The DREB2C.L-IAGLU module contributes to long-term heat stress via sugar metabolism in cucumber

Xiao Ma , Chuang Li , Yong Yuan , Xitong Zhong , Yafei Huang , Jiacai Chen , Yan Geng , Yuyan Li , Zhaoyang Zhou , Ming Xin , Xiaolan Zhang , Jianyu Zhao

Horticulture Research ›› 2026, Vol. 13 ›› Issue (3) : 341

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Horticulture Research ›› 2026, Vol. 13 ›› Issue (3) :341 DOI: 10.1093/hr/uhaf341
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The DREB2C.L-IAGLU module contributes to long-term heat stress via sugar metabolism in cucumber
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Abstract

Cucumber is an important vegetable crop with thermophilic but heat-sensitive growth characteristics. Heat stress threatens cucumber growth and development, leading to a decline in both quality and yield. However, the evaluation system and molec- ular mechanism of long-term heat tolerance remain unclear. Here, an evaluation system in response to long-term heat stress was established, and chlorophyll a content and catalase(CAT) activity were identified as key evaluation indices for determining the heat tolerance of cucumber seedlings. Transcriptomic and physiological analyses revealed that sugar metabolism played a pivotal role in the heat response. Notably, the expression of CsIAGLU (Indoleacetic Acid glucosyltransferase) was significantly upregulated in heat-tolerant genotype PS76, whereas it was not induced in the heat-sensitive genotype PWRG. Loss of function of CsIAGLU by gene editing resulted in increased sensitivity to heat stress along with higher sugar contents, accelerated stomatal closure, and chlorophyll degradation. Furthermore, CsDREB2C.L, a positive regulator of heat stress response, directly bound to the CsIAGLU promoter to enhance its expression. Overexpression of CsDREB2C.L and CsIAGLU maintained stable sugar contents, thereby keeping stomatal opening and sustaining leaf greening to resist heat stress. Taken together, our findings provide valuable insights into the mechanism of heat resistance in cucumber.

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Xiao Ma, Chuang Li, Yong Yuan, Xitong Zhong, Yafei Huang, Jiacai Chen, Yan Geng, Yuyan Li, Zhaoyang Zhou, Ming Xin, Xiaolan Zhang, Jianyu Zhao. The DREB2C.L-IAGLU module contributes to long-term heat stress via sugar metabolism in cucumber. Horticulture Research, 2026, 13 (3) : 341 DOI:10.1093/hr/uhaf341

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Acknowledgements

This work was supported by the National Natural Science Foun-dation of China (32402569, 32025033, and 32372699), China Post-doctoral Science Foundation (2023M733805), the PhD Scientific Research and Innovation Foundation of Sanya Yazhou Bay Science and Technology City (HSPHDSRF-2023-05-013), and Pinduoduo-China Agricultural University Research Fund (PC2023B01002).

Authors contributions

J.Z., X.Z., M.X., Z.Z, and X.M. designed the research. X.M., C.L., and X.Z. performed the experiments. J.C. performed the gene edit-ing. X.Z., Y.H., Y.Y., Y.G., and Y.L. provided experimental assistance. X.Z., J.Z., and X.M. wrote the paper; all the authors revised the manuscript.

Data availability

The data that support the findings of this study are included in the manuscript or supplementary materials. The RNA-seq data have been deposited in the China National Center for Bioinformation National Genomics Data Center (https://ngdc.cncb.ac.cn/) under accession number CRA025585.

Conflicts of interest statement

The authors declare that they have no conflict of interest.

Supplementary material

Supplementary material is available at Horticulture Research online.

References

[1]

Huang J, Zhao X, Bürger M. et al. Two interacting ethylene response factors regulate heat stress response. Plant Cell. 2021; 33:338-57

[2]

Kerbler SM, Wigge PA. Temperature sensing in plants. Annu Rev Plant Biol. 2023; 74:341-66

[3]

Zhao C, Liu B, Piao S. et al. Temperature increase reduces global yields of major crops in four independent estimates. Proc Natl Acad Sci USA. 2017; 114:9326-31

[4]

Lesk C, Rowhani P, Ramankutty N. Influence of extreme weather disasters on global crop production. Nature. 2016; 529:84-7

[5]

Zahra N, Hafeez MB, Ghaffar A. et al. Plant photosynthesis under heat stress: effects and management. Environ Exp Bot. 2023; 206:105178

[6]

Gommers C. Keep cool and open up: temperature-induced stomatal opening. Plant Physiol. 2020; 182:1188-9

[7]

Liang Y, Xie W, Yang C. et al. A quick and effective method for thermostability differentiation in cucumber ( Cucumis sativus L.). Physiol Plant. 2024; 176:1-14

[8]

Zhang S, Ye H, Kong L. et al. Multivariate analysis compares and evaluates heat tolerance of potato germplasm. Plants. 2024; 13:1-17

[9]

Shi Q, Liu Z, Gao W. et al. Identification of heat tolerance and screening of heat tolerance indexes in different Chinese cabbage seedlings. Sci Hortic. 2023; 322:112381

[10]

Asim M, Zhang Y, Sun Y. et al. Leaf senescence attributes: the novel and emerging role of sugars as signaling molecules and the overlap of sugars and hormones signaling nodes. Crit Rev Biotechnol. 2023; 43:1092-110

[11]

Liu, Chen G, He M. et al. ABI5 promotes heat stress-induced chlorophyll degradation by modulating the stability of MYB44 in cucumber. Hortic Res. 2023; 10:1-13

[12]

Zhu X, Chen J, Xie Z. et al. Jasmonic acid promotes degreening via MYC2/3/4- and ANAC019/055/072-mediated regulation of major chlorophyll catabolic genes. Plant J. 2015; 84:597-610

[13]

Sato H, Mizoi J, Shinozaki K. et al. Complex plant responses to drought and heat stress under climate change. Plant J. 2024; 117:1873-92

[14]

Zhang H, Zhu J, Gong Z. et al. Abiotic stress responses in plants. Nat Rev Genet. 2021; 23:104-19

[15]

Dong N, Sun Y, Guo T. et al. UDP-GLUCOSYLTRANSFERASE regulates grain size and abiotic stress tolerance associated with metabolic flux redirection in rice. Nat Commun. 2020; 11:11

[16]

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

[17]

Sakuma Y, Maruyama K, Qin F. et al. Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc Natl Acad Sci USA. 2006; 103:18822-7

[18]

Xie DL, Huang HM, Zhou CY. et al. HsfA1a confers pollen thermotolerance through upregulating antioxidant capacity, protein repair, and degradation in Solanum lycopersicum L. Hortic Res. 2022; 9:1-14

[19]

Schramm F, Larkindale J, Kiehlmann E. et al. A cascade of transcription factor DREB2A and heat stress transcription factor HsfA3 regulates the heat stress response of Arabidopsis. Plant J. 2008; 53:264-74

[20]

Wang F, Liu Y, Shi Y. et al. SUMoylation stabilizes the transcription factor DREB2A to improve plant thermotolerance. Plant Physiol. 2020; 183:41-50

[21]

Dong S, Zhang S, Wei S. et al. Identification of quantitative trait loci controlling high-temperature tolerance in cucumber ( Cucumis sativus L.) seedlings. Plants. 2020; 9:1-11

[22]

Sun Y, Zang C, Yao T. et al. Research advances on heat tolerance of cucumber in China. China Fruit Veg. 2018; 38:57-62

[23]

Yu B, Yan S, Zhou H. et al. Overexpression of CsCaM3 improves high temperature tolerance in cucumber. Front Plant Sci. 2018; 9:1-14

[24]

Liu Y, Dong S, Bo K. et al. QTL mapping of heat tolerance in cucumber (Cucumis sativus L.) at adult stage. Plants. 2021; 10:1-14

[25]

Chen X, Wang Z, Tang R. et al. Genome-wide identification and expression analysis of Hsf and Hsp gene families in cucumber (Cucumis sativus L.). Plant Growth Regul. 2021; 95:223-39

[26]

Liang Y, Yang C, Ming F. et al. A bHLH transcription factor, CsSPT, regulates high-temperature resistance in cucumber. Hortic Plant J. 2024; 10:503-14

[27]

Chen J, Huang Y, Liu X. et al. CsIAGLU regulates the angle of leaf petiole by affecting endogenous content of auxin in cucumber (Cucumis sativus L.). Genes. 2022; 13:13

[28]

Huang J, Hai Z, Wang R. et al. Genome-wide analysis of HSP20 gene family and expression patterns under heat stress in cucumber ( Cucumis sativus L.). Front. Plant Sci. 2022; 13:13

[29]

Kelly G, Moshelion M, David-Schwartz R. et al. Hexokinase mediates stomatal closure. Plant J. 2013; 75:977-88

[30]

Zait Y, Zhu M, Ando E. et al. Apoplastic metabolomics reveals sugars as mesophyll messengers regulating guard cell ion transport under red light. Nat Plants. 2025; 11:1847-62

[31]

Mateo-Bonmatí E, Casanova-Sáez R, Šimura J. et al. Broadening the roles of UDP-GLYCOSYLTRANSFERASES in auxin homeostasis and plant development. New Phytol. 2021; 232:642-54

[32]

Brunoni F, Collani S, Casanova-Sáez R. et al. Conifers exhibit a characteristic inactivation of auxin to maintain tissue homeostasis. New Phytol. 2020; 226:1753-65

[33]

Wang Z, Dong S, Liu Y. et al. A genome-wide association study identifies candidate genes for heat tolerance in adult cucumber plants. Hortic Plant J. 2025; 11:774-87

[34]

Salvi P, Agarrwal R, Kajal. et al. Sugar transporters and their molecular tradeoffs during abiotic stress responses in plants. Physiol Plant. 2022; 174:e13652

[35]

Jeandet P, Formela-Luboińska M, Labudda M. et al. The role of sugars in plant responses to stress and their regulatory function during development. Int J Mol Sci. 2022; 23:5161

[36]

Li G, Zhao Y. The critical roles of three sugar-related proteins (HXK, SnRK1, TOR) in regulating plant growth and stress responses. Hortic Res. 2024;11:uhae099

[37]

Sun L, Sui X, Lucas WJ. et al. Down-regulation of the sucrose transporter CsSUT1 causes male sterility by altering. Plant Physiol. 2019; 180:986-97

[38]

Li Y, Liu H, Yao X. et al. Hexose transporter CsSWEET7a in cucumber mediates phloem unloading in companion cells for fruit development. Plant Physiol. 2021; 186:640-54

[39]

Moore CE, Meacham-Hensold K, Lemonnier P. et al. The effect of increasing temperature on crop photosynthesis: from enzymes to ecosystems. J Exp Bot. 2021; 72:2822-44

[40]

Lin Y, Zhou YN, Liang XG. et al. Exogenous methylglyoxal alleviates drought-induced ‘plant diabetes’ and leaf senescence in maize. J Exp Bot. 2023; 75:1982-96

[41]

Chaplin AK, Chernukhin I, Bechtold U. Profiling of advanced glycation end products uncovers abiotic stress-specific target proteins in Arabidopsis. J Exp Bot. 2019; 70:653-70

[42]

Asim M, Guo M, Khan R. et al. Investigation of sugar signaling behaviors involved in sucrose-induced senescence initiation and progression in N. tabacum. Plant Physiol Biochem. 2022; 184:112-25

[43]

Huai B, Yuan P, Ma X. et al. Sugar transporter TaSTP3 activation by TaWRKY19/61/82 enhances stripe rust susceptibility in wheat. New Phytol. 2022; 236:266-82

[44]

Li P, Li YJ, Zhang FJ. et al. The Arabidopsis UDP-GLYCOSYLTRANSFERASES UGT79B2 and UGT79B3, contribute to cold, salt and drought stress tolerance via modulating anthocyanin accumulation. Plant J. 2017; 89:85-103

[45]

Gao R, Han T, Xun H. et al. MYB transcription factors GmMYBA2 and GmMYBR function in a feedback loop to control pigmentation of seed coat in soybean. J Exp Bot. 2021; 72:4401-18

[46]

Yan S, Yu B, Ming F. et al. CsIVP modulates low nitrogen and high-temperature resistance in cucumber. Plant Cell Physiol. 2022; 63:605-17

[47]

Chen H, Eun J, Ju C. et al. Arabidopsis DREB2C functions as a transcriptional activator of HsfA3 during the heat stress response. Biochem Biophys Res Commun. 2010; 401:238-44

[48]

Ding R, Che X, Shen Z. et al. Metabolome and transcriptome profiling provide insights into green apple peel reveals light-and UV-B-responsive pathway in anthocyanins accumulation. BMC Plant Biol. 2021; 21:351

[49]

Liao Y, Smyth GK, Shi W. FeatureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2014; 30:923-30

[50]

Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014; 15:1-21

[51]

Kanehisa M, Araki M, Goto S. et al. KEGG for linking genomes to life and the environment. Nucleic Acids Res. 2008;36:D480-4

[52]

Gene Ontology Consortium. Gene ontology consortium: going forward. Nucleic Acids Res. 2015;43:D1049-56

[53]

Xin T, Tian H, Ma Y. et al. Targeted creation of new mutants with compact plant architecture using CRISPR/Cas9 genome editing by an optimized genetic transformation procedure in cucurbit plants. Hortic Res. 2022;9:uhab086

[54]

Shang Y, Ma Y, Zhou Y. et al. Biosynthesis, regulation, and domestication of bitterness in cucumber. Science. 2014; 346:1084-8

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