Morpho-Physiological Traits and Molecular Intricacies Associated with Tolerance to Combined Drought and Pathogen Stress in Plants

  • Vadivelmurugan Irulappan
  • Muthappa Senthil-KumarEmail author


Crops in field conditions are challenged by the simultaneous occurrence of drought and pathogen stress. In the past, research was primarily focused on studying the impact of individual stresses on plants and selection of crop varieties potentially tolerant to particular stress by yield-associated morpho-physiological traits. However, several molecular responses of crop plants underlying morpho-physiological features to concurrent stresses are not similar to that of individual stresses. Certain morpho-physiological traits such as cell membrane stability, leaf water potential, stomatal movement, and root length were shown to be altered distinctly under combined stress to combat the stress condition. However, the relevance of such traits under combined stress tolerance is not precisely known. In this chapter, from the extensive literature survey, we identified several morpho-physiological changes that could be cognate with better plant performance under combined stress and represented them as traits that have potential to impart combined stress tolerance. We have comprehensively explained physiological and molecular basis for each trait and, where possible, suggested the ways to exploit the information for identification of varieties with prospective traits. Also, we proposed the need for systematically studying the underlying regulatory traits under combined stress conditions in the future.


Combined stress Drought Pathogen infection Morpho-physiological traits Combined stress tolerance 



Combined stress tolerance project at MS-K Lab is supported by the DBT—Innovative Young Biotechnologist Award (BT/09/IYBA/2015/07). VI acknowledges DBT-JRF (DBT/2015/NIPGR/430) for his Ph.D. program. Authors thank Dr. Aarti Gupta and Dr. Prachi Pandey for critical reading of the chapter.


  1. Atkinson NJ, Urwin PE (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot 63(10):3523–3543CrossRefGoogle Scholar
  2. Ayalew H, Liu H, & Yan G (2017) Identification and validation of root length QTLs for water stress resistance inhexaploid wheat (Titicum aestivum L.). Euphytica 213(6):126Google Scholar
  3. Bajji M, Kinet JM, Lutts S (2002) The use of the electrolyte leakage method for assessing cell membrane stability as a water stress tolerance test in durum wheat. Plant Growth Regul 36(1):61–70CrossRefGoogle Scholar
  4. Bernier J, Serraj R, Kumar A, Venuprasad R, Impa S, Veereshgowda RP, Oane R, Spaner D, Atlin G (2009) The large-effect drought-resistance QTL qtl12. 1 increases water uptake in upland rice. Field Crop Res 110(2):139–146CrossRefGoogle Scholar
  5. Blaker N, MacDonald J (1981) Predisposing effects of soil moisture extremes on the susceptibility of rhododendron to Phytophthora root and crown rot. Phytopathology 71(83):1–834Google Scholar
  6. Blanco-Lopez M (1983) Effect of irrigation on susceptibility of sunflower to Macrophomina phaseoli. Plant Dis 67(11):1214–1217CrossRefGoogle Scholar
  7. Blum A, Shpiler L, Golan G, Mayer J (1989) Yield stability and canopy temperature of wheat genotypes under drought-stress. Field Crop Res 22(4):289–296CrossRefGoogle Scholar
  8. Borah P, Sharma E, Kaur A, Chandel G, Mohapatra T, Kapoor S, Khurana JP (2017) Analysis of drought-responsive signalling network in two contrasting rice cultivars using transcriptome-based approach. Sci Rep 7:42131CrossRefPubMedPubMedCentralGoogle Scholar
  9. Bradley DJ, Gilbert GS, Parker IM (2003) Susceptibility of clover species to fungal infection: the interaction of leaf surface traits and environment. Am J Bot 90(6):857–864CrossRefPubMedGoogle Scholar
  10. Choi HK, Iandolino A, da Silva FG, Cook DR (2013) Water deficit modulates the response of Vitis vinifera to the Pierce's disease pathogen Xylella fastidiosa. Mol Plant-Microbe Interact 26(6):643–657CrossRefPubMedGoogle Scholar
  11. Cook R, Papendick R (1972) Influence of water potential of soils and plants on root disease. Annu Rev Phytopathol 10(1):349–374CrossRefGoogle Scholar
  12. Dossa GS, Torres R, Henry A, Oliva R, Maiss E, Cruz CV, Wydra K (2017) Rice response to simultaneous bacterial blight and drought stress during compatible and incompatible interactions. Eur J Plant Pathol 147(1):115–127CrossRefGoogle Scholar
  13. Dryden P, Van Alfen NK (1984) Soil moisture, root system density, and infection of roots of pinto beans by Fusarium solani f. Sp. phaseoli under dryland conditions. Phytopathology 74(2):132–135CrossRefGoogle Scholar
  14. Duniway J, Durbin R (1971) Detrimental effect of rust infection on the water relations of bean. Plant Physiol 48(1):69–72CrossRefPubMedPubMedCentralGoogle Scholar
  15. Ehleringer J, Björkman O, Mooney HA (1976) Leaf pubescence: effects on absorptance and photosynthesis in a desert shrub. Science 192(4237):376–377CrossRefPubMedGoogle Scholar
  16. Eyal Z, Blum A (1989) Canopy temperature as a correlative measure for assessing host response to Septoriatritici blotch of wheat. Plant Dis 73(6):468–471CrossRefGoogle Scholar
  17. Fanizza G, Ricciardi L, Bagnulo C (1991) Leaf greenness measurements to evaluate water stressed genotypes in Vitis vinifera. Euphytica 55(1):27–31CrossRefGoogle Scholar
  18. Gao Y, Lynch JP (2016) Reduced crown root number improves water acquisition under water deficit stress in maize (Zea mays L.). J Exp Bot 67(15):4545–4557CrossRefPubMedPubMedCentralGoogle Scholar
  19. González-Dugo M, Moran M, Mateos L, Bryant R (2006) Canopy temperature variability as an indicator of crop water stress severity. Irrig Sci 24(4):233–240CrossRefGoogle Scholar
  20. Govrin EM, Levine A (2000) The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr Biol 10(13):751–757CrossRefPubMedGoogle Scholar
  21. Grammatikopoulos G, Manetas Y (1994) Direct absorption of water by hairy leaves of Phlomis fruticosa and its contribution to drought avoidance. Can J Bot 72(12):1805–1811CrossRefGoogle Scholar
  22. Grimmer MK, John Foulkes M, Paveley ND (2012) Foliar pathogenesis and plant water relations: a review. J Exp Bot 63(12):4321–4331CrossRefPubMedGoogle Scholar
  23. Gupta A, Dixit SK, Senthil-Kumar M (2016) Drought stress predominantly endures Arabidopsis thaliana to Pseudomonas syringae infection. Front Plant Sci 7:808PubMedPubMedCentralGoogle Scholar
  24. Gupta A, Senthil-Kumar M (2017) Concurrent stresses are perceived as new state of stress by the plants: overview of impact of abiotic and biotic stress combinations. In: plant tolerance to individual and concurrent stresses. Springer India, pp 1–15 New DelhiGoogle Scholar
  25. Ishiga Y, Ishiga T, Uppalapati SR, Mysore KS (2013) Jasmonate ZIM-domain (JAZ) protein regulates host and nonhost pathogen-induced cell death in tomato and Nicotianabenthamiana. PLoS One 8(9):e75728CrossRefPubMedPubMedCentralGoogle Scholar
  26. 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 J 27(4):325–333CrossRefPubMedGoogle Scholar
  27. Jäger K, Fábián A, Tompa G, Deák C, Höhn M, Olmedilla A, Barnabás B, Papp I (2011) New phenotypes of the drought-tolerant cbp20Arabidopsis thaliana mutant have changed epidermal morphology. Plant Biol 13(1):78–84CrossRefPubMedGoogle Scholar
  28. Jenks MA, Joly RJ, Peters PJ, Rich PJ, Axtell JD, Ashworth EN (1994) Chemically induced cuticle mutation affecting epidermal conductance to water vapor and disease susceptibility in Sorghum bicolor (L.) Moench. Plant Physiol 105(4):1239–1245CrossRefPubMedPubMedCentralGoogle Scholar
  29. Jiménez-Díaz RM, Castillo P, del Mar Jiménez-Gasco M, Landa BB, Navas-Cortés JA (2015) Fusarium wilt of chickpeas: biology, ecology and management. Crop Prot 73:16–27CrossRefGoogle Scholar
  30. Kim KS, Park SH, Jenks MA (2007) Changes in leaf cuticular waxes of sesame (Sesamum indicum L.) plants exposed to water deficit. J Plant Physiol 164(9):1134–1143CrossRefPubMedGoogle Scholar
  31. Korves TM, Bergelson J (2003) A developmental response to pathogen infection in Arabidopsis. Plant Physiol 133(1):339–347CrossRefPubMedPubMedCentralGoogle Scholar
  32. Kosma DK, Bourdenx B, Bernard A, Parsons EP, Lü S, Joubès J, Jenks MA (2009) The impact of water deficiency on leaf cuticle lipids of Arabidopsis. Plant Physiol 151(4):1918–1929CrossRefPubMedPubMedCentralGoogle Scholar
  33. Kroumova AB, Shepherd RW, Wagner GJ (2007) Impacts of T-Phylloplanin gene knockdown and of Helianthus and Datura phylloplanins on Peronospora tabacina spore germination and disease potential. Plant Physiol 144(4):1843–1851CrossRefPubMedPubMedCentralGoogle Scholar
  34. Lai A, Cianciolo V, Chiavarini S, Sonnino A (2000) Effects of glandular trichomes on the development of Phytophthora infestans infection in potato (S. tuberosum). Euphytica 114(3):165–174CrossRefGoogle Scholar
  35. Landa BB, Navas-Cortés JA, Jiménez-Díaz RM (2004) Integrated management of fusarium wilt of chickpea with sowing date, host resistance, and biological control. Phytopathology 94(9):946–960CrossRefPubMedGoogle Scholar
  36. Liu X, Liu C (2016) Effects of drought-stress on fusarium crown rot development in barley. PLoS One 11(12):e0167304CrossRefPubMedPubMedCentralGoogle Scholar
  37. Loarce Y, Navas E, Paniagua C, Fominaya A, Manjón JL, Ferrer E (2016) Identification of genes in a partially resistant genotype of Avenasativa expressed in response to Puccinia coronata infection. Front Plant Sci 7:731CrossRefPubMedPubMedCentralGoogle Scholar
  38. Lopez F, Chauhan Y, Johansen C (1997) Effects of timing of drought stress on leaf area development and canopy light interception of short-duration pigeonpea. J Agron Crop Sci 178(1):1–7CrossRefGoogle Scholar
  39. Mahalakshmi V, Bidinger F (1985) Flowering response of pearl millet to water stress during panicle development. Ann Appl Biol 106(3):571–578CrossRefGoogle Scholar
  40. Manjarrez-Sandoval P, González-Hernández VA, Mendoza-Onofre LE, Engleman E (1989) Drought stress effects on the grain yield and panicle development of sorghum. Can J Plant Sci 69(3):631–641CrossRefGoogle Scholar
  41. Marcell LM, Beattie GA (2002) Effect of leaf surface waxes on leaf colonization by Pantoeaagglomerans and Clavibacter michiganensis. Mol Plant-Microbe Interact 15(12):1236–1244CrossRefPubMedGoogle Scholar
  42. Mayek-Pérez N, GarcÍa-Espinosa R, López-Castañeda C, Acosta-Gallegos JA, 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(4):185–195CrossRefGoogle Scholar
  43. McElrone AJ, Sherald JL, Forseth IN (2001) Effects of water stress on symptomatology and growth of Parthenocissus quinquefolia infected by Xylella fastidiosa. Plant Dis 85(11):1160–1164CrossRefGoogle Scholar
  44. McElrone AJ, Sherald JL, Forseth IN (2003) Interactive effects of water stress and xylem-limited bacterial infection on the water relations of a host vine. J Exp Bot 54(381):419–430CrossRefPubMedGoogle Scholar
  45. Melotto M, Underwood W, Koczan J, Nomura K, He SY (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126(5):969–980CrossRefPubMedGoogle Scholar
  46. Mohr PG, Cahill DM (2003) Abscisic acid influences the susceptibility of Arabidopsis thaliana to Pseudomonas syringaepv. tomato and Peronospora parasitica. Funct Plant Biol 30(4):461–469CrossRefGoogle Scholar
  47. Mantri NL, Ford R, Coram TE, & Pang EC (2010) Evidence of unique and shared responses to major biotic andabiotic stresses in chickpea. Environmental and experimental botany 69(3): 286–292Google Scholar
  48. Nguyen TTX, Dehne H-W, Steiner U (2016) Maize leaf trichomes represent an entry point of infection for fusarium species. Fungal Biol 120(8):895–903CrossRefPubMedGoogle Scholar
  49. Oerke E, Steiner U, Dehne H, Lindenthal M (2006) Thermal imaging of cucumber leaves affected by downy mildew and environmental conditions. J Exp Bot 57(9):2121–2132CrossRefPubMedGoogle Scholar
  50. Oren L, Ezrati S, Cohen D, Sharon A (2003) Early events in the Fusarium verticillioides-maize interaction characterized by using a green fluorescent protein-expressing transgenic isolate. Appl Environ Microbiol 69(3):1695–1701CrossRefPubMedPubMedCentralGoogle Scholar
  51. Pandey P, Irulappan V, Bagavathiannan MV, Senthil-Kumar M (2017) Impact of combined abiotic and biotic stresses on plant growth and avenues for crop improvement by exploiting physio-morphological traits. Front Plant Sci 8:537PubMedPubMedCentralGoogle Scholar
  52. Pandey P, Ramegowda V, Senthil-Kumar M (2015) Shared and unique responses of plants to multiple individual stresses and stress combinations: physiological and molecular mechanisms. Front Plant Sci 6:723CrossRefPubMedPubMedCentralGoogle Scholar
  53. Papp I, Mur L, Dalmadi A, Dulai S, Koncz C (2004) A mutation in the cap binding protein 20 gene confers drought. Plant Mol Biol 55(5):679–686CrossRefPubMedGoogle Scholar
  54. Paul N, Ayres P (1984) Effects of rust and post-infection drought on photosynthesis, growth and water relations in groundsel. Plant Pathol 33(4):561–569CrossRefGoogle Scholar
  55. Pauwels L, Goossens A (2011) The JAZ proteins: a crucial interface in the jasmonate signaling cascade. Plant Cell 23(9):3089–3100CrossRefPubMedPubMedCentralGoogle Scholar
  56. Pennypacker B, Leath K, Hill R (1991) Impact of drought stress on the expression of resistance to Verticillium albo-atrum in alfalfa. Phytopathology 81(9):1014–1024CrossRefGoogle Scholar
  57. Pétriacq P, Stassen JH, Ton J (2016) Spore density determines infection strategy by the plant pathogenic fungus Plectosphaerella cucumerina. Plant Physiol 170(4):2325–2339CrossRefPubMedPubMedCentralGoogle Scholar
  58. Pinter P, Stanghellini M, Reginato R, Idso S, Jenkins A, Jackson R (1979) Remote detection of biological stresses in plants with infrared thermometry. Science 205(4406):585–586CrossRefPubMedGoogle Scholar
  59. Prasch CM, Sonnewald U (2013) Simultaneous application of heat, drought, and virus to Arabidopsis plants reveals significant shifts in signaling networks. Plant Physiol 162(4):1849–1866CrossRefPubMedPubMedCentralGoogle Scholar
  60. Ramegowda V, 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 176:47–54CrossRefPubMedGoogle Scholar
  61. Ramegowda V, Senthil-Kumar M, Ishiga Y, Kaundal A, Udayakumar M, Mysore KS (2013) Drought stress acclimation imparts tolerance to Sclerotiniasclerotiorum and Pseudomonas syringae in Nicotianabenthamiana. Int J Mol Sci 14(5):9497–9513CrossRefPubMedPubMedCentralGoogle Scholar
  62. Ramos LJ, Volin RB (1987) Role of stomatal opening and frequency on infection of Lycopersicon spp. by Xanthomonas campestris pv. vesicatoria. Phytopathology 77(9):1311–1317CrossRefGoogle Scholar
  63. Ramu VS, Paramanantham A, Ramegowda V, Mohan-Raju B, Udayakumar M, Senthil-Kumar M (2016) Transcriptome analysis of sunflower genotypes with contrasting oxidative stress tolerance reveals individual-and combined-biotic and abiotic stress tolerance mechanisms. PLoS One 11(6):e0157522CrossRefPubMedPubMedCentralGoogle Scholar
  64. Rasmussen S, Barah P, Suarez-Rodriguez MC, Bressendorff S, Friis P, Costantino P, Mundy J (2013) Transcriptome responses to combinations of stresses in Arabidopsis. Plant Physiol 161(4):1783–1794CrossRefPubMedPubMedCentralGoogle Scholar
  65. Reis EM, Boareto C, Danelli ALD, Zoldan SM (2016) Anthesis, the infectious process and disease progress curves for fusarium head blight in wheat. Summa Phytopathol 42(2):134–139CrossRefGoogle Scholar
  66. Ristic Z, Jenks MA (2002) Leaf cuticle and water loss in maize lines differing in dehydration avoidance. J Plant Physiol 159(6):645–651CrossRefGoogle Scholar
  67. Rizhsky L, Liang H, Shuman J, Shulaev V, Davletova S, Mittler R (2004) When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 134(4):1683–1696CrossRefPubMedPubMedCentralGoogle Scholar
  68. Rojas CM, Senthil-Kumar M, Tzin V, Mysore K (2014) Regulation of primary plant metabolism during plant-pathogen interactions and its contribution to plant defense. Front Plant Sci 5:17CrossRefPubMedPubMedCentralGoogle Scholar
  69. Rolando JL, Ramírez DA, Yactayo W, Monneveux P, Quiroz R (2015) Leaf greenness as a drought tolerance related trait in potato (Solanum tuberosum L.). Environ Exp Bot 110:27–35CrossRefGoogle Scholar
  70. Sharma M, Ghosh R, Pande S (2015) Dry root rot (Rhizoctonia bataticola (Taub.) Butler): an emerging disease of chickpea–where do we stand? Arch Phytopathol Plant Protect 48(13–16):797–812CrossRefGoogle Scholar
  71. Sinha R, Gupta A, Senthil-Kumar M (2016) Understanding the impact of drought on foliar and xylem invading bacterial pathogen stress in chickpea. Front Plant Sci 7:902PubMedPubMedCentralGoogle Scholar
  72. Smith R, Heritage A, Stopper M, Barrs H (1986) Effect of stripe rust (Pucciniastriiformis west.) and irrigation on the yield and foliage temperature of wheat. Field Crop Res 14:39–51CrossRefGoogle Scholar
  73. Stark JC, Pavek JJ, McCann IR (1991) Using canopy temperature measurements to evaluate drought tolerance of potato genotypes. J Am Soc Hortic Sci 116(3):412–415Google Scholar
  74. Suzuki N, Rivero RM, Shulaev V, Blumwald E, Mittler R (2014) Abiotic and biotic stress combinations. New Phytol 203(1):32–43CrossRefPubMedGoogle Scholar
  75. Shamsudin NAA, Swamy BM, Ratnam W, Cruz MTS, Raman A, & Kumar A. (2016) Marker assisted pyramiding ofdrought yield QTLs into a popular Malaysian rice cultivar, MR219. BMC genetics, 17(1):30Google Scholar
  76. Tombesi S, Nardini A, Frioni T, Soccolini M, Zadra C, Farinelli D, Poni S, Palliotti A (2015) Stomatal closure is induced by hydraulic signals and maintained by ABA in drought-stressed grapevine. Sci Rep 5:12449CrossRefPubMedPubMedCentralGoogle Scholar
  77. Tripathy J, Zhang J, Robin S, Nguyen TT, Nguyen H (2000) QTLs for cell-membrane stability mapped in rice (Oryza sativa L.) under drought stress. TAG Theor Appl Genet 100(8):1197–1202CrossRefGoogle Scholar
  78. Turek I, Marondedze C, Wheeler JI, Gehring C, Irving HR (2014) Plant natriuretic peptides induce proteins diagnostic for an adaptive response to stress. Front Plant Sci 5:661CrossRefPubMedPubMedCentralGoogle Scholar
  79. Wagner G, Wang E, Shepherd R (2004) New approaches for studying and exploiting an old protuberance, the plant trichome. Ann Bot 93(1):3–11CrossRefPubMedPubMedCentralGoogle Scholar
  80. Wagner GJ (1991) Secreting glandular trichomes: more than just hairs. Plant Physiol 96(3):675–679CrossRefPubMedPubMedCentralGoogle Scholar
  81. Wang SG, Jia SS, Sun DZ, Hua F, Chang XP, Jing RL (2016) Mapping QTLs for stomatal density and size under drought stress in wheat (Triticum aestivum L.). J Integr Agric 15(9):1955–1967CrossRefGoogle Scholar
  82. Williams GM, Ayres PG (1981) Effects of powdery mildew and water stress on CO2 exchange in uninfected leaves of barley. Plant Physiol 68(3):527–530CrossRefPubMedPubMedCentralGoogle Scholar
  83. Winkel T, Renno J-F, Payne W (1997) Effect of the timing of water deficit on growth, phenology and yield of pearl millet (Pennisetum glaucum (L.) R. Br.) grown in Sahelian conditions. J Exp Bot 48(5):1001–1009CrossRefGoogle Scholar
  84. Wu L, Wang X, Xu R, Li H (2013) Difference between resistant and susceptible maize to systematic colonization as revealed by DsRed-labeled Fusarium verticillioides. Crop J 1(1):61–69CrossRefGoogle Scholar
  85. Yan H, Wu L, Filardo F, Yang X, Zhao X, Fu D (2017) Chemical and hydraulic signals regulate stomatal behavior and photosynthetic activity in maize during progressive drought. Acta Physiol Plant 39(6):125CrossRefGoogle Scholar
  86. Zhan A, Schneider H, Lynch J (2015) Reduced lateral root branching density improves drought tolerance in maize. Plant Physiology 168:1603–1615CrossRefPubMedPubMedCentralGoogle Scholar
  87. Zhao D, Glynn NC, Glaz B, Comstock JC, Sood S (2011) Orange rust effects on leaf photosynthesis and related characters of sugarcane. Plant Dis 95(6):640–647CrossRefGoogle Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Vadivelmurugan Irulappan
    • 1
  • Muthappa Senthil-Kumar
    • 1
    Email author
  1. 1.National Institute of Plant Genome ResearchNew DelhiIndia

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