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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Upregulation of TaHSP90A transcripts enhances heat tolerance and increases grain yield in wheat under changing climate conditions

Ali Ammar A , Zulfiqar Ali https://orcid.org/0000-0003-1228-3338 A B C * , Muhammad Abu Bakar Saddique A , Muhammad Habib-ur-Rahman D and Imtiaz Ali E
+ Author Affiliations
- Author Affiliations

A Institute of Plant Breeding and Biotechnology, MNS University of Agriculture, Multan 6000, Pakistan.

B Department of Plant Breeding & Genetics, University of Agriculture, Faisalabad 38000, Pakistan.

C Programs and Projects Department, Islamic Organization for Food Security, Astana 019900, Kazakhstan.

D Department of Agronomy, MNS University of Agriculture, Multan 6000, Pakistan.

E Regional Agricultural Research Institute, Bahawalpur 63100. Pakistan.


Handling Editor: Inzamam Haq

Functional Plant Biology 51, FP23275 https://doi.org/10.1071/FP23275
Submitted: 8 November 2023  Accepted: 18 January 2024  Published: 8 February 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Plants have certain adaptation mechanisms to combat temperature extremes and fluctuations. The heat shock protein (HSP90A) plays a crucial role in plant defence mechanisms under heat stress. In silico analysis of the eight TaHSP90A transcripts showed diverse structural patterns in terms of intron/exons, domains, motifs and cis elements in the promoter region in wheat. These regions contained cis elements related to hormones, biotic and abiotic stress and development. To validate these findings, two contrasting wheat genotypes E-01 (thermo-tolerant) and SHP-52 (thermo-sensitive) were used to evaluate the expression pattern of three transcripts TraesCS2A02G033700.1, TraesCS5B02G258900.3 and TraesCS5D02G268000.2 in five different tissues at five different temperature regimes. Expression of TraesCS2A02G033700.1 was upregulated (2-fold) in flag leaf tissue after 1 and 4 h of heat treatment in E-01. In contrast, SHP-52 showed downregulated expression after 1 h of heat treatment. Additionally, it was shown that under heat stress, the increased expression of TaHSP90A led to an increase in grain production. As the molecular mechanism of genes involved in heat tolerance at the reproductive stage is mostly unknown, these results provide new insights into the role of TaHSP90A transcripts in developing phenotypic plasticity in wheat to develop heat-tolerant cultivars under the current changing climate scenario.

Keywords: abiotic stress, climate change, food security, functional genomics, heat shock proteins, heat tolerance, spatial and temporal expression, Triticum aestivum L.

References

Ahuja I, de Vos RCH, Bones AM, Hall RD (2010) Plant molecular stress responses face climate change. Trends in Plant Science 15(12), 664-674.
| Crossref | Google Scholar | PubMed |

Ali Z, Zhang DY, Xu ZL, Yi JX, He XL, Huang YH, Liu XU, Khan AA, Trethowan RM, Ma HX (2012) Uncovering the salt response of soybean by unraveling its wild and cultivated functional genomes using tag sequencing. PLoS ONE 7(11), e48819.
| Crossref | Google Scholar | PubMed |

Al-Khatib K, Paulsen GM (1990) Photosynthesis and productivity during high temperature stress of wheat genotypes from major world regions. Journal of Crop Science 30(5), 1127-1132.
| Crossref | Google Scholar |

Ammar A, Ali Z, Saddique MAB, Habib-Ur-Rahman M, Ali I (2023) Genetic analysis and expression profiling of TaHSP90A transcripts confer heat tolerance in wheat. SABRAO Journal of Breeding and Genetics 55(3), 653-670.
| Crossref | Google Scholar |

Babenko VN, Rogozin IB, Mekhedov SL, Koonin EV (2004) Prevalence of intron gain over intron loss in the evolution of paralogous gene families. Nucleic Acids Research 32(12), 3724-3733.
| Crossref | Google Scholar | PubMed |

Bailey TL, Williams N, Misleh C, Li WW (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Research 34, W369-W373.
| Crossref | Google Scholar | PubMed |

Borrill P, Adamski N, Uauy C (2015) Genomics as the key to unlocking the polyploid potential of wheat. New Phytologist 208(4), 1008-1022.
| Crossref | Google Scholar | PubMed |

Chaudhary R, Baranwal VK, Kumar R, Sircar D, Chauhan H (2019) Genome-wide identification and expression analysis of Hsp70, Hsp90, and Hsp100 heat shock protein genes in barley under stress conditions and reproductive development. Functional and Integrative Genomics 19, 1007-1022.
| Crossref | Google Scholar | PubMed |

Chauhan H, Khurana N, Tyagi AK, Khurana JP, Khurana P (2011) Identification and characterization of high temperature stress responsive genes in bread wheat (Triticum aestivum L.) and their regulation at various stages of development. Plant Molecular Biology 75, 35-51.
| Crossref | Google Scholar | PubMed |

Chen J, Gao T, Wan S, Zhang Y, Yang J, Yu Y, et al. (2018) Genome-wide identification, classification and expression analysis of the HSP gene superfamily in tea plant (Camellia sinensis). International Journal of Molecular Sciences 19(9), 2633.
| Crossref | Google Scholar | PubMed |

De Maio A (1999) Heat shock proteins: facts, thoughts, and dreams. Shock 11(1), 1-12.
| Crossref | Google Scholar | PubMed |

Farooq M, Bramley H, Palta JA, Siddique KHM (2011) Heat stress in wheat during reproductive and grain-filling phases. Critical Reviews in Plant Sciences 30(6), 491-507.
| Crossref | Google Scholar |

Gil KE, Kim WY, Lee HJ, Faisal M, Saquib Q, Alatar AA, Park CM (2017) Zeitlupe contributes to a thermoresponsive protein quality control system in Arabidopsis. The Plant Cell 29(11), 2882-2894.
| Crossref | Google Scholar | PubMed |

Gouache D, Bris XL, Bogard M, Deudon O, Page C, Gate P (2012) Evaluating agronomic adaptation options to increasing heat stress under climate change during wheat grain filling in France. European Journal of Agronomy 39, 62-70.
| Crossref | Google Scholar |

Hu W, Hu G, Han B (2009) Genome-wide survey and expression profiling of heat shock proteins and heat shock factors revealed overlapped and stress specific response under abiotic stresses in rice. Plant Science 176((4)), 583-590.
| Crossref | Google Scholar |

Irshad A, Ahmed RI, Ur Rehman S, Sun G, Ahmad F, Sher MA, Aslam MZ, Hassan MM, Qari SH, Aziz MK, Khan Z (2022) Characterization of salt tolerant wheat genotypes by using morpho-physiological, biochemical, and molecular analysis. Frontier in Plant Science 13, 956298.
| Crossref | Google Scholar |

Krishna P, Gloor G (2001) The HSP90 family of proteins in Arabidopsis thaliana. Cell Stress and Chaperones 6(3), 238-246.
| Crossref | Google Scholar | PubMed |

Leach LJ, Belfield EJ, Jiang C, Brown C, Mithani A, Harberd NP (2014) Patterns of homoeologous gene expression shown by RNA sequencing in hexaploid bread wheat. BMC Genomics 15(1), 276.
| Crossref | Google Scholar |

Lee MH, Kim KM, Sang WG, Kang CS, Choi C (2022) Comparison of gene expression changes in three wheat varieties with different susceptibilities to heat stress using RNA Seq analysis. Internal Journal of Molecular Sciences 23, 10734.
| Crossref | Google Scholar | PubMed |

Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S (2002) Plant care, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Research 30(1), 325-327.
| Crossref | Google Scholar | PubMed |

Lesk C, Rowhani P, Ramankutty N (2016) Influence of extreme weather disasters on global crop production. Nature 529(7584), 84-87.
| Crossref | Google Scholar | PubMed |

Li W, Chen Y, Ye M, Wang D, Chen Q (2020) Evolutionary history of the heat shock protein 90 (Hsp90) family of 43 plants and characterization of Hsp90s in Solanum tuberosum. Molecular Biological Reports 47(9), 6679-6691.
| Crossref | Google Scholar | PubMed |

Liu Y, Wan H, Yang Y, Wei Y, Li Z, Ye Q, Wang R, Ruan M, Yao Z, Zhou G (2014) Genome-wide identification and analysis of heat shock protein 90 in tomato. Hereditas 36(10), 1043-1052.
| Google Scholar | PubMed |

Liu L, Han R, Yu N, Zhang W, Xing L, Xie D, Peng D (2018) A method for extracting high-quality total RNA from plant rich in polysaccharides and polyphenols using Dendrobium huoshanense. PLoS ONE 13(5), e0196592.
| Crossref | Google Scholar | PubMed |

Lu Y, Zhao P, Zhang A, Ma L, Xu S, Wang X (2020) Alternative splicing diversified the heat response and evolutionary strategy of conserved Heat Shock Protein 90s in hexaploid wheat (Triticum aestivum L.). Frontier in Genetics 11, 577897.
| Crossref | Google Scholar |

Maestri E, Klueva N, Perrotta C, Gulli M, Nguyen HT, Marmiroli N (2002) Molecular genetics of heat tolerance and heat shock proteins in cereals. Plant Molecular Biology 48, 667-681.
| Crossref | Google Scholar | PubMed |

Majoul T, Bancel E, Triboï E, Ben Hamida J, Branlard G (2004) Proteomic analysis of the effect of heat stress on hexaploid wheat grain: characterization of heat-responsive proteins from non-prolamins fraction. Proteomics 4(2), 505-513.
| Crossref | Google Scholar | PubMed |

Maphosa L, Langridge P, Taylor H, Parent B, Emebiri LC, Kuchel H, Reynolds MP, Chalmers KJ, Okada A, Edwards J, Mather DE (2014) Genetic control of grain yield and grain physical characteristics in a bread wheat population grown under a range of environmental conditions. Theoratical & Applied Genetics 127(7), 1607-1624.
| Crossref | Google Scholar | PubMed |

Mohammadi AS, Hadi H, Toorchi M, Pawłowski TA, Asgari LB, Price GW, Farooq M, Astatkie T (2023) Morpho-physiological responses and growth indices of triticale to drought and salt stresses. Scientific Reports 13(1), 8896.
| Crossref | Google Scholar |

Pearl LH, Prodromou C (2006) Structure and mechanism of the HSP90 molecular chaperone machinery. Annual Review of Biochemistry 75, 271-294.
| Crossref | Google Scholar |

Richter K, Buchner J (2001) Hsp90: chaperoning signal transduction. Journal of Cellular Physiology 188(3), 281-290.
| Crossref | Google Scholar | PubMed |

Richter K, Haslbeck M, Buchner J (2010) The heat shock response: life on the verge of death. Molecular Cell 40(2), 253-266.
| Crossref | Google Scholar | PubMed |

Rizzolo K, Wong P, Tillier ERM, Houry WA (2014) The interaction network of the HSP90 molecular chaperone. In ‘The molecular chaperones interaction networks in protein folding and degradation’. (Ed. W Houry) pp. 111–131. (Springer) doi:10.1007/978-1-4939-1130-1_5

Roy SW, Penny D (2007) On the incidence of intron loss and gain in paralogous gene families. Molecular Biology and Evolution 24(8), 1579-1581.
| Crossref | Google Scholar | PubMed |

Saddique MAB, Ali Z, Sher MA, Farid B, Ikram RM, Ahmad MS (2020) Proline, total antioxidant capacity, and OsP5CS gene activity in radical and plumule of rice are efficient drought tolerance indicator traits. International Journal of Agronomy 2020, 8862792.
| Crossref | Google Scholar |

Song Z, Pan F, Yang C, Jia H, Jiang H, He F, et al. (2019) Genome-wide identification and expression analysis of HSP90 gene family in Nicotiana tabacum. BMC Genetics 20, 35.
| Crossref | Google Scholar | PubMed |

Swindell WR, Huebner M, Weber AP (2007) Transcriptional profiling of Arabidopsis heat shock proteins and transcription factors reveals extensive overlap between heat and non-heat stress response pathways. BMC Genomics 8, 125.
| Crossref | Google Scholar | PubMed |

Tahir T, Rasheed A, Kayani S, Shahzad A (2023) High-throughput digital imaging analysis for grain morphology of historical wheat cultivars of Pakistan. Genetic Resources and Crop Evolution
| Crossref | Google Scholar |

Tashiro T, Wardlaw IF (1990) The response to high temperature shock and humidity changes prior to and during the early stages of grain development in wheat. Functional Plant Biology 17(5), 551-561.
| Crossref | Google Scholar |

Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in plants: an overview. Environmental & Experimental Botany 61(3), 199-223.
| Crossref | Google Scholar |

Wang R, Zhang Y, Kieffer M, Yu H, Kepinski S, Estelle M (2016) HSP90 regulates temperature-dependent seedling growth in Arabidopsis by stabilizing the auxin co-receptor F-box protein TIR1. Nature Communications 7, 10269.
| Crossref | Google Scholar |

Wheeler TR, Batts GR, Ellis RH, Hadley P, Morison JIL (1996) Growth and yield of winter wheat (Triticum aestivum) crops in response to CO2 and temperature. Journal of Agricultural Sciences 127(1), 37-48.
| Crossref | Google Scholar |

Yabe N, Takahashi T, Komeda Y (1994) Analysis of tissue-specific expression of Arabidopsis thaliana HSP90-family gene HSP81. Plant Cell Physiology 35(8), 1207-1219.
| Crossref | Google Scholar | PubMed |

Young JC, Moarefi I, Hartl FU (2001) Hsp90: a specialized but essential protein-folding tool. The Journal of Cell Biology 154(2), 267-273.
| Crossref | Google Scholar | PubMed |

Zhao C, Liu B, Piao S, Wang X, Lobell DB, Huang Y, Huang M, Yao Y, Bassu S, Ciais P, Durand J-L, Elliott J, Ewert F, Janssens IA, Li T, Lin E, Liu Q, Martre P, Müller C, Peng S, Peñuelas J, Ruane AC, Wallach D, Wang T, Wu D, Liu Z, Zhu Y, Zhu Z, Asseng S (2017) Temperature increase reduces global yields of major crops in four independent estimates. Proceedings of the National Academy of Sciences 114(35), 9326-9331.
| Crossref | Google Scholar |

Zheng B, Chenu K, Chapman SC (2016) Velocity of temperature and flowering time in wheat – assisting breeders to keep pace with climate change. Global Change Biology 22(2), 921-933.
| Crossref | Google Scholar | PubMed |

Zuehlke A, Johnson JL (2010) HSP90 and co-chaperones twist the functions of diverse client proteins. Biopolymers: Original Research on Biomolecules 93(3), 211-217.
| Crossref | Google Scholar |