet A, Goffner D, Molina A. Disease resistance or growth: the role of plant hormones in balancing immune responses and fitness costs. Front Plant Sci. 2013;24:4.
Deyholos MK. Making the most of drought and salinity transcriptomics. Plant Cell Environ. 2010;33(4):648–54.
Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L. MYB transcription factors in Arabidopsis. Trends Plant Sci. 2010;15(10):573–81.
Eizenberg H, Colquhoun J, Mallory-Smith CA. The relationship between temperature and small broomrape (Orobanche minor) parasitism in red clover (Trifolium pratense). Weed Biol Ecol. 2004;52(5);735–741.
Eizenberg H, Hershenhorn J, Plakhine D, Kleifeld Y, Shtienberg D, Rubin B. Effect of temperature on susceptibility of sunflower varieties to sunflower broomrape (Orobanche cumana) and Egyptian broomrape (Orobanche aegyptiaca). Weed Sci. 2009;51(3):279–86.
English-Loeb GM. Plant drought stress and outbreaks of spider mites: a field test. Ecology. 1990;71:1401–11.
English-Loeb G, Stout MJ, Duffey SS. Drought stress in tomatoes: changes in plant chemistry and potential nonlinear consequences for insect herbivores. Oikos. 1997;79:456–68.
Erb M, Köllner TG, Degenhardt J, Zwahlen C, Hibbard BE, Turlings TC. The role of abscisic acid and water stress in root herbivore-induced leaf resistance. New Phytol. 2011;189(1):308–20.
Feng DX, Tasset C, Hanemian M, Barlet X, Hu J, Trémousaygue D, et al. Biological control of bacterial wilt in Arabidopsis thaliana involves abscissic acid signalling. New Phytol. 2012;194(4):1035–45.
Fischer R, Byerlee D, Edmeades GO, editors. Can technology deliver on the yield challenge to 2050. Expert meeting on how to feed the world in 2009.
Fu D, Uauy C, Distelfeld A, Blechl A, Epstein L, Chen X, et al. A kinase-START gene confers temperature-dependent resistance to wheat stripe rust. Science. 2009;323(5919):1357–60.
Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, et al. 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(4):436–42. doi:10.1016/j.pbi.2006.05.014.
Garrett K, Dendy S, Frank E, Rouse M, Travers S. Climate change effects on plant disease: genomes to ecosystems. Annu Rev Phytopathol. 2006;44:489–509.
Gaspar T, Franck T, Bisbis B, Kevers C, Jouve L, Hausman J, et al. Concepts in plant stress physiology. Application to plant tissue cultures. Plant Growth Regul. 2002;37(3):263–85.
Goel AK, Lundberg D, Torres MA, Matthews R, Akimoto-Tomiyama C, Farmer L, et al. The Pseudomonas syringae type III effector HopAM1 enhances virulence on water-stressed plants. Mol Plant-Microbe Interact. 2008;21(3):361–70.
Gregory PJ, Johnson SN, Newton AC, Ingram JS. Integrating pests and pathogens into the climate change/food security debate. J Exp Bot. 2009;60(10):2827–38.
Gu Z, Wang J, Huang J, Zhang H. Cloning and characterization of a novel rice gene family encoding putative dual-specificity protein kinases, involved in plant responses to abiotic and biotic stresses. Plant Sci. 2005;169(3):470–7.
Gupta A, Kaur N. Sugar signalling and gene expression in relation to carbohydrate metabolism under abiotic stresses in plants. J Biosci. 2005;30(5):761–76.
Gutbrodt B, Mody K, Dorn S. Drought changes plant chemistry and causes contrasting responses in lepidopteran herbivores. Oikos. 2011;120(11):1732–40.
Henfling J, Bostock R, Kuc J. Effect of abscisic acid on rishitin and lubimin accumulation and resistance to Phytophthora infestans and Cladosporium cucumerinum in potato tuber tissue slices. Phytopathology. 1980;70(11):1074–8.
Herms DA, Mattson WJ. The dilemma of plants: to grow or defend. Q Rev Biol. 1992;67:283–335.
Himanen SJ, Nerg A-M, Nissinen A, Pinto DM, Stewart CN, Poppy GM, et al. Effects of elevated carbon dioxide and ozone on volatile terpenoid emissions and multitrophic communication of transgenic insecticidal oilseed rape (Brassica napus). New Phytol. 2009;181(1):174–86.
Holopainen JK, Gershenzon J. Multiple stress factors and the emission of plant VOCs. Trends Plant Sci. 2010;15(3):176–84.
Iyer NJ, Tang Y, Mahalingam R. Integrative analysis of combined water-deficit and ozone stress in Medicago truncatula. Plant Cell Environ. 2013;36:706–20.
Jacobsen JV, Hanson AD, Chandler PC. Water stress enhances expression of an α-amylase gene in barley leaves. Plant Physiol. 1986;80(2):350–9.
Jiang C-J, Shimono M, Sugano S, Kojima M, Yazawa K, Yoshida R, et al. Abscisic acid interacts antagonistically with salicylic acid signaling pathway in rice-Magnaporthe grisea interaction. Mol Plant-Microbe Interact. 2010;23(6):791–8.
Khan MR, Khan MW. Interaction of Meloidogyne incognita and coal-smoke pollutants on tomato. Nematropica. 1996;26(1):47–56.
Koga H, Dohi K, Mori M. 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. 2004;65(1):3–9.
Koo AJK, Cooke TF, Howe GA. Cytochrome P450 CYP94B3 mediates catabolism and inactivation of the plant hormone jasmonoyl-L-isoleucine. Proc Natl Acad Sci U S A. 2011;108(22):9298–303.
Kusajima M, Yasuda M, Kawashima A, Nojiri H, Yamane H, Nakajima M, et al. Suppressive effect of abscisic acid on systemic acquired resistance in tobacco plants. J Gen Plant Pathol. 2010;76(2):161–7.
Laurie-Berry N, Joardar V, Street IH, Kunkel BN. The Arabidopsis thaliana JASMONATE INSENSITIVE 1 gene is required for suppression of salicylic acid-dependent defenses during infection by Pseudomonas syringae. Mol Plant Microbe Interact. 2006;19(7):789–800.
Leakey ADB, Ainsworth EA, Bernacchi CJ, Rogers A, Long SP, Ort DR. Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE. J Exp Bot. 2009;60(10):2859–76.
Lee SC, Luan S. ABA signal transduction at the crossroad of biotic and abiotic stress responses. Plant Cell Environ. 2012;35(1):53–60.
Lobell DB, Cassman KG, Field CB. Crop yield gaps: their importance, magnitudes, and causes. Ann Rev Environ Res. 2009;34(1):179.
Loreto F, Schnitzler J-P. Abiotic stresses and induced BVOCs. Trends Plant Sci. 2010;15(3):154–66.
Luck J, Spackman M, Freeman A, Griffiths W, Finlay K, Chakraborty S. Climate change and diseases of food crops. Plant Pathol. 2011;60(1):113–21.
Luna E, Pastor V, Robert J, Flors V, Mauch-Mani B, Ton J. Callose deposition: a multifaceted plant defense response. Mol Plant Microbe Interact. 2011;24(2):183–93.
Luo M, Liang XQ, Dang P, Holbrook CC, Bausher MG, Lee RD, et al. Microarray-based screening of differentially expressed genes in peanut in response to Aspergillus parasiticus infection and drought stress. Plant Sci. 2005;169(4):695–703.
Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, et al. Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science. 2009;324(5930):1064–8.
Maldonado AM, Doerner P, Dixon RA, Lamb CJ, Cameron RK. A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature. 2002;419(6905):399–403. [10.1038/nature00962]
Mattson WJ, Haack RA. The role of drought in outbreaks of plant-eating insects. BioScience. 1987;37(2):110–8.
Mauch-Mani B, Mauch F. The role of abscisic acid in plant-pathogen interactions. Curr Opin Plant Biol. 2005;8(4):409–14.
Maxmen A. Crop pests: under attack. Nature. [Outlook]. 2013;501(7468):S15–7.
Mayek-Perez N, GarcÍa-Espinosa R, LÓpez-CastaÑeda C, Acosta-Gallegos JA, Simpson J. Water relations, histopathology and growth of common bean (Phaseolus vulgaris L.) during pathogenesis of Macrophomina phaseolina under drought stress. Physiol Mol Plant Pathol. 2002;60(4):185–95.
Melotto M, Underwood W, Koczan J, Nomura K, He SY. Plant stomata function in innate immunity against bacterial invasion. Cell. 2006;126(5):969–80.
Mengiste T, Chen X, Salmeron J, Dietrich R. The BOTRYTIS SUSCEPTIBLE1 gene encodes an R2R3MYB transcription factor protein that is required for biotic and abiotic stress responses in Arabidopsis. Plant Cell Online. 2003;15(11):2551–65.
Miller G, Mittler R. Could heat shock transcription factors function as hydrogen peroxide sensors in plants? Ann Bot. 2006;98(2):279–88.
Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R. Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ. 2010;33(4):453–67.
Mittler R. Abiotic stress, the field environment and stress combination. Trends Plant Sci. 2006;11(1):15–9.
Mittler R, Blumwald E. Genetic engineering for modern agriculture: challenges and perspectives. Annu Rev Plant Biol. 2010;61:443–62.
Mohr PG, Cahill DM. Abscisic acid influences the susceptibility of Arabidopsis thaliana to Pseudomonas syringae pv. tomato and Peronospora parasitica. Funct Plant Biol. 2003;30(4):461–9.
Mohr PG, Cahill DM. Suppression by ABA of salicylic acid and lignin accumulation and the expression of multiple genes, in Arabidopsis infected with Pseudomonas syringae pv. tomato. Funct Integr Genomics. 2007;7(3):181–91.
Molina A, García-Olmedo F. Enhanced tolerance to bacterial pathogens caused by the transgenic expression of barley lipid transfer protein LTP2. Plant J. 1997;12(3):669–75.
Moriondo M, Giannakopoulos C, Bindi M. Climate change impact assessment: the role of climate extremes in crop yield simulation. Clim Change. 2011;104(3-4):679–701.
Nakashima K, Tran L-SP, Van Nguyen D, Fujita M, Maruyama K, Todaka D, et al. Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J. 2007;51(4):617–30.
Narusaka Y, Narusaka M, Seki M, Umezawa T, Ishida J, Nakajima M, et al. Crosstalk in the responses to abiotic and biotic stresses in Arabidopsis: analysis of gene expression in cytochrome P450 gene superfamily by cDNA microarray. Plant Mol Biol. 2004;55(3):327–42.
Németh M, Janda T, Horváth E, Páldi E, Szalai G. Exogenous salicylic acid increases polyamine content but may decrease drought tolerance in maize. Plant Sci. 2002;162(4):569–74.
Newton AC, Johnson SN, Gregory PJ. Implications of climate change for diseases, crop yields and food security. Euphytica. 2011;179(1):3–18.
Pasquali G, Biricolti S, Locatelli F, Baldoni E, Mattana M. Osmyb4 expression improves adaptive responses to drought and cold stress in transgenic apples. Plant Cell Rep. 2008;27(10):1677–86.
Peng X-x, Tang X-k, Zhou P-l, Hu Y-j, Deng X-b, He Y, et al. Isolation and expression patterns of rice WRKY82 transcription factor gene responsive to both biotic and abiotic stresses. Agric Sci China. 2011;10(6):893–901.
Pieterse CM, Leon-Reyes A, Van der Ent S, Van Wees SC. Networking by small-molecule hormones in plant immunity. Nat Chem Biol. 2009;5(5):308–16.
Prasch CM, Sonnewald U. Simultaneous application of heat, drought, and virus to Arabidopsis plants reveals significant shifts in signaling networks. Plant Physiol. 2013;162(4):1849–66.
Rasmussen S, Barah P, Suarez-Rodriguez MC, Bressendorff S, Friis P, Costantino P, et al. Transcriptome responses to combinations of stresses in Arabidopsis. Plant Physiol. 2013;161(4):1783–94.
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(4):1683–96.
Rogers A, Ainsworth EA, Leakey AD. Will elevated carbon dioxide concentration amplify the benefits of nitrogen fixation in legumes? Plant Physiol. 2009;151(3):1009–16.
Rohila JS, Yang Y. Rice mitogen-activated protein kinase gene family and its role in biotic and abiotic stress response. J Integr Plant Biol. 2007;49(6):751–9.
Runyon JB, Mescher MC, De Moraes CM. Volatile chemical cues guide host location and host selection by parasitic plants. Science. 2006;313(5795):1964–7.
Sánchez-Vallet A, López G, Ramos B, Delgado-Cerezo M, Riviere M-P, Llorente F, et al. Disruption of abscisic acid signaling constitutively activates Arabidopsis resistance to the necrotrophic fungus Plectosphaerella cucumerina. Plant Physiol. 2012;160(4):2109–24.
Santino A, Taurino M, De Domenico S, Bonsegna S, Poltronieri P, Pastor V, et al. Jasmonate signaling in plant development and defense response to multiple (a) biotic stresses. Plant Cell Rep. 2013;32(7):1085–98.
Sawinski K, Mersmann S, Robatzek S, Böhmer M. Guarding the green: pathways to stomatal immunity. Mol Plant Microbe Interact. 2013;26(6):626–32.
Scherm H. Climate change: can we predict the impacts on plant pathology and pest management? Can J Plant Pathol. 2004;26(3):267–73.
Schmidhuber J, Tubiello FN. Global food security under climate change. Proc Natl Acad Sci U S A. 2007;104(50):19703–8.
Sharma R, De Vleesschauwer D, Sharma MK, Ronald PC. Recent advances in dissecting stress-regulatory crosstalk in rice. Mol Plant. 2013;6(2):250–60.
Shimono M, Koga H, Akagi A, Hayashi N, Goto S, Sawada M, et al. Rice WRKY45 plays important roles in fungal and bacterial disease resistance. Mol Plant Pathol. 2012;13(1):83–94.
Singh P, Siva R, Gothandam KM, Babu S. Naturally existing levels of Osmyb4 gene expression in rice cultivars correlate with their reaction to fungal and bacterial pathogens. J Phytopathol. 2013;161(10):730–4.
Smit AL, Vamerali T. The influence of potato cyst nematodes (Globodera pallida) and drought on rooting dynamics of potato (Solanum tuberosum L. ). Eur J Agron. 1998;9(2–3):137–46.
Sun Y, Cao H, Yin J, Kang L, Ge F. Elevated CO2 changes the interactions between nematode and tomato genotypes differing in the JA pathway. Plant Cell Environ. 2010;33(5):729–39.
Suzuki N, Rivero RM, Shulaev V, Blumwald E, Mittler R. Abiotic and biotic stress combinations. New Phytol. 2014;203(1):32–43.
Takasaki H, Maruyama K, Kidokoro S, Ito Y, Fujita Y, Shinozaki K, et al. The abiotic stress-responsive NAC-type transcription factor OsNAC5 regulates stress-inducible genes and stress tolerance in rice. Mol Genet Genomics. 2010;284(3):173–83.
Tao Z, Liu H, Qiu D, Zhou Y, Li X, Xu C, et al. A pair of allelic WRKY genes play opposite roles in rice-bacteria interactions. Plant Physiol. 2009;151(2):936.
Tao Z, Kou Y, Liu H, Li X, Xiao J, Wang S. OsWRKY45 alleles play different roles in abscisic acid signalling and salt stress tolerance but similar roles in drought and cold tolerance in rice. J Exp Bot. 2011;62(14):4863–74.
Tariq M, Wright DJ, Bruce TJ, Staley JT. Drought and root herbivory interact to alter the response of above-ground parasitoids to aphid infested plants and associated plant volatile signals. PLoS ONE. 2013;8(7):e69013.
Ton J, Mauch-Mani B. β-amino-butyric acid-induced resistance against necrotrophic pathogens is based on ABA-dependent priming for callose. Plant J. 2004;38(1):119–30.
Ton J, Flors V, Mauch-Mani B. The multifaceted role of ABA in disease resistance. Trends Plant Sci. 2009;14(6):310–7.
Tumlinson JH. The importance of volatile organic compounds in ecosystem functioning. J Chem Ecol. 2014;40(3):212–3.
van Hulten M, Pelser M, Van Loon L, Pieterse CM, Ton J. Costs and benefits of priming for defense in Arabidopsis. Proc Natl Acad Sci U S A. 2006;103(14):5602–7.
Vannini C, Iriti M, Bracale M, Locatelli F, Faoro F, Croce P, et al. The ectopic expression of the rice Osmyb4 gene in Arabidopsis increases tolerance to abiotic, environmental and biotic stresses. Physiol Mol Plant Pathol. 2006;69(1):26–42.
Vannini C, Campa M, Iriti M, Genga A, Faoro F, Carravieri S, et al. Evaluation of transgenic tomato plants ectopically expressing the rice Osmyb4 gene. Plant Sci. 2007;173(2):231–9.
Vignols F, Wigger M, García-Garrido JM, Grellet F, Kader J-C, Delseny M. Rice lipid transfer protein (LTP) genes belong to a complex multigene family and are differentially regulated. Gene. 1997;195(2):177–86.
von Koskull-Döring P, Scharf K-D, Nover L. The diversity of plant heat stress transcription factors. Trends Plant Sci. 2007;12(10):452–7.
Vuorinen T, Nerg A-M, Holopainen JK. Ozone exposure triggers the emission of herbivore-induced plant volatiles, but does not disturb tritrophic signalling. Environ Pollut. 2004;131(2):305–11.
Wang W, Vinocur B, Altman A. Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta. 2003;218(1):1–14.
Wasilewska A, Vlad F, Sirichandra C, Redko Y, Jammes F, Valon C, et al. An update on abscisic acid signaling in plants and more…. Mol Plant. 2008;1(2):198–217.
Webb K, Ona I, Bai J, Garrett K, Mew T, Cruz V, et al. A benefit of high temperature: increased effectiveness of a rice bacterial blight disease resistance gene. New Phytol. 2010;185(2):568–76.
Xiao J, Cheng H, Li X, Xiao J, Xu C, Wang S. Rice WRKY13 regulates cross talk between abiotic and biotic stress signaling pathways by selective binding to different cis-elements. Plant Physiol. 2013;163(4):1868–82.
Yasuda M, Ishikawa A, Jikumaru Y, Seki M, Umezawa T, Asami T, et al. Antagonistic interaction between systemic acquired resistance and the abscisic acid-mediated abiotic stress response in Arabidopsis. Plant Cell Online. 2008;20(6):1678–92.
Yokotani N, Sato Y, Tanabe S, Chujo T, Shimizu T, Okada K, et al. WRKY76 is a rice transcriptional repressor playing opposite roles in blast disease resistance and cold stress tolerance. J Exp Bot. 2013a;64(16):5085–97.
Yokotani N, Ichikawa T, Kondou Y, Iwabuchi M, Matsui M, Hirochika H, et al. Role of the rice transcription factor JAmyb in abiotic stress response. J Plant Res. 2013b;126(1):131–9.
Yoshida T, Ohama N, Nakajima J, Kidokoro S, Mizoi J, Nakashima K, et al. Arabidopsis HsfA1 transcription factors function as the main positive regulators in heat shock-responsive gene expression. Mol Genet Genomics. 2011;286(5–6):321–32.
Zavala JA, Casteel CL, DeLucia EH, Berenbaum MR. Anthropogenic increase in carbon dioxide compromises plant defense against invasive insects. Proc Natl Acad Sci U S A. 2008;105(13):5129–33.
Zhang T, Liu Y, Yang T, Zhang L, Xu S, Xue L, et al. Diverse signals converge at MAPK cascades in plant. Plant Physiol Biochem. 2006;44(5):274–83.
Zhu Y, Qian W, Hua J. Temperature modulates plant defense responses through NB-LRR proteins. PLoS Pathog. 2010;6(4):e1000844.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2015 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Atkinson, N., Jain, R., Urwin, P. (2015). The Response of Plants to Simultaneous Biotic and Abiotic Stress. In: Mahalingam, R. (eds) Combined Stresses in Plants. Springer, Cham. https://doi.org/10.1007/978-3-319-07899-1_9
Download citation
DOI: https://doi.org/10.1007/978-3-319-07899-1_9
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-07898-4
Online ISBN: 978-3-319-07899-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)