Impact of combined abiotic and biotic stresses on plant growth and avenues for crop improvement by exploiting physio-morphological traits

Frontiers in Plant Science

Volumn 8, Issue , 2017, Pages

  Pandey, Prachi ^a   Irulappan, Vadivelmurugan ^a   Bagavathiannan, Muthukumar V ^b   Senthil Kumar, Muthappa ^a  

^a NATIONAL INSTITUTE OF PLANT GENOME RESEARCH   (India)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Crop production; Drought and pathogen infection; Morpho physiological traits; Productivity; Stress combinations; Stress interaction

Indexed keywords

EID: 85018620926     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2017.00537     Document Type: Review

References (117)

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 cinerea and Oidium neolycopersici. Plant Pathol. 55, 178-186. doi: 10.1111/j.1365-3059.2006.01340.x
2. Ahmed, I. M., Dai, H., Zheng, W., Cao, F., Zhang, G., Sun, D., et al. (2013). Genotypic differences in physiological characteristics in the tolerance to drought and salinity combined stress between Tibetan wild and cultivated barley. Plant Physiol. Biochem. 63, 49-60. doi: 10.1016/j.plaphy.2012.11.004
3. Aldahadha, A. M. A. (2012). Effect of Root Diseases and Drought on Water use Efficiency of Wheat. Doctoral thesis, University of New England, Armidale.
4. Allah, A. A., Shimaa, A., Zayed, B., and Gohary, A. E. (2010). The role of root system traits in the drought tolerance of rice (Oryza sativa L.). Int. J. Agric. Biol. Sci. 1, 83-87.
5. Armstrong-Cho, C., and Gossen, B. D. (2005). Impact of glandular hair exudates on infection of chickpea by Ascochyta rabiei. Can. J. Bot. 83, 22-27. doi: 10.1139/b04-147
6. 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
7. Balota, M., Rush, C. M., Payne, W. A., and Lazar, M. D. (2005). The effect of take-all disease on gas-exchange rates and biomass in two winter wheat lines with different drought response. Plant Soil 275, 337-348. doi: 10.1007/s11104-005-2680-y
8. Barnes, J. D., and Davison, A. W. (1988). The influence of ozone on the winter hardiness of Norway Spruce [Picea abies (L) Karst]. New Phytol. 108, 159-166. doi: 10.1111/j.1469-8137.1988.tb03692.x
9. Belisario, A., Maccaroni, M., Corazza, L., Balmas, V., and Valier, A. (2002). Occurrence and etiology of brown apical necrosis on Persian (English) walnut fruit. Plant Dis. 86, 599-602. doi: 10.1094/PHYTO-01-15-0029-R
10. Berta, G., Sampo, S., Gamalero, E., Massa, N., and Lemanceau, P. (2005). Suppression of Rhizoctonia root-rot of tomato by Glomus mossae BEG12 and Pseudomonas fluorescens A6RI is associated with their effect on the pathogen growth and on the root morphogenesis. Eur. J. Plant Pathol. 111, 279-288. doi: 10.1007/s10658-004-4585-7
11. Bethenod, O., Huber, L., and Slimi, H. (2001). Photosynthetic response of wheat to stress induced by Puccinia recondita and post-infection drought. Photosynthetica 39, 581-590. doi: 10.1023/A:1015664314720
12. Bloomer, R. H., Lloyd, A. M., and Symonds, V. V. (2014). The genetic architecture of constitutive and induced trichome density in two new recombinant inbred line populations of Arabidopsis thaliana: phenotypic plasticity, epistasis, and bidirectional leaf damage response. BMC Plant Biol. 14:119. doi: 10.1186/1471-2229-14-11
13. Blum, A. (2009). Effective use of water (EUW) and not water-use efficiency (WUE) is the target of crop yield improvement under drought stress. Field Crop Res. 112, 119-123. doi: 10.1016/j.fcr.2009.03.009
14. Blum, A., Shpiler, L., Golan, G., and Mayer, J. (1989). Yield stability and canopy temperature of wheat genotypes under drought-stress. Field Crop Res. 22, 289-296. doi: 10.1016/0378-4290(89)90028-2
15. Burman, U., and Lodha, S. (1996). Macrophomina phaseolina induced changes in plant water relations of resistant and susceptible cowpea genotypes. Indian Phytopathol. 49, 254-259.
16. Caffarraa, A., Rinaldia, M., Eccela, E., Rossib, V., and Pertota, I. (2012). Modelling the impact of climate change on the interaction between grapevine and its pests and pathogens: European grapevine moth and powdery mildew. Agric. Ecosyst. Environ. 148, 89-101. doi: 10.1016/j.agee.2011.11.017
17. Calo, L., García, I., Gotor, C., and Romero, L. C. (2006). Leaf hairs influence phytopathogenic fungus infection and confer an increased resistance when expressing a Trichoderma αα-1, 3-glucanase. J. Exp. Bot. 57, 3911-3920. doi: 10.1093/jxb/erl155
18. Choudhary, A., Pandey, P., and Senthil-Kumar, M. (2016). “Tailored responses to simultaneous drought stress and pathogen infection in plants,” in Drought Stress Tolerance in Plants, Vol. 1, eds M. A. Hossain, S. H. Wani, S. Bhattacharjee, D. J. Burritt, and L.-S. P. Tran (Cham: Springer International Publishing), 427-438. doi: 10.1007/978-3-319-28899-4_18
19. Coakley, S. M., Scherm, H., and Chakraborty, S. (1999). Climate change and plant disease management. Annu. Rev. Phytopathol. 37, 399-426. doi: 10.1146/annurev.phyto.37.1.399
20. Comas, L. H., Becker, S. R., Cruz, V. M. V., Byrne, P. F., and Dierig, D. A. (2013). Root traits contributing to plant productivity under drought. Front. Plant Sci. 4:442. doi: 10.3389/fpls.2013.00442
21. Cordes, R. C., and Bauman, T. T. (1984). Field competition between ivy leaf morning glory (Ipomoea hederacea) and soybeans (Glycine max). Weed Sci. 32, 364-370.
22. Crisp, P. A., Ganguly, D., Eichten, S. R., Borevitz, J. O., and Pogson, B. J. (2016). Reconsidering plant memory: intersections between stress recovery, RNA turnover, and epigenetics. Sci. Adv. 2:e1501340. doi: 10.1126/sciadv.1501340
23. Daami-Remadi, M., Souissi, A., Oun, H. B., Mansour, M., and Nasraoui, B. (2009). Salinity effects on fusarium wilt severity and tomato growth. Dyn. Soil Dyn. Plant 3, 61-69.
24. Davis, J. R., McMaster, G. M., Callihan, R. H., Garner, J. G., and McDole, R. E. (1974). The relationship of irrigation timing and soil treatments to control potato scab. Phytopathology 64, 1404-1410. doi: 10.1094/Phyto-64-1404
25. Davis, S., Bosque-Perez, N., Foote, N., Magney, T., and Eigenbrode, S. (2014). REACCH Annual Report Year 4. Available at: https://www.reacchpna.org/node/170
26. Diourte, M., Starr, J. L., Jeger, M. J., Stack, J. P., and Rosenow, D. T. (1995). Charcoal rot (Macrophomina phaseolina) resistance and the effects of water stress on disease development in sorghum. Plant Pathol. 44, 196-202. doi: 10.1111/j.1365-3059.1995.tb02729.x
27. Dow, R. L., Powell, N. L., and Porter, D. M. (1988). Effects of modification of the plant canopy environment on Sclerotinia blight of peanut. Peanut Sci. 15, 1-5. doi: 10.3146/i0095-3679-15-1-1
28. Dryden, P., and Van Alfen, N. K. (1984). Soil moisture, root system density, and infection of roots of pinto beans by Fusarium solani f. sp. phaseoli under dryland conditions. Phytopathology 74, 132-135. doi: 10.1094/Phyto-74-132
29. Duniway, J. M. (1977). Predisposing effect of water stress on the severity of Phytophthora root rot in safflower. Phytopathology 67, 884-889. doi: 10.1094/Phyto-67-884
30. Duniway, J. M., and Durbin, R. D. (1971). Detrimental effect of rust infection on the water relations of bean. Plant Physiol. 48, 69-72. doi: 10.1104/pp.48.1.69
31. Duveiller, E., Singh, R. P., and Nicol, J. M. (2007). The challenges of maintaining wheat productivity: pests, diseases and potential epidemics. Euphytica 157, 417-430. doi: 10.1007/s10681-007-9380-z
32. Enright, S. M., and Cipollini, D. (2007). Infection by powdery mildew Erysiphe cruciferarum (Erysiphaceae) strongly affects growth and fitness of Alliaria petiolata (Brassicaceae). Am. J. Bot. 94, 1813-1820. doi: 10.3732/ajb.94.11.1813
33. Eyal, Z., and Blum, A. (1989). Canopy temperature as a correlative measure for assessing host response to Septoria tritici blotch of wheat. Plant Dis. 73, 468-471. doi: 10.1094/PD-73-0468
34. Fitz Geral, J. N., Lehti-Shiu, M. D., Ingram, P. A., Deak, K. I., Biesiada, T., and Malamy, J. E. (2006). Identification of quantitative trait loci that regulate Arabidopsis root system size and plasticity. Genetics 172, 485-498. doi: 10.1534/genetics.105.047555
35. Froese, P. S., Murray, T. D., and Carter, A. H. (2016). Quantitative cephalosporium stripe disease resistance mapped in the wheat genome. Crop Sci. 56, 1586-1601. doi: 10.2135/cropsci2015.09.0568
36. Garcia, B. I. L., Sentelhas, P. C., Tapia, L. R., and Sparovek, G. (2008). Climatic risk for potato late blight in the Andes region of Venezuela. Sci. Agric. 65, 32-39. doi: 10.1590/S0103-90162008000700007
37. Garrett, K. A., Dendy, S. P., Frank, E. E., Rouse, M. N., and Travers, S. E. (2006). Climate change effects on plant disease: genomes to ecosystems. Annu. Rev. Phytopathol. 44, 489-509. doi: 10.1146/annurev.phyto.44.070505.143420
38. Giuliani, S., Sanguineti, M. C., Tuberosa, R., Bellotti, M., Salvi, S., and Landi, P. (2005). Root-ABA1, a major constitutive QTL, affects maize root architecture and leaf ABA concentration at different water regimes. J. Exp. Bot. 56, 3061-3070. doi: 10.1093/jxb/eri303
39. Gonzalez-Dugo, M. P., Moran, M. S., Mateos, L., and Bryant, R. (2005). Canopy temperature variability as an indicator of crop water stress severity. Irrigation Sci. 24, 233-240. doi: 10.1007/s00271-005-0022-8
40. Goudarzi, S., Banihashemi, Z., and Maftoun, M. (2011). Effect of salt and water stress on root infection by Macrophomina phaseolina and ion composition in shoot in sorghum. Iran J. Plant Pathol. 47, 69-83.
41. Grammatikopoulos, G., and Manetas, Y. (1994). Direct absorption of water by hairy leaves of Phlomis fruticosa and its contribution to drought avoidance. Can. J. Bot. 72, 1805-1811. doi: 10.1139/b94-222
42. Gupta, A., Dixit, S. K., and Senthil-Kumar, M. (2016). Drought stress predominantly endures Arabidopsis thaliana to Pseudomonas syringae infection. Front. Plant Sci. 7:808. doi: 10.3389/fpls.2016.00808
43. Hagerty, C. H., Cuesta-Marcos, A., Cregan, P. B., Song, Q., McClean, P., Noffsinger, S., et al. (2015). Mapping and root rot resistance and root architecture quantitative trait loci in common bean. Crop Sci. 55, 1969-1977. doi: 10.2135/cropsci2014.11.0805
44. Hameed, M., Mansoor, U., Ashraf, M., and Rao, A. U. R. (2002). Variation in leaf anatomy in wheat germplasm from varying drought-hit habitats. Int. J. Agric. Biol. 4, 12-16.
45. Hatmi, S., Gruau, C., Trotel-Aziz, P., Villaume, S., Rabenoelina, F., Baillieul, F., et al. (2015). Drought stress tolerance in grapevine involves activation of polyamine oxidation contributing to improved immune response and low susceptibility to Botrytis cinerea. J. Exp. Bot. 66, 775-787. doi: 10.1093/jxb/eru436
46. Higginbotham, R. W., Paulitz, T. C., and Kidwell, K. K. (2004). Virulence of Pythium species isolated from wheat fields in eastern Washington. Plant Dis. 88, 1021-1026. doi: 10.1094/PDIS.2004.88.9.1021
47. Isaacson, T., Kosma, D. K., Matas, A. J., Buda, G. J., He, Y., Yu, B., et al. (2009). Cutin deficiency in the tomato fruit cuticle consistently affects resistance to microbial infection and biomechanical properties, but not transpirational water loss. Plant J. 60, 363-377. doi: 10.1111/j.1365-313X.2009.03969.x
48. Jackson, R. D. (1986). Remote sensing of biotic and abiotic plant stress. Annu. Rev. Phytopathol. 24, 265-287. doi: 10.1146/annurev.py.24.090186.001405
49. Jedmowski, C., Ashoub, A., Momtaz, O., and Brüggemann, W. (2015). Impact of drought, heat, and their combination on chlorophyll fluorescence and yield of wild barley (Hordeum spontaneum). J. Bot. 2015, 9. doi: 10.1155/2015/120868
50. Jenks, M. A., Joly, R. J., Peters, P. J., Rich, P. J., Axtell, J. D., and Ashworth, E. N. (1994). Chemically induced cuticle mutation affecting epidermal conductance to water vapor and disease susceptibility in Sorghum bicolor (L.) Moench. Plant Physiol. 105, 1239-1245. doi: 10.1104/pp.105.4.1239
51. Kaddour, A. A., and Fuller, M. P. (2004). The effect of elevated CO2 and drought on the vegetative growth and development of durum wheat (Triticum durum Desf.) cultivars. Cereal Res. Commun. 32, 225-232.
52. Kamilova, F., Kravchenko, L. V., Shaposhnikov, A. I., Makarova, N., and Lugtenberg, B. (2006). Effects of the tomato pathogen Fusarium oxysporum f. sp radicis-lycopersici and of the biocontrol bacterium Pseudomonas fluorescens WCS365 on the composition of organic acids and sugars in tomato root exudate. Mol. Plant Microbe Interact. 19, 1121-1126. doi: 10.1094/MPMI-19-1121
53. Kosma, D. K., Bourdenx, B., Bernard, A., Parsons, E. P., Lü, S., Joubès, J., et al. (2009). The impact of water deficiency on leaf cuticle lipids of Arabidopsis. Plant Physiol. 151, 1918-1929. doi: 10.1104/pp.109.141911
54. Kudela, V. (2009). Potential impact of climate change on geographic distribution of plant pathogenic bacteria in central Europe. Plant Prot. Sci. 45, S27-S32.
55. Lacape, J.-M., and Nguyen, T. B. (2005). Mapping quantitative trait loci associated with leaf and stem pubescence in cotton. J. Hered. 96, 441-444. doi: 10.1093/jhered/esi052
56. Ladanyi, M., and Horvath, L. (2010). A review of the potential climate change impact on insect populations-general and agricultural aspects. Appl. Ecol. Environ. Res. 8, 143-152. doi: 10.15666/aeer/0802_143151
57. Lai, A., Cianciolo, V., Chiavarini, S., and Sonnino, A. (2000). Effects of glandular trichomes on the development of Phytophthora infestans infection in potato (S. tuberosum). Euphytica 114, 165-174. doi: 10.1023/A:1003924318577
58. Lamey, H. A. (1988). Sugarbeet Research and Extension Reports, Vol. 19. Available at: http://www.sbreb.org/brochures/Mildew/index2.htm, 158-161
59. Lamichhane, J. R., and Venturi, V. (2015). Synergisms between microbial pathogens in plant disease complexes: a growing trend. Front. Plant Sci. 6:385. doi: 10.3389/fpls.2015.00385
60. Lapwood, D. H., and Hering, T. F. (1968). Infection of potato tubers by common scab during brief periods when soil is drying. Eur. Potato J. 11, 177-187. doi: 10.1007/BF02364421
61. Loreto, F., and Bongi, G. (1989). Combined low temperature-high light effect on gas-exchange properties of jojoba leaves. Plant Physiol. 91, 1580-1585. doi: 10.1104/pp.91.4.1580
62. Lynch, J. P., Chimungu, J. G., and Brown, K. M. (2014). Root anatomical phenes associated with water acquisition from drying soil: targets for crop improvement. J Exp. Bot. 65, 6155-6166. doi: 10.1093/jxb/eru162
63. 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. doi: 10.1007/978-3-319-07899-1_1
64. Marcell, L. M., and Beattie, G. A. (2002). Effect of leaf surface waxes on leaf colonization by Pantoea agglomerans and Clavibacter michiganensis. Mol. Plant Microb. Interact. 15, 1236-1244. doi: 10.1094/MPMI.2002.15.12.1236
65. Martin, J. T. (1964). Role of cuticle in the defense against plant disease. Annu. Rev. Phytopathol. 2, 81-100. doi: 10.1146/annurev.py.02.090164.000501
66. 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
67. McDonald, A., Riha, S., DiTommasob, A., and DeGaetanoa, A. (2009). Climate change and the geography of weed damage: analysis of U.S. maize systems suggests the potential for significant range transformations. Agric. Ecosyst. Environ. 130, 131-140. doi: 10.1016/j.agee.2008.12.007
68. McElrone, A. J., Sherald, J. L., and Forseth, I. N. (2003). Interactive effects of water stress and xylem limited bacterial infection on the water relations of a host vine. J. Exp. Bot. 54, 419-430. doi: 10.1093/jxb/erg046
69. Mihail, J. D. (1989). Macrophomina phaseolina: spatio-temporal dynamics of inoculum and of disease in a highly susceptible crop. Phytopathology 79, 848-855. doi: 10.1094/Phyto-79-848
70. 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
71. Monier, J. M., and Lindow, S. E. (2003). Differential survival of solitary and aggregated bacterial cells promotes aggregate formation on leaf surfaces. Proc. Natl. Acad. Sci. U.S.A. 100, 15977-15982. doi: 10.1073/pnas.2436560100
72. 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
73. Nonomura, T., Xu, L., Wada, M., Kawamura, S., Miyajima, T., Nishitomi, A., et al. (2009). Trichome exudates of Lycopersicon pennellii form a chemical barrier to suppress leaf-surface germination of Oidium neolycopersici conidia. Plant Sci. 176, 31-37. doi: 10.1016/j.plantsci.2008.09.002
74. Odvody, G. N., and Dunkle, L. D. (1979). Charcoal stalk rot of sorghum: effect of environment on host-parasite relations. Phytopathology 69, 250-254. doi: 10.1094/Phyto-69-250
75. Olaya, G., and Abawi, G. S. (1996). Effect of water potential on mycelial growth and on production and germination of sclerotia of Macrophomina phaseolina. Plant Dis. 80, 1351-1354. doi: 10.1094/PD-80-1351
76. Oldenburg, E., Manderscheid, R., Erbs, M., and Weigel, H. J. (2009). “Interaction of free air carbon dioxide enrichment (FACE) and controlled summer drought on fungal infections of maize,” in Crop Plant Resistance to Biotic and Abiotic Factors: Current Potential and Future Demands, eds F. Feldmann, D. V. Alford, and C. Furk (Berlin: Julius Kühn-Institut), 75-83.
77. Pandey, P., Ramegowda, V., and Senthil-Kumar, M. (2015a). Shared and unique responses of plants to multiple individual stresses and stress combinations: physiological and molecular mechanisms. Front. Plant Sci. 6:723. doi: 10.3389/fpls.2015.00723
78. Pandey, P., Sinha, R., Mysore, K. S., and Senthil-Kumar, M. (2015b). “Impact of concurrent drought stress and pathogen infection on plants,” in Combined Stresses in Plants, ed. R. Mahalingam (Cham: Springer International Publishing), 203-222.
79. Pastor-Corrales, M. A., and Abawi, G. S. (1988). Reactions of selected bean accessions to infection by Macrophomina phaseolina. Plant Dis. 72, 39-41. doi: 10.1094/PD-72-0039
80. Patterson, D. T. (1995). Effects of environmental stress on weed/crop interaction. Weed Sci. 43, 483-490.
81. Patterson, D. T., and Flint, E. P. (1979). Effects of chilling on cotton (Gossypium hirsutum), velvetleaf (Abutilon theophrasti), and spurred anoda (Anoda cristata). Weed Sci. 27, 473-479.
82. Pautasso, M., Döring, T. F., Garbelotto, M., Pellis, L., and Jeger, M. J. (2012). Impacts of climate change on plant diseases-opinions and trends. Eur. J. Plant Pathol. 133, 295-313. doi: 10.1007/s10658-012-9936-1
83. Peters, K., Breitsameter, L., and Gerowitt, B. (2014). Impact of climate change on weeds in agriculture: a review. Agric. Sustain. Dev. 34, 707-721. doi: 10.1007/s13593-014-0245-2
84. Pinter, P. J., Stanghellini, M. E., Reginato, R. J., Idso, S. B., Jenkins, A. D., and Jackson, R. D. (1979). Remote detection of biological stresses in plants with infrared thermometry. Science 205, 585-586. doi: 10.1126/science.205.4406.585
85. Pinto, R. S., and Reynolds, M. P. (2015). Common genetic basis for canopy temperature depression under heat and drought stress associated with optimized root distribution in bread wheat.TAG. Theor. Appl. Genet. 128, 575-585. doi: 10.1007/s00122-015-2453-9
86. Potato Council News (2011). Available at. http://www.potatopro.com/news/2011/continuing-drought-increases-common-scab-threat-uk-potato-growers
87. Pouzoulet, J., Pivovaroff, A. L., Santiago, L. S., and Rolshausen, P. E. (2014). Can vessel dimension explain tolerance toward fungal vascular wilt diseases in woody plants? Lessons from Dutch elm disease and esca disease in grapevine. Front. Plant Sci. 5:253. doi: 10.3389/fpls.2014.00253
88. 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. Crop Sci. 197, 430-441. doi: 10.1111/j.1439-037X.2011.00477.x
89. 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
90. Puckette, M. C., Weng, H., and Mahalingam, R. (2007). Physiological and biochemical responses to acute ozone-induced oxidative stress in Medicago truncatula. Plant Physiol. Biochem. 45, 70-79. doi: 10.1016/j.plaphy.2006.12.004
91. 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
92. Ramu, V. S., Paramanantham, A., Ramegowda, V., Mohan-Raju, B., Udayakumar, M., and 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:e0157522. doi: 10.1371/journal.pone.0157522
93. Ristaino, J. B., and Duniway, J. M. (1989). Effect of pre-inoculation and post-inoculation water stress on the severity of Phytophthora root rot in processing tomatoes. Plant Dis. 73, 349-352. doi: 10.1094/PD-73-0349
94. 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
95. Roy, B. A., Stanton, M. L., and Eppley, S. M. (1999). Effects of environmental stress on leaf hair density and consequences for selection. J. Evol. Biol. 12, 1089-1103. doi: 10.1046/j.1420-9101.1999.00107.x
96. Scherm, H., and Coakley, S. M. (2003). Plant pathogens in a changing world. Australas. Plant Pathol. 32, 157-165. doi: 10.1071/AP03015
97. Schroth, M. N., and Hildebrand, D. C. (1964). Influence of plant exudates on root-infecting fungi. Annu. Rev. Phytopathol. 2, 101-132. doi: 10.1146/annurev.py.02.090164.000533
98. Sharma, M., and Pande, S. (2013). Unravelling effects of temperature and soil moisture stress response on development of dry root rot [Rhizoctonia bataticola (Taub.)] Butler in Chickpea. Am. J. Plant Sci. 4, 584-589. doi: 10.4236/ajps.2013.43076
99. Sharma, S. K., Sharma, P. N., and Sharma, B. K. (2012). Epidemiological studies on stem rot of chickpea. Indian Phytopathol. 54, 185-187.
100. Simonetta, S., Avidano, L., and Berta, G. (2007). Morphogenetic effects induced by pathogenic and non-pathogenic Rhizoctonia solani Kühn strains on tomato roots. Caryologia 60, 141-145. doi: 10.1080/00087114.2007.10589563
101. Sinha, R., Gupta, A., and Senthil-Kumar, M. (2016). Understanding the impact of drought on foliar and xylem invading bacterial pathogen stress in chickpea. Front. Plant Sci. 7:902. doi: 10.3389/fpls.2016.00902
102. Smith, D., Chilvers, M., Dorrance, A., Hughes, T., Mueller, D., Niblack, T., et al. (2015). Soybean Disease Management. Available at: http://cropprotectionnetwork.org/soybean/charcoal-rot/
103. Song, Y., Yu, J., and Huang, B. (2014). Elevated CO2-mitigation of high temperature stress associated with maintenance of positive carbon balance and carbohydrate accumulation in kentucky bluegrass. PLoS ONE 9:e89725. doi: 10.1371/journal.pone.0089725
104. Srinivasan, S., Gomez, S. M., Kumar, S. S., Ganesh, S. K., Biji, K. R., Senthil, A., et al. (2008). QTLs linked to leaf epicuticular wax, physio-morphological and plant production traits under drought stress in rice (Oryza sativa L.). Plant Growth Regul. 56, 245-256. doi: 10.1007/s10725-008-9304-5
105. Stuart, B. L., Harrison, S. K., Abernathy, J. R., Krieg, D. R., and Wendt, C. W. (1984). The response of cotton (Gossypium hirsutum) water relations to smooth pigweed (Amaranthus hybridus) competition. Weed Sci. 32, 126-132.
106. Su, L., Dai, Z., Li, S., and Xin, H. (2015). A novel system for evaluating drought-cold tolerance of grapevines using chlorophyll fluorescence. BMC Plant Biol. 15:82. doi: 10.1186/s12870-015-0459-8
107. Suzuki, N., Rivero, R. M., Shulaev, V., Blumwald, E., and Mittler, R. (2014). Abiotic and biotic stress combinations. New Phytol. 203, 32-43. doi: 10.1111/nph.12797
108. Thaler, J. S., and Bostock, R. M. (2004). Interactions between abscisic-acid-mediated responses and plant resistance to pathogens and insects. Ecology 85, 48-58. doi: 10.1890/02-0710
109. Triky-Dotan, S., Yermiyahu, U., Katan, J., and Gamliel, A. (2005). Development of crown and root rot disease of tomato under irrigation with saline water. Phytopathology 95, 1438-1444. doi: 10.1094/PHYTO-95-1438
110. Umamaheswari, C., Ramakrishnan, G., and Nallathambi, P. (2000). Role of inoculum level on disease incidence of dry root rot caused by Macrophomina phaseolina in groundnut. Madras Agric. J. 87, 71-73.
111. Valerio, M., Lovelli, S., Perniola, M., Di Tommaso, T., and Ziska, L. (2013). The role of water availability on weed-crop interactions in processing tomato for southern Italy. Acta Agric. Scand. Sect. B 63, 62-68. doi: 10.1080/09064710.2012.715184
112. Welfare, K., Yeo, A. R., and Flowers, T. J. (2002). Effects of salinity and ozone, individually and in combination, on the growth and ion contents of two chickpea (Cicer arietinum L.) varieties. Environ. Pollut. 120, 397-403. doi: 10.1016/S0269-7491(02)00109-4
113. Xiong, L., Wang, R. G., Mao, G., and Koczan, J. M. (2006). Identification of drought tolerance determinants by genetic analysis of root response to drought stress and abscisic acid. Plant Physiol. 142, 1065-1074. doi: 10.1104/pp.106.084632
114. Xu, P., Chen, F., Mannas, J. P., Feldman, T., Sumner, L. W., and Roossinck, M. J. (2008). Virus infection improves drought tolerance. New Phytol. 180, 911-921. doi: 10.1111/j.1469-8137.2008.02627.x
115. Zhan, A., Schneider, H., and Lynch, J. (2015). Reduced lateral root branching density improves drought tolerance in maize. Plant Physiol. 168, 1603-1615. doi: 10.1104/pp.15.00187
116. Zhou, L., Ni, E., Yang, J., Zhou, H., Liang, H., Li, J., et al. (2013). Rice OsGL1-6 is involved in leaf cuticular wax accumulation and drought resistance. PLoS ONE 8:e65139. doi: 10.1371/journal.pone.0065139
117. 2. Agron. J. 102, 118-123. doi: 10.2134/agronj2009.0205