Heat stress responses in a large set of winter wheat cultivars (Triticum aestivum L.) depend on the timing and duration of stress

Autoři: Krisztina Balla aff001;  Ildikó Karsai aff001;  Péter Bónis aff002;  Tibor Kiss aff001;  Zita Berki aff001;  Ádám Horváth aff001;  Marianna Mayer aff003;  Szilvia Bencze aff004;  Ottó Veisz aff003
Působiště autorů: Molecular Breeding Department, Agricultural Institute, Centre for Agricultural Research, Hungarian Academy of Sciences, Martonvásár, Hungary aff001;  Crop Production Department, Agricultural Institute, Centre for Agricultural Research, Hungarian Academy of Sciences, Martonvásár, Hungary aff002;  Cereal Breeding Department, Agricultural Institute, Centre for Agricultural Research, Hungarian Academy of Sciences, Martonvásár, Hungary aff003;  Research Institute of Organic Agriculture, Budapest, Hungary aff004
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: 10.1371/journal.pone.0222639


The adverse effects of heat on plant yield strongly depend on its duration and the phenological stage of the crops when the heat occurs. To clarify the effects of these two aspects of heat stress, systematic research was conducted under controlled conditions on 101 wheat cultivars of various geographic origin. Different durations of heat stress (5, 10 and 15 days) were applied starting from three developmental stages (ZD49: booting stage, ZD59: heading, ZD72: 6th day after heading). Various morphological, yield-related traits and physiological parameters were measured to determine the stress response patterns of the wheat genotypes under combinations of the duration and the timing of heat stress. Phenological timing significantly influenced the thousand-kernel weight and reproductive tiller number. The duration of heat stress was the most significant component in determining both seed number and seed weight, as well as the grain yield consequently, explaining 51.6% of its phenotypic variance. Irrespective of the developmental phase, the yield-related traits gradually deteriorated over time, and even a 5-day heat stress was sufficient to cause significant reductions. ZD59 was significantly more sensitive to heat than either ZD49 or ZD72. The photosynthetic activity of the flag leaf was mostly determined by heat stress duration. No significant associations were noted between physiological parameters and heat stress response as measured by grain yield. Significant differences were observed between the wheat genotypes in heat stress responses, which varied greatly with developmental phase. Based on the grain yield across developmental phases and heat stress treatments, eight major response groups of wheat genotypes could be identified, and among them, three clusters were the most heat-tolerant. These cultivars are currently included in crossing schemes, partially for the identification of the genetic determinants of heat stress response and partially for the development of new wheat varieties with better heat tolerance.

Klíčová slova:

Physical sciences – Physics – Classical mechanics – Mechanical stress – Thermal stresses – Condensed matter physics – Phase transitions – Vaporization – Evaporation – Biology and life sciences – Organisms – Eukaryota – Plants – Grasses – Wheat – Plant science – Plant anatomy – Seeds – Plant physiology – Plant defenses – Plant resistance to abiotic stress – Plant pathology – Plant ecology – Plant-environment interactions – Plant biochemistry – Photosynthesis – Ecology – Anatomy – Head – Ears – Biochemistry – Engineering and technology – Manufacturing processes – Heat treatment – Ecology and environmental sciences – Medicine and health sciences


1. Nagy BA, Boros T. Climate Change Policy in Hungary, Executive Summary. Policy Solutions, Friedrich Ebert Stiftung. Nov 2011. Available from: http://www.fesbp.hu/common/pdf/Climate_Change_Policy.pdf Cited 31 May 2019.

2. Kumudini S, Andrade FH, Boote KJ, Brown GA, Dzotsi KA, Edmeades GO, et al. Predicting maize phenology: intercomparison of functions for developmental response to temperature. Agron J. 2014;106: 2087–2097.

3. Hatfield JL, Prueger JH. Temperature extremes: effect on plant growth and development. Weather Clim Extrem. 2015;10: 4–10.

4. Lakatos M, Szépszó G, Bihari Z, Krüzselyi I, Szabó P, Bartholy J, et al. Changes in climatic extremes in Hungary: recent and future. Summary of Hungarian results in connection with the thematic report on the risk and management of extreme climate events in the IPCC 2012. 29 Febr 2012. Available from: https://www.met.hu/doc/IPCC_jelentes/HREX_jelentes-2012.pdf Cited 31 May 2019.

5. Wahid A, Gelani S, Ashraf M, Foolad M. Heat tolerance in plants: an overview. Environ Exp Bot. 2007;61: 199–223.

6. Rezaei E, Webber H, Gaiser T, Naab J, Ewert F. Heat stress in cereals: mechanisms and modelling. Eur J Agron. 2015;64: 98–113.

7. Kaushal N, Bhandari K, Siddique KHM, Nayyar H. Food crops face rising temperatures: an overview of responses, adaptive mechanisms, and approaches to improve heat tolerance. Cogent Food Agric. 2016;2. doi: 10.1080/23311932.2015.1134380

8. Porter JR, Gawith M. Temperatures and the growth and development of wheat: a review. Eur J Agron. 1999;10: 23–36.

9. Ferris R. Effect of high temperature stress at anthesis on grain yield and biomass of field-grown crops of wheat. Ann Bot. 1998;82: 631–639.

10. Semenov MA, Porter JR. Climatic variability and the modelling of crop yields. Agric For Meteorol. 1995;73: 265–283.

11. Kobza J, Edwards GE. Influences of leaf temperature on photosynthetic carbon metabolism in wheat. Plant Physiol. 1987;83: 69–74. doi: 10.1104/pp.83.1.69 16665218

12. Chowdhury SI, Wardlaw IF. The effect of temperature on kernel development in cereals. Aust J Agric Res. 1978;29: 205–223.

13. Tewolde H, Fernandez CJ, Erickson CA. Wheat cultivars adapted to post-heading high temperature stress. J Agron Crop Sci. 2006;192: 111–120.

14. Fischer RA. Number of kernels in wheat crops and the influence of solar radiation and temperature. J Agric Sci. 1985;105: 447–461.

15. Ortiz-Monasterio I, Dhillon SS, Fischer RA. Date of sowing effects on grain yield and yield components of irrigated spring wheat cultivars and relationships with radiation and temperature in Ludhiana, India. Field Crops Res. 1994;37: 169–184.

16. McMaster GS. Phenology, development, and growth of the wheat (Triticum aestivum L.) shoot apex: a review. Adv Agron. 1997;59: 63–118.

17. Saini HS, Aspinall D. Effect of water deficit on sporogenesis in wheat (Triticum aestivum L.). Ann Bot. 1981;48: 623–633.

18. Saini HS, Sedgley M, Aspinall D. Effect of heat stress during floral development on pollen tube growth and ovary anatomy in wheat (Triticum aestivum L.). Aust J Plant Physiol. 1983;10: 137–144.

19. Wollenweber B, Porter JR, Schellberg J. Lack of interaction between extreme high-temperature events at vegetative and reproductive growth stages in wheat. J Agron Crop Sci. 2003;189: 142–150.

20. Lobell DB, Schlenker W, Costa-Roberts J. Climate trends and global crop production since 1980. Science. 2011;333: 616–620. doi: 10.1126/science.1204531 21551030

21. Stone PJ, Nicolas ME. Wheat cultivars vary widely in their responses of grain yield and quality to short periods of post-anthesis heat stress. Aust J Plant Physiol. 1994;21: 887–900.

22. Stone PJ, Nicolas ME. Effect of timing of heat stress during grain filling on two wheat varieties differing in heat tolerance. I. Grain growth. Aust J Plant Physiol. 1995;22: 927–934.

23. Talukder ASMHM McDonald GK, Gill GS. Effect of short-term heat stress prior to flowering and early grain set on the grain yield of wheat. Field Crops Res. 2014;160: 54–63.

24. Stone PJ, Nicolas ME. A survey of the effects of high temperature during grain filling on yield and quality of 75 wheat cultivars. Aust J Agric Res. 1995;46: 475–492.

25. Rahman MA, Chikushi J, Yoshida S, Karim A. Growth and yield components of wheat genotypes exposed to high temperature stress under control environment. Bangladesh J Agric Res. 2009;34: 360–372.

26. Yin X, Guo W, Spiertz JH. A quantitative approach to characterize sink–source relationships during grain filling in contrasting wheat genotypes. Field Crops Res. 2009;114: 119–126.

27. Vignjevic M, Wang X, Olesen JE, Wollenweber B. Traits in spring wheat cultivars associated with yield loss caused by a heat stress episode after anthesis. J Agron Crop Sci. 2015;201: 32–48.

28. Yang J, Sears RG, Gill BS, Paulsen GM. Growth and senescence characteristics associated with tolerance of wheat-alien amphiploids to high temperature under controlled conditions. Euphytica. 2002;126: 185–193.

29. Shah NH, Paulsen GM. Interaction of drought and high temperature on photosynthesis and grain-filling of wheat. Plant Soil. 2003;257: 219–226.

30. Harding SA, Guikema JA, Paulsen GM. Photosynthetic decline from high temperature stress during maturation of wheat: II. Interaction with source and sink processes. Plant Physiol. 1990;92: 654–658. doi: 10.1104/pp.92.3.654 16667330

31. Liu B, Asseng S, Wang A, Wang S, Tang L, Cao W, et al. Modelling the effects of post-heading heat stress on biomass growth of winter wheat. Agric For Meteorol. 2017;247: 476–490.

32. Djanaguiraman M, Boyle DL, Welti R, Jagadish SVK, Prasad PVV. Decreased photosynthetic rate under high temperature in wheat is due to lipid desaturation, oxidation, acylation, and damage of organelles. BMC Plant Biol. 2018;18: 55. doi: 10.1186/s12870-018-1263-z 29621997

33. Ristic Z, Bukovnik U, Prasad PVV. Correlation between heat stability of thylakoid membranes and loss of chlorophyll in winter wheat under heat stress. Crop Sci. 2007;47: 2067–2073.

34. Khan SU, Gurmani AR, Qayyum A, Khan H. Heat tolerance evaluation of wheat (Triticum aestivum L.) genotypes based on some potential heat tolerance indicators. J Chem Soc Pak. 2013;35: 647–653.

35. Yang J, Zhang J, Wang Z, Zhu Q, Liu L. Water deficit–induced senescence and its relationship to the remobilization of pre-stored carbon in wheat during grain filling. Agron J. 2001;93: 196–206.

36. Gregersen PL, Holm PB. Transcriptome analysis of senescence in the flag leaf of wheat (Triticum aestivum L.). Plant Biotechnol J. 2007;5: 192–206. doi: 10.1111/j.1467-7652.2006.00232.x 17207268

37. Al-Khatib K, Paulsen GM. Mode of high temperature injury to wheat during grain development. Physiol Plant. 1984;61: 363–368.

38. Harding SA, Guikema JA, Paulsen GM. Photosynthetic decline from high temperature stress during maturation of wheat. Interaction with senescence processes. Plant Physiol. 1990;92: 648–653. doi: 10.1104/pp.92.3.648 16667329

39. Reynolds MP, Delgado MIB, Gutiérrez-Rodríguez M, Larqué-Saavedra A. Photosynthesis of wheat in a warm, irrigated environment I: genetic diversity and crop productivity. Field Crops Res. 2000;66: 37–50.

40. Liu B, Asseng S, Liu L, Tang L, Cao W, Zhu Y. Testing the responses of four wheat crop models to heat stress at anthesis and grain filling. Glob Chang Biol. 2016;22: 1890–1903. doi: 10.1111/gcb.13212 26725507

41. Bhullar SS, Jenner CF. Differential responses to high temperatures of starch and nitrogen accumulation in the grain of four cultivars of wheat. Aust J Plant Physiol. 1985;12: 363–375.

42. Farooq M, Bramley H, Palta JA, Siddique KHM. Heat stress in wheat during reproductive and grain-filling phases. Crit Rev Plant Sci. 2011;30: 491–507.

43. Salvucci ME, Crafts-Brandner SJ. Inhibition of photosynthesis by heat stress: the activation state of Rubisco as a limiting factor in photosynthesis. Physiol Plant. 2004;120: 179–186. doi: 10.1111/j.0031-9317.2004.0173.x 15032851

44. Xu XL, Zhang YH, Wang ZM. Effect of heat stress during grain filling on phosphoenolpyruvate carboxylase and ribulose-1,5-bisphosphate carboxylase/oxygenase activities of various green organs in winter wheat. Photosynthetica. 2004;42: 317–320.

45. Camejo D, Rodríguez P, Morales MA, Dell’Amico JM, Torrecillas A, Alarcón JJ. High temperature effects on photosynthetic activity of two tomato cultivars with different heat susceptibility. J Plant Physiol. 2005;162: 281–289. 15832680

46. Feng B, Liu P, Li G, Dong ST, Wang FH, Kong LA, et al. Effect of heat stress on the photosynthetic characteristics in flag leaves at the grain-filling stage of different heat-resistant winter wheat varieties. J Agron Crop Sci. 2014;200: 143–155.

47. Prasad PVV, Pisipati SR, Momčilović I, Ristic Z. 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. 2011;197: 430–441.

48. Mahrookashani A, Siebert S, Hüging H, Ewert F. Independent and combined effects of high temperature and drought stress around anthesis on wheat. J Agron Crop Sci. 2017;203: 453–463.

49. Balla K, Bedő Z, Veisz O. Effect of heat and drought stress on the photosynthetic processes of wheat. Cereal Res Commun. 2006;34: 381–384.

50. Balla K, Bedő Z, Veisz O. Study of physiological and agronomic traits in winter wheat under low water supplies. Cereal Res Commun. 2008;36: 1103–1106.

51. Balla K, Rakszegi M, Li Z, Békés F, Bencze S, Veisz O. Quality of winter wheat in relation to heat and drought shock after anthesis. Czech J Food Sci. 2011;29: 117–128.

52. Tottman DR, Makepeace RJ, Broad H. An explanation of the decimal code for the growth stages of cereals, with illustrations. Ann Appl Biol. 1979;93: 221–234.

53. Rashid MA, Andersen MN, Wollenweber B, Kørup K, Zhang X, Olesen JE. Impact of heat-wave at high and low VPD on photosynthetic components of wheat and their recovery. Environ Exp Bot. 2018;147: 138–146.

54. Rashid MA, Andersen MN, Wollenweber B, Zhang X, Olesen JE. Acclimation to higher VPD and temperature minimized negative effects on assimilation and grain yield of wheat. Agric For Meteorol. 2018;248: 119–129.

55. Sharma DK, Andersen SB, Ottosen C-O, Rosenqvist E. Wheat cultivars selected for high Fv/Fm under heat stress maintain high photosynthesis, total chlorophyll, stomatal conductance, transpiration and dry matter. Physiol Plant. 2015;153: 284–298. doi: 10.1111/ppl.12245 24962705

56. Brilli F, Hörtnagl L, Hammerle A, Haslwanter A, Hansel A, Loreto F, et al. Leaf and ecosystem response to soil water availability in mountain grasslands. Agric For Meteorol. 2011;151: 1731–1740. 24465071

57. Fujimura S, Shi P, Iwama K, Zhang X, Gopal J, Jitsuyama Y. Effects of CO2 increase on wheat growth and yield under different atmospheric pressures and their interaction with temperature. Plant Prod Sci. 2012;15: 118–124.

58. Bita CE, Gerats T. Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci. 2013;4: 273. doi: 10.3389/fpls.2013.00273 23914193

59. Hlavacova M, Pohankova E, Klem K, Hlavinka P, Trnka M. Effect of drought stress on selected winter wheat yield formation components within pot and field experimental design. In: Polák O, Cerkal R, Belcredi NB, Horký P, Vacek P, editors. Proceedings of International PhD students conference. MendelNet; 2016. pp. 63–68.

60. Kiss T, Bányai J, Balla K, Mayer M, Berki Z, Horváth Á, et al. Comparative study of the developmental traits and yield components of bread wheat under field conditions in several years of multi-sowing time experiments. Crop Sci. 2019;59: 591–604.

61. Ali MB, Ibrahim AMH, Malla S, Rudd J, Hays DB. Family-based QTL mapping of heat stress tolerance in primitive tetraploid wheat (Triticum turgidum L.). Euphytica. 2013;192: 189–203.

62. Cossani CM, Reynolds MP. Heat stress adaptation in elite lines derived from synthetic hexaploid wheat. Crop Sci. 2015;55: 2719–2735.

63. Barber HM, Lukac M, Simmonds J, Semenov MA, Gooding MJ. Temporally and genetically discrete periods of wheat sensitivity to high temperature. Front Plant Sci. 2017;8: 51. doi: 10.3389/fpls.2017.00051 28179910

64. Bergkamp B, Impa SM, Asebedo AR, Fritz AK, Jagadish SVK. Prominent winter wheat varieties response to post-flowering heat stress under controlled chambers and field based heat tents. Field Crops Res. 2018;222: 143–152.

65. Prasad PVV, Djanaguiraman M. Response of floret fertility and individual grain weight of wheat to high temperature stress: sensitive stages and thresholds for temperature and duration. Funct Plant Biol. 2014;41: 1261–1269.

66. Prasad PVV, Pisipati SR, Mutava RN, Tuinstra MR. Sensitivity of grain Sorghum to high temperature stress during reproductive development. Crop Sci. 2008;48: 1911–1917.

67. Randall PJ, Moss HJ. Some effects of temperature regime during grain filling on wheat quality. Aust J Agric Res. 1990;41: 603–617.

68. Wardlaw IF. The effect of high temperature on kernel development in wheat: variability related to pre-heading and post-anthesis conditions. Aust J Plant Physiol. 1994;21: 731–739.

69. Stone PJ, Nicolas ME. Comparison of sudden heat stress with gradual exposure to high temperature during grain filling in two wheat varieties differing in heat tolerance. I. Grain growth. Aust J Plant Physiol. 1995;22: 935–944.

70. Blumenthal CS, Bekes F, Batey IL, Wrigley CW, Moss HJ, Mares DJ, et al. Interpretation of grain quality results from wheat variety trials with reference to high temperature stress. Aust J Agric Res. 1991;42: 325–334.

71. Shirdelmoghanloo H, Cozzolino D, Lohraseb I, Collins NC. Truncation of grain filling in wheat (Triticum aestivum) triggered by brief heat stress during early grain filling: association with senescence responses and reductions in stem reserves. Funct Plant Biol. 2016;43: 919–930.

72. Kamrani M, Hoseini Y, Ebadollahi A. Evaluation for heat stress tolerance in durum wheat genotypes using stress tolerance indices. Arch Agron Soil Sci. 2017;64: 38–45.

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