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Gene expression analysis of wheat (Triticum aestivum L.) during the vegetative stage under high ambient temperature condition

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Abstract

This study was conducted to acquire a comprehensive understanding of the growth characteristics of winter wheat in the Republic of Korea (ROK). The specific focus was on investigating physiological responses to temperature during the vegetative stages. We implemented four different temperature conditions, ranging from an average of 17 to 26 °C, in a climate-controlled growth chamber. We traced the 19 representative genes responsive to ambient high temperatures and heat stress. Hsp90.1-A1, HSP101 and MYB73 exhibited an increase in response to the rising temperature. Other genes such as ELF3, PIF4, VRNA1, SKP1 and HsfA1b decreased under high-temperature conditions. However, many transcription factors responding to high temperatures and genes related to the cell division cycle showed fluctuating expression, suggesting the presence of an optimal temperature within the range of 17 to 26 °C. Among them, Hsp90.1-A1, HSP101, YUCCA2, and MYB73 manifested significant differences in expression between 23 and 26 °C at 50 DAT, where a critical limit temperature of heat tolerance and heat stress may exist; therefore, these genes may be helpful as the probe to check the heat-related characteristics in wheat breeding. There are regional limitations, where the average temperature during the cultivation season is below 26 °C. The optimal range is between 20 and 23 °C, and the degree of activity during early vegetative growth becomes a vital trait for ensuring stable wheat production. This trait is anticipated to pose a challenging target for future wheat breeding in the Republic of Korea.

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References

  • Ahn H, Jo K, Jeong D, Pak M, Hur J, Jung W, Kim S (2019) PropaNet: time-varying condition-specific transcriptional network construction by network propagation. Front Plant Sci 10:698

    Article  PubMed Central  PubMed  Google Scholar 

  • Akter N, Islam MR (2017) Heat stress effects and management in wheat. A review. Agronomy Sustain Dev 37:1–17

    CAS  Google Scholar 

  • Alonso-Peral MM, Oliver SN, Casao MC, Greenup AA, Trevaskis B (2011) The promoter of the cereal VERNALIZATION1 gene is sufficient for transcriptional induction by prolonged cold. PLoS ONE 6(12):e29456

    Article  CAS  PubMed Central  ADS  PubMed  Google Scholar 

  • Asseng S, Ewert F, Martre P, Rötter RP, Lobell DB et al (2015) Rising temperatures reduce global wheat production. Nat Clim Chang 5(2):143–147

    Article  ADS  Google Scholar 

  • Babbar R, Karpinska B, Grover A, Foyer CH (2021) Heat-induced oxidation of the nuclei and cytosol. Front Plant Sci 11:617779

    Article  PubMed Central  PubMed  Google Scholar 

  • Blázquez MA, Nelson DC, Weijers D (2020) Evolution of plant hormone response pathways. Annu Rev Plant Biol 71:327–353

    Article  PubMed  Google Scholar 

  • Dias AS, Bagulho AS, Lidon FC (2008) Ultrastructure and biochemical traits of bread and durum wheat grains under heat stress. Braz J Plant Physiol 20:323–333

    Article  Google Scholar 

  • Dixon LE, Karsai I, Kiss T, Adamski NM, Liu Z, Ding Y, Allard V, Boden SA, Griffiths S (2019) VERNALIZATION1 controls developmental responses of winter wheat under high ambient temperatures. Development. 146(3): dev172684.

  • Farooq M, Bramley H, Palta JA, Siddique KH (2011) Heat stress in wheat during reproductive and grain-filling phases. Crit Rev Plant Sci 30(6):491–507

    Article  Google Scholar 

  • Gong M, van der Luit AH, Knight MR, Trewavas AJ (1998) Heat-shock-induced changes in intracellular Ca2+ level in tobacco seedlings in relation to thermotolerance. Plant Physiol 116(1):429–437

    Article  CAS  PubMed Central  Google Scholar 

  • Gupta NK, Agarwal S, Agarwal VP, Nathawat NS, Gupta S, Singh G (2013) Effect of short-term heat stress on growth, physiology and antioxidative defence system in wheat seedlings. Acta Physiol Plant 35:1837–1842

    Article  CAS  Google Scholar 

  • Heo JH, Seong HJ, Yang WH, Jung W (2020) Growth responses and differences in gene expression depending on cultivation temperature between alternative type wheat varieties. J Crop Sci Biotechnol 23:47–55

    Article  Google Scholar 

  • Jang SJ, Shin SH, Yee ST, Hwang B, Im KH, Park KY (2005) Effects of abiotic stresses on cell cycle progression in tobacco BY-2 cells. Mol Cells. 20(1)

  • Jung JH, Domijan M, Klose C, Biswas S, Ezer D, Gao M, Khattak AK, Box MS, Charoensawan V, Cortijo S, Kumar M, Grant A, Locke JC, Schäfer E, Jaeger KE, Wigge PA (2016) Phytochromes function as thermosensors in Arabidopsis. Science 354(6314):886–889

    Article  CAS  ADS  PubMed  Google Scholar 

  • Kang CS, Cheong YK, Kim KH, Kim HS, Kim YJ et al (2014) A wheat variety, “Sooan” with good noodle quality, red grain wheat, higher winter hardiness and pre-harvest sprouting resistance. Korean J Breeding Sci. 46(3):260–267

    Article  Google Scholar 

  • Khan Z, Shahwar D (2020) Role of heat shock proteins (HSPs) and heat stress tolerance in crop plants. Sustain Agricult Era Clim Change. 211–234

  • Khanna-Chopra R (2012) Leaf senescence and abiotic stresses share reactive oxygen species-mediated chloroplast degradation. Protoplasma 249(3):460–481

    Article  Google Scholar 

  • Kosová K, Vítámvás P, Prášil IT, Renaut J (2011) Plant proteome changes under abiotic stress—contribution of proteomics studies to understanding plant stress response. J Proteomics 74(8):1301–1322

    Article  PubMed  Google Scholar 

  • Kotak S, Larkindale J, Lee U, von Koskull-Döring P, Vierling E, Scharf KD (2007) Complexity of the heat stress response in plants. Curr Opin Plant Biol 10(3):310–316

    Article  CAS  PubMed  Google Scholar 

  • Ku JH, Lee MS, Song JW, Lee HJ, Park SK (2000) Effect of rootzone cooling on growth of cool-season turfgrasses during summer season. Korean J Horticult Sci Technol 18(1)

  • Kumar RR, Goswami S, Singh K, Dubey K, Rai GK et al (2018) Characterization of novel heat-responsive transcription factor (TaHSFA6e) gene involved in regulation of heat shock proteins (HSPs)—A key member of heat stress-tolerance network of wheat. J Biotechnol 279:1–12

    Article  PubMed  Google Scholar 

  • Kumar RR, Arora K, Goswami S, Sakhare A, Singh B, Chinnusamy V, Praveen S (2020) MAPK enzymes: a ROS activated signaling sensors involved in modulating heat stress response, tolerance and grain stability of wheat under heat stress. 3 Biotech. 10: 1–11

  • Li C, Liang Y, Chen C, Li J, Xu Y, Xu Z, Ma H, Chong K (2006) Cloning and expression analysis of TSK1, a wheat SKP1 homologue, and functional comparison with Arabidopsis ASK1 in male meiosis and auxin signalling. Funct Plant Biol 33(4):381–390

    Article  CAS  PubMed  Google Scholar 

  • Li B, Gao K, Ren H, Tang W (2018) Molecular mechanisms governing plant responses to high temperatures. J Integr Plant Biol 60(9):757–779

    Article  PubMed  Google Scholar 

  • Liu A, Yu Y, Duan X, Sun X, Duanmu H, Zhu Y (2015a) GsSKP21, a Glycine soja S- phase kinase-associated protein, mediates the regulation of plant alkaline tolerance and ABA sensitivity. Plant Mol Biol 87(1–2):111–124

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Feng L, Li J, He Z (2015b) Genetic and epigenetic control of plant heat responses. Front Plant Sci 6: 267

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real- time quantitative PCR and the 2− ΔΔCT method. Methods 25(4):402–408

    Article  CAS  PubMed  Google Scholar 

  • Luo MC, Gu YQ, Puiu D, Wang H, Twardziok SO et al (2017) Genome sequence of the progenitor of the wheat D genome Aegilops tauschii. Nature 551(7681):498–502

    Article  CAS  PubMed Central  ADS  PubMed  Google Scholar 

  • Luo Y, Liu X, Li W (2021) Exogenously-supplied trehalose inhibits the growth of wheat seedlings under high temperature by affecting plant hormone levels and cell cycle processes. Plant Signaling and Behavior, 1907043

  • Matsukura S, Mizoi J, Yoshida T, Todaka D, Ito Y, Maruyama K, Shinozaki K, Yamaguchi-Shinozaki K (2010) Comprehensive analysis of rice DREB2-type genes that encode transcription factors involved in the expression of abiotic stress- responsive genes. Mol Genet Genomics 283(2):185–196

    Article  CAS  PubMed  Google Scholar 

  • Mazzoni-Putman SM, Brumos J, Zhao C, Alonso JM, Stepanova AN (2021) Auxin interactions with other hormones in plant development. Cold Spring Harb Perspect Biol 13(10):a039990

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Oh E, Zhu JY, Bai MY, Arenhart RA, Sun Y, Wang ZY (2014) Cell elongation is regulated through a central circuit of interacting transcription factors in the Arabidopsis hypocotyl. Elife 3:e03031

    Article  PubMed Central  PubMed  Google Scholar 

  • Ohama N, Sato H, Shinozaki K, Yamaguchi-Shinozaki K (2017) Transcriptional regulatory network of plant heat stress response. Trends Plant Sci 22(1):53–65

    Article  CAS  PubMed  Google Scholar 

  • Prasad P, Djanaguiraman M (2014) 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 41(12):1261–1269

    Article  CAS  PubMed  Google Scholar 

  • Qi F, Zhang F (2020) Cell cycle regulation in the plant response to stress. Front Plant Sci 10:1765

    Article  PubMed Central  PubMed  Google Scholar 

  • Qiao L, Zhang W, Li X, Zhang L, Zhang X, Li X, Guo H, Ren Y, Zheng J, Chang Z (2018) Characterization and expression patterns of auxin response factors in wheat. Front Plant Sci 9:1395

    Article  PubMed Central  PubMed  Google Scholar 

  • Quint M, Delker C, Franklin KA, Wigge PA, Halliday KJ, van Zanten M (2016) Molecular and genetic control of plant thermomorphogenesis. Nat Plants. 2(1):1–9

    Article  Google Scholar 

  • Raines CA (2011) Increasing photosynthetic carbon assimilation in C3 plants to improve crop yield: current and future strategies. Plant Physiol 155(1):36–42

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Roberts DM, Harmon AC (1992) Calcium-modulated proteins: targets of intracellular calcium signals in higher plants. Annu Rev Plant Biol 43(1):375–414

    Article  CAS  Google Scholar 

  • Sajid M, Rashid B, Ali Q, Husnain T (2018) Mechanisms of heat sensing and responses in plants. It is not all about Ca 2+ ions. Biologia Plantarum. 62(3): 409–420

  • Song J, Liu Q, Hu B, Wu W (2017) Photoreceptor PhyB involved in Arabidopsis temperature perception and heat-tolerance formation. Int J Mol Sci 18(6):1194

    Article  PubMed Central  PubMed  Google Scholar 

  • Wang F, Huo SN, Guo J, Zhang XS (2006) Wheat D-type cyclin Triae; CYCD2; 1 regulate development of transgenic Arabidopsis plants. Planta 224(5):1129–1140

    Article  CAS  PubMed  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. Nat Commun 7(1):1–11

    Google Scholar 

  • Wilkinson S, Kudoyarova GR, Veselov DS, Arkhipova TN, Davies WJ (2012) Plant hormone interactions: innovative targets for crop breeding and management. J Exp Bot 63(9):3499–3509

    Article  CAS  PubMed  Google Scholar 

  • Yan L, Loukoianov A, Blechl A, Tranquilli G, Ramakrishna W, SanMiguel P, Bennetzen JL, Echenique V, Dubcovsky J (2004) The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science 303(5664):1640–1644

    Article  CAS  PubMed Central  ADS  PubMed  Google Scholar 

  • Yan L, Fu D, Li C, Blechl A, Tranquilli G, Bonafede M, Sanchez A, Valarik M, Yasuda S, Dubcovsky J (2006) The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proc Natl Acad Sci 103(51):19581–19586

    Article  CAS  PubMed Central  ADS  PubMed  Google Scholar 

  • Zhang B, Wang X, Wang X, Ma L, Wang Z, Zhang X (2018) Molecular characterization of a novel vernalization allele Vrn-B1d and its effect on heading time in Chinese wheat (Triticum aestivum L.) landrace Hongchunmai. Mol Breeding. 38(10): 1–10

  • Zhao Q, Zhou L, Liu J, Du X, Asad MA, Huang F, Pan G, Cheng F (2018) Relationship of ROS accumulation and superoxide dismutase isozymes in developing anther with floret fertility of rice under heat stress. Plant Physiol Biochem 122:90–101

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by the Agenda Project (PJ015289022023) of the Rural Development Administration, Republic of Korea. WJ designed the project. HS carried out the experiment, and JH supported the fieldwork. WJ and HS biologically interpreted the results and wrote the paper.

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Correspondence to Woosuk Jung.

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This work was supported by the Agenda Project (PJ015289022023) of the Rural Development Administration, Republic of Korea.

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Seong, H., Heo, J.H. & Jung, W. Gene expression analysis of wheat (Triticum aestivum L.) during the vegetative stage under high ambient temperature condition. J. Crop Sci. Biotechnol. 27, 261–272 (2024). https://doi.org/10.1007/s12892-023-00228-x

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