CIRCADIAN CLOCK-ASSOCIATED 1 represses thermotolerance by inhibiting HEAT SHOCK FACTOR A2 expression in nonheading Chinese cabbage

Ying He , Dong Xiao , Xlin Hou , Yiran Li , Hongfang Zhu

Horticulture Research ›› 2026, Vol. 13 ›› Issue (5) : 33

PDF (2132KB)
Horticulture Research ›› 2026, Vol. 13 ›› Issue (5) :33 DOI: 10.1093/hr/uhag033
Articles
research-article
CIRCADIAN CLOCK-ASSOCIATED 1 represses thermotolerance by inhibiting HEAT SHOCK FACTOR A2 expression in nonheading Chinese cabbage
Author information +
History +
PDF (2132KB)

Abstract

In the context of global warming, elevated temperatures present serious challenges to the growth, quality, and productivity of nonheading Chinese cabbage (NHCC). Understanding the mechanisms underlying thermotolerance in NHCCs is therefore critically important. In this study, we investigated the influence of heat stress (HS) duration and circadian rhythm on gene expression using time-resolved transcriptome sequencing. The results showed that during the early stages of HS, NHCC primarily engaged in physiological processes such as stimulus perception and signal transduction. In contrast, prolonged HS exposure activated antioxidant metabolism, reduced photosynthetic capacity, and accelerated leaf senescence. Weighted gene coexpression network analysis (WGCNA) further revealed a strong link between circadian regulation and HS responses. Notably, our findings demonstrate that the core circadian clock component CIRCADIAN CLOCK ASSOCIATED 1 (BcCCA1) negatively regulated heat tolerance by repressing the transcription of BcHSFA2. Collectively, these results provide new insights into the molecular mechanisms underlying HS responses in NHCCs and highlight the regulatory role of circadian rhythms in plant thermotolerance.

Cite this article

Download citation ▾
Ying He, Dong Xiao, Xlin Hou, Yiran Li, Hongfang Zhu. CIRCADIAN CLOCK-ASSOCIATED 1 represses thermotolerance by inhibiting HEAT SHOCK FACTOR A2 expression in nonheading Chinese cabbage. Horticulture Research, 2026, 13 (5) : 33 DOI:10.1093/hr/uhag033

登录浏览全文

4963

注册一个新账户 忘记密码

Acknowledgements

This work was supported by the Shanghai Agricultural Science and Technology Innovation Program (Grant No. K2023015) and Project supported by the Education Department of Hainan Province, project number: Hnjg2025ZD-98.

Author contributions

H.Z. and X.H. provided financial support. D.X. and Y.H. designed and conceived the study. Y.H. performed the experiments and data analysis. D.X. and Y.H. wrote the paper. D.X. and H.Z. revised the manuscript. Y.L. coordinated the study. All the authors read and approved the final manuscript.

Data availability

The data that support the findings of this study will be available in NCBI at (https://dataview.ncbi.nlm.nih.gov/object/PRJNA1282857?reviewer=toselqsndcsesnqickjshkfh36).

Conflicts of interest statement

The authors declare no conflicts of interest.

Supplementary material

Supplementary material is available at Horticulture Research online.

References

[1]

Li Y, Liu GF, Ma LM, et al. A chromosome-level reference genome of non-heading Chinese cabbage [ Brassica campestris (syn. Brassica rapa) ssp. chinensis] . Hortic Res. 2020; 7: 212.

[2]

Yue L, Li G, Dai Y, et al. Gene co-expression network analysis of the heat-responsive core transcriptome identifies hub genes in Brassica rapa . Planta. 2021; 253: 111.

[3]

Angadi SV, Cutforth HW, Miller PR, et al. Response of three Brassica species to high temperature stress during reproductive growth. Can J Plant Sci . 2000; 80: 693-701.

[4]

Balla K, Karsai I, Bónis P, et al. Heat stress responses in a large set of winter wheat cultivars (Triticum aestivum L.) depend on the timing and duration of stress . PLoS One. 2019; 14: e0222639.

[5]

Wahid A, Gelani S, Ashraf M, et al. Heat tolerance in plants: an overview. Environ Exp Bot . 2007; 61: 199-223.

[6]

Zinn KE, Tunc-Ozdemir M, Harper JF . Temperature stress and plant sexual reproduction: uncovering the weakest links. J Exp Bot. 2010; 61: 1959-68.

[7]

Bac-Molenaar JA, Fradin EF, Becker FF, et al. Genome-wide association mapping of fertility reduction upon heat stress reveals developmental stage-specific QTLs in Arabidopsis thaliana . Plant Cell. 2015; 27: 1857-74.

[8]

Xu J, Wolters-Arts M, Mariani C, et al. Heat stress affects vegetative and reproductive performance and trait correlations in tomato (Solanum lycopersicum) . Euphytica. 2017; 213: 156.

[9]

Blain GC . The modified Mann-Kendall test: on the performance of three variance correction approaches. Bragantia. 2013; 72: 416-25.

[10]

Chen J, Tang L, Shi P, et al. Effects of short-term post-anthesis high-temperature stress on dynamic process of accumulation of grain protein and its composition in rice (Oryza sativa L.) . Brazilian J Bot. 2016; 40: 49-58.

[11]

Wang L, Ma KB, Lu ZG, et al. Differential physiological, transcriptomic and metabolomic responses of Arabidopsis leaves under prolonged warming and heat shock. BMC Plant Biol. 2020; 20: 86.

[12]

Shi P, Zhu Y, Tang L, et al. Differential effects of temperature and duration of heat stress during anthesis and grain filling stages in rice. Environ Exp Bot . 2016; 132: 28-41.

[13]

Xalxo R, Yadu B, Chandra J, et al. Alteration in Carbohydrate Metabolism Modulates Thermotolerance of Plant under Heat Stress. Wiley; 2020: 77-115.

[14]

Nosaka Y, Nosaka AY . Generation and detection of reactive oxygen species in photocatalysis. Chem Rev. 2017; 117: 11302-36.

[15]

Liu J, Feng L, Li J, et al. Genetic and epigenetic control of plant heat responses. Front Plant Sci. 2015; 6: 267.

[16]

Strenkert D, Schmollinger S, Sommer F, et al. Transcription factor-dependent chromatin remodeling at heat shock and copper-responsive promoters in Chlamydomonas reinhardtii . Plant Cell. 2011; 23: 2285-301.

[17]

Ling Y, Mahfouz MM, Zhou S . Pre-mRNA alternative splicing as a modulator for heat stress response in plants. Trends Plant Sci. 2021; 26: 1153-70.

[18]

Kim YK, Jang SK . Continuous heat shock enhances translational initiation directed by internal ribosomal entry site. Biochem Biophys Res Commun. 2002; 297: 224-31.

[19]

Fang NN, Zhu M, Rose A, et al. Deubiquitinase activity is required for the proteasomal degradation of misfolded cytosolic proteins upon heat-stress. Nat Commun. 2016; 7: 12907.

[20]

Song WF, Zhao LJ, Zhang XM, et al. Effect of timing of heat stress during grain filling in two wheat varieties under moderate and very high temperature. Indian J Genetics Plant Breed . 2015; 75: 121.

[21]

Xu X, Xie Q . LNKs-RVEs complex ticks in the circadian gating of plant temperature stress responses. Stress Biology. 2023; 3: 1-4.

[22]

Geonhee H, Park J, Kim S, et al. Overexpression of BBX18 promotes thermomorphogenesis through the PRR5. Front Plant Sci . 2021; 12: 782352.

[23]

Jang J, Lee S, Kim J-I, et al. The roles of circadian clock genes in plant temperature stress responses. Int J Mol Sci . 2024; 25(2): 918.

[24]

Zhu JY, Oh E, Wang T, et al. TOC1-PIF4 interaction mediates the circadian gating of thermoresponsive growth in Arabidopsis. Nat Commun. 2016; 7(1): 13692.

[25]

Harmer SL . The circadian system in higher plants. Annu Rev Plant Biol. 2009; 60: 357-77.

[26]

Dodd AN, Salathia N, Hall A, et al. Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science. 2005; 309: 630-3.

[27]

Michael TP, Salomé PA, Yu HJ, et al. Enhanced fitness conferred by naturally occurring variation in the circadian clock. Science. 2003; 302: 1049-53.

[28]

Yakir E, Hilman D, Harir Y, et al. Regulation of output from the plant circadian clock. FEBS J. 2007; 274: 335-45.

[29]

Grinevich DO, Desai JS, Stroup KP, et al. Novel transcriptional responses to heat revealed by turning up the heat at night. Plant Mol Biol . 2019; 101: 1-19.

[30]

Eckardt NA . Temperature entrainment of the Arabidopsis circadian clock. Plant Cell . 2005; 17: 645-7.

[31]

McClung CR, Davis SJ . Ambient thermometers in plants: from physiological outputs towards mechanisms of thermal sensing. Curr Biol. 2010; 20: R1086-92.

[32]

Thines B, Harmon FG . Ambient temperature response establishes ELF3 as a required component of the core Arabidopsis circadian clock. Proc Natl Acad Sci USA. 2010; 107: 3257-62.

[33]

Karayekov E, Sellaro R, Legris M, et al. Heat shock-induced fluctuations in clock and light signaling enhance phytochrome B-mediated Arabidopsis deetiolation. Plant Cell. 2013; 25: 2892-906.

[34]

Gould PD, Locke JC, Larue C, et al. The molecular basis of temperature compensation in the Arabidopsis circadian clock. Plant Cell. 2006; 18: 1177-87.

[35]

Salome PA , Weigel D , McClung CR . The role of the Arabidopsis morning loop components CCA1, LHY, PRR7, and PRR9 in temperature compensation. Plant Cell. 2010; 22: 3650-61.

[36]

Yu J, Li P, Tu S, et al. Integrated analysis of the transcriptome and metabolome of Brassica rapa revealed regulatory mechanism under heat stress . Int J Mol Sci. 2023; 24: 13993.

[37]

Tabusam J, Shi Q, Feng D, et al. HSP70 gene family in Brassica rapa: genome-wide identification, characterization, and expression patterns in response to heat and cold stress . Cells. 2022; 11.

[38]

Yin L, Sun Y, Chen X, et al. Genome-wide analysis of the HD-zip gene family in Chinese cabbage (Brassica rapa subsp. pekinensis) and the expression pattern at high temperatures and in carotenoids regulation . Agronomy. 2023; 13(5): 1324.

[39]

Liu G, Xia Y, Liu T, et al. The DNA methylome and association of differentially methylated regions with differential gene expression during heat stress in Brassica rapa . Int J Mol Sci. 2018; 19(5): 1414.

[40]

Challinor AJ, Watson J, Lobell DB, et al. A meta-analysis of crop yield under climate change and adaptation. Nat Clim Chang. 2014; 4: 287-91.

[41]

Murcia G, Nieto C, Sellaro R, et al. Hysteresis in PHYTOCHROME-INTERACTING FACTOR 4 and EARLY-FLOWERING 3 dynamics dominates warm daytime memory in Arabidopsis. Plant Cell. 2022; 34: 2188-204.

[42]

Jones MA, Morohashi K, Grotewold E, et al. Arabidopsis JMJD5/JMJ30 acts independently of LUX ARRHYTHMO within the plant circadian clock to enable temperature compensation. Front Plant Sci. 2019; 10: 57.

[43]

Liu G, Wang J, Hou X . Transcriptome-wide N(6)-methyladenosine (m(6)A) methylome profiling of heat stress in Pak-choi (Brassica rapa ssp. chinensis) . Plants (Basel). 2020; 9(9): 1080.

[44]

Monks DE, Aghoram K, Courtney PD, et al. Hyperosmotic stress induces the rapid phosphorylation of a soybean phosphatidylinositol transfer protein homolog through activation of the protein kinases SPK1 and SPK2. Plant Cell . 2001; 13: 1205-19.

[45]

Kato M, Nagasaki-Takeuchi N, Ide Y, et al. PCaPs, possible regulators of PtdInsP signals on plasma membrane. Plant Signal Behav. 2010; 5: 848-50.

[46]

Ali U, Lu S, Fadlalla T, et al. The functions of phospholipases and their hydrolysis products in plant growth, development and stress responses. Prog Lipid Res . 2022; 86: 101158.

[47]

Suzuki N, Bajad S, Shuman J, et al. The transcriptional co-activator MBF1c is a key regulator of thermotolerance in Arabidopsis thaliana . J Biol Chem. 2008; 283: 9269-75.

[48]

Suzuki N, Sejima H, Tam R, et al. Identification of the MBF1 heat-response regulon of Arabidopsis thaliana . Plant J. 2011; 66: 844-51.

[49]

Guihur A, Rebeaud ME, Goloubinoff P . How do plants feel the heat and survive? Trends Biochem Sci. 2022; 47: 824-38.

[50]

Shamsi IH, Jiang S, Hussain N, et al. Coordinate role of ascorbate-glutathione in response to abiotic stresses. In: Anjum NA, Umar S, Chan M-T, eds. Ascorbate-Glutathione Pathway and Stress Tolerance in Plants. Springer Netherlands: Dordrecht, 2010, 323-36.

[51]

Zhang Y, Min H, Shi C, et al. Transcriptome analysis of the role of autophagy in plant response to heat stress. PLoS One. 2021; 16: e0247783.

[52]

Islam MR, Feng B, Cheng T, et al. Role of abscisic acid in thermal acclimation of plants. J Plant Biol. 2018; 61: 255-64.

[53]

Masclaux-Daubresse C , Chen Q , Havé M . Regulation of nutrient recycling via autophagy. Curr Opin Plant Biol . 2017; 39: 8-17.

[54]

Chen S-T, He N-Y, Chen J-H, et al. Identification of core subunits of photosystem II as action sites of HSP21, which is activated by the GUN5-mediated retrograde pathway in Arabidopsis. Plant J. 2017; 89: 1106-18.

[55]

Li N, Euring D, Cha JY, et al. Plant hormone-mediated regulation of heat tolerance in response to global climate change. Front Plant Sci. 2020; 11: 627969.

[56]

Poor P, Nawaz K, Gupta R, et al. Ethylene involvement in the regulation of heat stress tolerance in plants. Plant Cell Rep . 2022; 41: 675-98.

[57]

Zhang XL, Jiang L, Xin Q, et al. Structural basis and functions of abscisic acid receptors PYLs. Front Plant Sci . 2015; 6: 88.

[58]

Rehman A, Azhar MT, Hinze L, et al. Insight into abscisic acid perception and signaling to increase plant tolerance to abiotic stress. J Plant Interact. 2021; 16: 222-37.

[59]

Fujioka S, Yokota T . Biosynthesis and metabolism of brassinosteroids. Annu Rev Plant Biol. 2003; 54: 137-64.

[60]

Fatma M, Asgher M, Iqbal N, et al. Ethylene signaling under stressful environments: analyzing collaborative knowledge. Plants (Basel) . 2022; 11(17): 2211.

[61]

Xie Z, Nolan TM, Jiang H, et al. AP2/ERF transcription factor regulatory networks in hormone and abiotic stress responses in Arabidopsis. Front Plant Sci. 2019; 10: 228.

[62]

Singh P, Arif Y, Miszczuk E, et al. Specific roles of lipoxygenases in development and responses to stress in plants. Plants (Basel) . 2022; 11(7): 979.

[63]

Khan MIR, Kumari S, Nazir F, et al. Defensive role of plant hormones in advancing abiotic stress-resistant rice plants. Rice Sci . 2023; 30: 15-35.

[64]

Du H, Liu H, Xiong L . Endogenous auxin and jasmonic acid levels are differentially modulated by abiotic stresses in rice. Front Plant Sci . 2013; 4: 397.

[65]

Jajic I, Sarna T, Strzalka K . Senescence, stress, and reactive oxygen species. Plants (Basel) . 2015; 4: 393-411.

[66]

Jespersen D, Yu J, Huang B . Metabolite responses to exogenous application of nitrogen, cytokinin, and ethylene inhibitors in relation to heat-induced senescence in creeping bentgrass. PLoS One. 2015; 10: e0123744.

[67]

Mishra SK, Chaudhary C, Baliyan S, et al. Heat-stress-responsive HvHSFA2e gene regulates the heat and drought tolerance in barley through modulation of phytohormone and secondary metabolic pathways. Plant Cell Rep. 2024; 43: 172.

[68]

Szabados L, Savouré A . Proline: a multifunctional amino acid. Trends Plant Sci. 2010; 15: 89-97.

[69]

Dakhiya Y, Green R . The importance of the circadian system for adaptation to heat wave stress in wild barley (Hordeum spontaneum) . Environ Exp Bot. 2023; 206: 105152.

[70]

Tamaru T, Ikeda M . Circadian adaptation to cell injury stresses: a crucial interplay of BMAL1 and HSF1. J Physiol Sci. 2016; 66: 303-6.

[71]

Blair EJ, Bonnot T, Hummel M, et al. Contribution of time of day and the circadian clock to the heat stress responsive transcriptome in Arabidopsis. Sci Rep . 2019; 9: 4814.

[72]

Liu HC, Lämke J, Lin SY, et al. Distinct heat shock factors and chromatin modifications mediate the organ-autonomous transcriptional memory of heat stress. Plant J. 2018; 95: 401-13.

[73]

Ohama N, Sato H, Shinozaki K, et al. Transcriptional regulatory network of plant heat stress response. Trends Plant Sci . 2017; 22: 53-65.

[74]

Guo M, Long Y, Xu L, et al. CELL CYCLE SWITCH 52 regulates tillering by interacting with LATERAL SUPPRESSOR in non-heading Chinese cabbage. Plant Sci. 2021; 309: 110934.

PDF (2132KB)

199

Accesses

0

Citation

Detail

Sections
Recommended

/