Plant adaptations to the combination of drought and high temperatures

Physiologia Plantarum

Volumn 162, Issue 1, 2018, Pages 2-12

  Zandalinas, Sara I ^a   Mittler, Ron ^b   Balfagón, Damián ^a   Arbona, Vicent ^a   Gómez Cadenas, Aurelio ^a  

^a UNIVERSITAT JAUME I   (Spain)

^b UNIVERSITY OF NORTH TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; BIOLOGICAL MODEL; DROUGHT; HEAT; PHYSIOLOGICAL STRESS; PLANT PHYSIOLOGY;

ADAPTATION, PHYSIOLOGICAL; DROUGHTS; HOT TEMPERATURE; MODELS, BIOLOGICAL; PLANT PHYSIOLOGICAL PHENOMENA; STRESS, PHYSIOLOGICAL;

EID: 85013499812     PISSN: 00319317     EISSN: 13993054     Source Type: Journal    
DOI: 10.1111/ppl.12540     Document Type: Review

References (66)

1. Ahmed IM, Dai H, Zheng W, Cao F, Zhang G, Sun D, Wu F (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
2. Ahmed IM, Nadira UA, Bibi N, Cao F, He X, Zhang G, Wu F (2014) Secondary metabolism and antioxidants are involved in the tolerance to drought and salinity, separately and combined, in Tibetan wild barley. Environ Exp Bot 111: 1–12
3. 3 world. Plant Physiol 147: 13–19
4. Alhdad GM, Seal CE, Al-Azzawi MJ, Flowers TJ (2013) The effect of combined salinity and waterlogging on the halophyte Suaeda maritima: the role of antioxidants. Environ Exp Bot 87: 120–125
5. Aprile A, Havlickova L, Panna R, Marè C, Borrelli GM, Marone D, Perrotta C, Rampino P, De Bellis L, Curn V, Mastrangelo AM, Rizza F, Cattivelli L (2013) Different stress responsive strategies to drought and heat in two durum wheat cultivars with contrasting water use efficiency. BMC Genomics 14: 1–18
6. Atkinson NJ, Lilley CJ, Urwin PE (2013) Identification of genes involved in the response of Arabidopsis to simultaneous biotic and abiotic stresses. Plant Physiol 162: 2028–2041
7. Awasthi R, Kaushal N, Vadez V, Turner NC, Berger J, Siddique KHM, Nayyar H (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
8. Barnabás B, Jäger K, Fehér A (2008) The effect of drought and heat stress on reproductive processes in cereals. Plant Cell Environ 31: 11–38
9. Baxter A, Mittler R, Suzuki N (2014) ROS as key players in plant stress signalling. J Exp Bot 65: 1229–1240
10. Bi A, Fan J, Hu Z, Wang G, Amombo E, Fu J, Hu T (2016) Differential acclimation of enzymatic antioxidant metabolism and photosystem II photochemistry in tall fescue under drought and heat and the combined stresses. Front Plant Sci 7: 453
11. Bohler S, Sergeant K, Jolivet Y, Hoffmann L, Hausman J-F, Dizengremel P, Renaut J (2013) A physiological and proteomic study of poplar leaves during ozone exposure combined with mild drought. Proteomics 13: 1737–1754
12. 2 availability and inactivation of Rubisco limit photosynthesis in cotton plants under heat and drought stress in the field. Environ Exp Bot 83: 1–11
13. Casaretto JA, El-kereamy A, Zeng B, Stiegelmeyer SM, Chen X, Bi Y-M, Rothstein SJ (2016) Expression of OsMYB55 in maize activates stress-responsive genes and enhances heat and drought tolerance. BMC Genomics 17: 1–15
14. Castagna A, Di Baccio D, Ranieri AM, Sebastiani L, Tognetti R (2015) Effects of combined ozone and cadmium stresses on leaf traits in two poplar clones. Environ Sci Pollut Res 22: 2064–2075
15. Cherif J, Mediouni C, Ben Ammar W, Jemal F (2011) Interactions of zinc and cadmium toxicity in their effects on growth and in antioxidative systems in tomato plants (Solanum lycopersicum). J Environ Sci 23: 837–844
16. Cvikrová M, Gemperlová L, Martincová O, Vanková R (2013) Effect of drought and combined drought and heat stress on polyamine metabolism in proline-over-producing tobacco plants. Plant Physiol Biochem 73: 7–15
17. Danquah A, de Zelicourt A, Colcombet J, Hirt H (2014) The role of ABA and MAPK signaling pathways in plant abiotic stress responses. Biotechnol Adv 32: 40–52
18. De Boeck HJ, Bassin S, Verlinden M, Zeiter M, Hiltbrunner E (2015) Simulated heat waves affected alpine grassland only in combination with drought. New Phytol 209: 531–541
19. Gallas G, Waters ER (2015) Boechera species exhibit species-specific responses to combined heat and high light stress. PLoS One 10: e0129041
20. Gilroy S, Suzuki N, Miller G, Choi W-G, Toyota M, Devireddy AR, Mittler R (2014) A tidal wave of signals: calcium and ROS at the forefront of rapid systemic signaling. Trends Plant Sci 19: 623–630
21. Giraud E, Ho LHM, Clifton R, Carroll A, Estavillo G, Tan Y-F, Howell KA, Ivanova A, Pogson BJ, Millar AH, Whelan J (2008) The absence of ALTERNATIVE OXIDASE1a in Arabidopsis results in acute sensitivity to combined light and drought stress. Plant Physiol 147: 595–610
22. Haghjou MM, Shariati M, Smirnoff N (2009) The effect of acute high light and low temperature stresses on the ascorbate-glutathione cycle and superoxide dismutase activity in two Dunaliella salina strains. Physiol Plant 135: 272–280
23. Hu X, Wu L, Zhao F, Zhang D, Li N, Zhu G, Li C, Wang W (2015) Phosphoproteomic analysis of the response of maize leaves to drought, heat and their combination stress. Front Plant Sci 6: 1–21
24. Iyer NJ, Tang Y, Mahalingam R (2013) Physiological, biochemical and molecular responses to a combination of drought and ozone in Medicago truncatula. Plant Cell Environ 36: 706–720
25. Jiang Y, Huang B (2001) Drought and heat stress injury to two cool-season turfgrasses in relation to antioxidant metabolism and lipid peroxidation. Crop Sci 41: 436–442
26. Jin R, Wang Y, Liu R, Gou J, Chan Z (2016) Physiological and metabolic changes of Purslane (Portulaca oleracea L.) in response to drought, heat, and combined stresses. Front Plant Sci 6: 1–11
27. Johnson SM, Lim F-L, Finkler A, Fromm H, Slabas AR, Knight MR (2014) Transcriptomic analysis of Sorghum bicolor responding to combined heat and drought stress. BMC Genomics 15: 1–19
28. Keles Y, Oncel I (2002) Response of antioxidative defence system to temperature and water stress combinations in wheat seedlings. Plant Sci 163: 783–790
29. Koussevitzky S, Suzuki N, Huntington S, Armijo L, Sha W, Cortes D, Shulaev V, Mittler R (2008) Ascorbate peroxidase 1 plays a key role in the response of Arabidopsis thaliana to stress combination. J Biol Chem 283: 34197–34203
30. Kumar D, Datta R, Hazra S, Sultana A, Mukhopadhyay R, Chattopadhyay S (2015) Transcriptomic profiling of Arabidopsis thaliana mutant pad2.1 in response to combined cold and osmotic stress. PLoS One 10: e0122690
31. Lawlor DW (2013) Genetic engineering to improve plant performance under drought: physiological evaluation of achievements, limitations, and possibilities. J Exp Bot 64: 83–108
32. Li X, Yang Y, Sun X, Lin H, Chen J, Ren J, Hu X, Yang Y (2014) Comparative physiological and proteomic analyses of poplar (Populus yunnanensis) plantlets exposed to high temperature and drought. PLoS One 9: e107605
33. Liu X, Wu H, Ji C, Wei L, Zhao J, Yu J (2013) An integrated proteomic and metabolomic study on the chronic effects of mercury in Suaeda salsa under an environmentally relevant salinity. PLoS One 8: e64041
34. Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11: 15–19
35. Mittler R, Blumwald E (2010) Genetic engineering for modern agriculture: challenges and perspectives. Annu Rev Plant Biol 61: 443–462
36. Muñoz-Espinoza VA, López-Climent MF, Casaretto JA, Gómez-Cadenas A (2015) Water stress responses of tomato mutants impaired in hormone biosynthesis reveal abscisic acid, jasmonic acid and salicylic acid interactions. Front Plant Sci 6: 1–14
37. Nishiyama Y, Murata N (2014) Revised scheme for the mechanism of photoinhibition and its application to enhance the abiotic stress tolerance of the photosynthetic machinery. Appl Microbiol Biotechnol 98: 8777–8796
38. Obata T, Witt S, Lisec J, Palacios-Rojas N, Florez-Sarasa I, Araus JL, Cairns JE, Yousfi S, Fernie AR (2015) Metabolite profiles of maize leaves in drought, heat and combined stress field trials reveal the relationship between metabolism and grain yield. Plant Physiol 169: 2665–2683
39. 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: 1–14
40. Perdomo JA, Conesa MÀ, Medrano H, Ribas-Carbó M, Galmés J (2014) Effects of long-term individual and combined water and temperature stress on the growth of rice, wheat and maize: relationship with morphological and physiological acclimation. Physiol Plant 155: 149–165
41. 2. J Plant Physiol 170: 1517–1525
42. 2 emissions after the 2008–2009 global financial crisis. Nat Clim Chang 2: 2–4
43. Prasad PVV, Pisipati SR, Momčilović I, 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
44. Prasch CM, Sonnewald U (2013) Simultaneous application of heat, drought, and virus to Arabidopsis plants reveals significant shifts in signaling networks. Plant Physiol 162: 1849–1866
45. Priyanka B, Sekhar K, Reddy VD, Rao KV (2010) Expression of pigeonpea hybrid-proline-rich protein encoding gene (CcHyPRP) in yeast and Arabidopsis affords multiple abiotic stress tolerance. Plant Biotechnol J 8: 76–87
46. Rampino P, Mita G, Fasano P, Borrelli GM, Aprile A, Dalessandro G, De Bellis L, Perrotta C (2012) Novel durum wheat genes up-regulated in response to a combination of heat and drought stress. Plant Physiol Biochem 56: 72–78
47. Rasmussen S, Barah P, Suarez-Rodriguez MC, Bressendorff S, Friis P, Costantino P, Bones AM, Nielsen HB, Mundy J (2013) Transcriptome responses to combinations of stresses in Arabidopsis. Plant Physiol 161: 1783–1794
48. Rivero RM, Mestre TC, Mittler R, Rubio F, Garcia-Sanchez F, Martinez V (2013) The combined effect of salinity and heat reveals a specific physiological, biochemical and molecular response in tomato plants. Plant Cell Environ 37: 1059–1073
49. Rizhsky L, Liang H, Mittler R (2002) The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiol 130: 1143–1151
50. 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: 1683–1696
51. Rollins J, Habte E, Templer SE, Colby T, Schmidt J, 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
52. Sainz M, Díaz P, Monza J, 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
53. Sales CRG, Ribeiro RV, Silveira JAG, Machado EC, Martins MO, Lagôa AMMA (2013) Superoxide dismutase and ascorbate peroxidase improve the recovery of photosynthesis in sugarcane plants subjected to water deficit and low substrate temperature. Plant Physiol Biochem 73: 326–336
54. Shaik R, Ramakrishna W (2014) Machine learning approaches distinguish multiple stress conditions using stress-responsive genes and identify candidate genes for broad resistance in rice. Plant Physiol 164: 481–495
55. Srivastava G, Kumar S, Dubey G, Mishra V, Prasad SM (2012) Nickel and ultraviolet-B stresses induce differential growth and photosynthetic responses in Pisum sativum L. seedlings. Biol Trace Elem Res 149: 86–96
56. Suzuki N, Rivero RM, Shulaev V, Blumwald E, Mittler R (2014) Abiotic and biotic stress combinations. New Phytol 203: 32–43
57. Suzuki N, Basil E, Hamilton JS, Inupakutika MA, Zandalinas SI, Tripathy D, Yuting L, Dion E, Fukui G, Kumazaki A, Nakano R, Rivero RM, Verbeck GF, Azad RK, Blumwald E, Mittler R (2016) ABA is required for plant acclimation to a combination of salt and heat stress. PLoS One 11: e0147625
58. Vile D, Pervent M, Belluau M, Vasseur F, Bresson J, Muller B, Granier C, Simonneau T (2012) Arabidopsis growth under prolonged high temperature and water deficit: independent or interactive effects? Plant Cell Environ 35: 702–718
59. Wang G-P, Hui Z, Li F, Zhao M-R, Zhang J, Wang W (2010) Improvement of heat and drought photosynthetic tolerance in wheat by overaccumulation of glycinebetaine. Plant Biotechnol Rep 4: 213–222
60. 2 concentration on Cd and Zn accumulation dynamics in Triticum aestivum L. J Environ Sci 47: 109–119
61. Yang Y, Chen J, Liu Q, Ben C, Todd CD, Shi J, Yang Y, Hu X (2012) Comparative proteomic analysis of the thermotolerant plant Portulaca oleracea acclimation to combined high temperature and humidity stress. J Proteome Res 11: 3605–3623
62. Yoshida T, Mogami J, Yamaguchi-Shinozaki K (2014) ABA-dependent and ABA-independent signaling in response to osmotic stress in plants. Curr Opin Plant Biol 21: 133–139
63. Zandalinas SI, Rivero RM, Martínez V, Gómez-Cadenas A, Arbona V (2016a) Tolerance of citrus plants to the combination of high temperatures and drought is associated to the increase in transpiration modulated by a reduction in abscisic acid levels. BMC Plant Biol 16: 105
64. Zandalinas SI, Balfagón D, Arbona V, Gómez-Cadenas A, Inupakutika MA, Mittler R (2016b) ABA is required for the accumulation of APX1 and MBF1c during a combination of water deficit and heat stress. J Exp Bot 67: 5381–5390
65. Zhang M, Li G, Li G, Huang W, Bi T, Chen G, Tang Z, Su W, Sun W (2010) Proteomic study of Carissa spinarum in response to combined heat and drought stress. Proteomics 10: 3117–3129
66. 2 mitigates the impact of combined heat wave and drought stress in Arabidopsis thaliana at multiple organizational levels. Glob Chang Biol 20: 3670–3685