[en] Dehydration response element binding (DREB) transcription factors play a pivotal role in plant abiotic stress responses, but its evolutionary and functional characterization in buckwheat remains unexplored. Here, we conducted a comprehensive analysis of the DREB gene family across three buckwheat species, revealing segmental duplication as the primary driver of family expansion and potential purifying selection during evolution. A FtDREB02 gene, classified as group A2, was identified through Genome-wide association analysis (GWAS) on drought tolerance and delphinidin content. Functional validation in Arabidopsis thaliana and hairy root of Tartary buckwheat (Fagopyrum tataricum) demonstrated that overexpression of this gene promotes delphinidin biosynthesis and enhances plant resistance to water scarcity. Through the integration of DAP-seq and PEG transcriptome cluster analysis, A FtANS candidate was screened. Functional studies showed that FtDREB02 regulates delphinidin content by binding directly to DRE elements of FtANS promoter. This research identifies and comprehensively analyzes the DREB family within buckwheat species, elucidating the regulatory mechanisms of FtDREB02 in controlling flavonoid biosynthesis and drought resistance, providing potential genetic resources for breeding buckwheat varieties with excellent agronomic traits.
Disciplines :
Agriculture & agronomy Chemistry
Author, co-author :
Wang, Jing ; Université de Liège - ULiège > TERRA Research Centre ; National Key Facility for Crop Gene Resources and Genetic Improvement Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, China ; Sanya Nan Fan Research Institute, Chinese Academy of Agricultural Sciences, Sanya, Hainan, China
Chen, Yanhua; National Key Facility for Crop Gene Resources and Genetic Improvement Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, China ; Sanya Nan Fan Research Institute, Chinese Academy of Agricultural Sciences, Sanya, Hainan, China
Dongqing, Fan; National Key Facility for Crop Gene Resources and Genetic Improvement Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, China ; Sanya Nan Fan Research Institute, Chinese Academy of Agricultural Sciences, Sanya, Hainan, China
He, Yuqi
Guan, Chaonan; National Key Facility for Crop Gene Resources and Genetic Improvement Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, China ; Sanya Nan Fan Research Institute, Chinese Academy of Agricultural Sciences, Sanya, Hainan, China
Shi, Yaliang; National Key Facility for Crop Gene Resources and Genetic Improvement Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, China
Wang, Xiangru; National Key Facility for Crop Gene Resources and Genetic Improvement Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, China
Lin, Hao; National Key Facility for Crop Gene Resources and Genetic Improvement Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, China
Fauconnier, Marie-Laure ; Université de Liège - ULiège > Département GxABT > Chemistry for Sustainable Food and Environmental Systems (CSFES)
Purcaro, Giorgia ; Université de Liège - ULiège > Département GxABT > Chemistry for Sustainable Food and Environmental Systems (CSFES)
Quinet, Muriel; Groupe de Recherche en Physiologie Végétale (GRPV) Earth and Life Institute-Agronomy (ELI-A), Université Catholique de Louvain Croix du Sud 45, Louvain-la-Neuve, Belgium
Genva, Manon ; Université de Liège - ULiège > Département GxABT > Chemistry for Sustainable Food and Environmental Systems (CSFES)
Jha, Rintu; National Key Facility for Crop Gene Resources and Genetic Improvement Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, China
Zhang, Kaixuan; National Key Facility for Crop Gene Resources and Genetic Improvement Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, China ; Sanya Nan Fan Research Institute, Chinese Academy of Agricultural Sciences, Sanya, Hainan, China
Zhou, Meiliang; National Key Facility for Crop Gene Resources and Genetic Improvement Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, China ; Sanya Nan Fan Research Institute, Chinese Academy of Agricultural Sciences, Sanya, Hainan, China
This research was supported by the National Key Research andDevelopment Program of China (2022YFE0140800) and theNational High-level University Graduate Scholarship Program ofthe China Scholarship Council (202303250057).
Agarwal, P.K., Gupta, K., Lopato, S. & Agarwal, P. (2017) Dehydration responsive element binding transcription factors and their applications for the engineering of stress tolerance. Journal of Experimental Botany, 68, 2135–2148. Available from: https://doi.org/10.1093/jxb/erx118
An, J.P., Zhang, X.W., Bi, S.Q., You, C.X., Wang, X.F. & Hao, Y.J. (2020) The ERF transcription factor MdERF38 promotes drought stress-induced anthocyanin biosynthesis in apple. The Plant Journal, 101, 573–589. Available from: https://doi.org/10.1111/tpj.14555
Barton, K.E. & Koricheva, J. (2010) The ontogeny of plant defense and herbivory: characterizing general patterns using meta-analysis. The American Naturalist, 175, 481–493. Available from: https://doi.org/10.1086/650722
Cella Pizarro, L. & Bisigato, A.J. (2010) Allocation of biomass and photoassimilates in juvenile plants of six Patagonian species in response to five water supply regimes. Annals of Botany, 106, 297–307. Available from: https://doi.org/10.1093/aob/mcq109
Changan, S.S., Kumar, V. & Tyagi, A. (2023) Expression pattern of candidate genes and their correlation with various metabolites of abscisic acid biosynthetic pathway under drought stress in rice. Physiologia Plantarum, 175, e14102. Available from: https://doi.org/10.1111/ppl.14102
Chen, C., Chen, H., Zhang, Y., Thomas, H.R., Frank, M.H., He, Y. et al. (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Molecular Plant, 13, 1194–1202. Available from: https://doi.org/10.1016/j.molp.2020.06.009
Clough, S.J. & Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal, 16, 735–743. Available from: https://doi.org/10.1046/j.1365-313x.1998.00343.x
Cui, M., Zhang, W., Zhang, Q., Xu, Z., Zhu, Z., Duan, F. et al. (2011) Induced over-expression of the transcription factor OsDREB2A improves drought tolerance in rice. Plant Physiology and Biochemistry, 49, 1384–1391. Available from: https://doi.org/10.1016/j.plaphy.2011.09.012
Du, W., Yang, J., Li, Q., Jiang, W. & Pang, Y. (2024) Medicago truncatula β-glucosidase 17 contributes to drought and salt tolerance through antioxidant flavonoid accumulation. Plant, Cell & Environment, 47, 3076–3089. Available from: https://doi.org/10.1111/pce.14928
Dubouzet, J.G., Sakuma, Y., Ito, Y., Kasuga, M., Dubouzet, E.G., Miura, S. et al. (2003) OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. The Plant Journal, 33, 751–763. Available from: https://doi.org/10.1046/j.1365-313X.2003.01661.x
Fang, Z.W., Xu, X.Y., Gao, J.F., Wang, P.K., Liu, Z.X. & Feng, B.L. (2015) Characterization of FeDREB1 promoter involved in cold- and drought-inducible expression from common buckwheat (Fagopyrum esculentum). Genetics and Molecular Research, 14, 7990–8000. Available from: https://doi.org/10.4238/2015.July.17.7
Flagel, L.E. & Wendel, J.F. (2009) Gene duplication and evolutionary novelty in plants. The New Phytologist, 183, 557–564. Available from: https://doi.org/10.1111/j.1469-8137.2009.02923.x
Fujita, Y., Fujita, M., Satoh, R., Maruyama, K., Parvez, M.M., Seki, M. et al. (2005) AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell, 17, 3470–3488. Available from: https://doi.org/10.1105/tpc.105.035659
Gahlaut, V., Jaiswal, V., Kumar, A. & Gupta, P.K. (2016) Transcription factors involved in drought tolerance and their possible role in developing drought tolerant cultivars with emphasis on wheat (Triticum aestivum L.). Theoretical and Applied Genetics, 129, 2019–2042. Available from: https://doi.org/10.1007/s00122-016-2794-z
Gao, Y., Shi, Y., Jahan, T., Huda, M.N., Hao, L., He, Y. et al. (2025) Buckwheat UDP-glycosyltransferase FtUGT71K6 and FtUGT71K7 tandem repeats contribute to drought tolerance by regulating epicatechin synthesis. Plant, Cell & Environment, 48, 4066–4082. Available from: https://doi.org/10.1111/pce.15412
González-Villagra, J., Cohen, J.D. & Reyes-Díaz, M.M. (2019) Abscisic acid is involved in phenolic compounds biosynthesis, mainly anthocyanins, in leaves of Aristotelia chilensis plants (Mol.) subjected to drought stress. Physiologia Plantarum, 165, 855–866. Available from: https://doi.org/10.1111/ppl.12789
Guo, F., Guan, R., Sun, X., Zhang, C., Shan, C., Liu, M. et al. (2023) Integrated metabolome and transcriptome analyses of anthocyanin biosynthesis reveal key candidate genes involved in colour variation of Scutellaria baicalensis flowers. BMC Plant Biology, 23, 643. Available from: https://doi.org/10.1186/s12870-023-04591-3
He, J., Hao, Y., He, Y., Li, W., Shi, Y., Khurshid, M. et al. (2024) Genome-wide associated study identifies FtPMEI13 gene conferring drought resistance in Tartary buckwheat. The Plant Journal, 120, 2398–2419. Available from: https://doi.org/10.1111/tpj.17119
He, M., He, Y., Zhang, K., Lu, X., Zhang, X., Gao, B. et al. (2022) Comparison of buckwheat genomes reveals the genetic basis of metabolomic divergence and ecotype differentiation. The New Phytologist, 235, 1927–1943. Available from: https://doi.org/10.1111/nph.18306
Heinz, S., Benner, C., Spann, N., Bertolino, E., Lin, Y.C., Laslo, P. et al. (2010) Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Molecular Cell, 38, 576–589. Available from: https://doi.org/10.1016/j.molcel.2010.05.004
Hinojosa-Gómez, J., San Martín-Hernández, C., Heredia, J.B., León-Félix, J., Osuna-Enciso, T. & Muy-Rangel, M.D. (2020) Anthocyanin induction by drought stress in the calyx of roselle cultivars. Molecules, 25, 1555. Available from: https://doi.org/10.3390/molecules25071555
Hou, S.Y., Du, W., Hao, Y.R., Han, Y.H., Li, H.Y., Liu, L.L. et al. (2021) Elucidation of the regulatory network of flavonoid biosynthesis by profiling the metabolome and transcriptome in Tartary buckwheat. Journal of Agricultural and Food Chemistry, 69, 7218–7229. Available from: https://doi.org/10.1021/acs.jafc.1c00190
Hu, X., Liang, J., Wang, W., Cai, C., Ye, S., Wang, N. et al. (2023) Comprehensive genome-wide analysis of the DREB gene family in Moso bamboo (Phyllostachys edulis): evidence for the role of PeDREB28 in plant abiotic stress response. The Plant Journal, 116, 1248–1270. Available from: https://doi.org/10.1111/tpj.16420
Hu, Y., Chen, X. & Shen, X. (2022) Regulatory network established by transcription factors transmits drought stress signals in plant. Stress Biology, 2, 26. Available from: https://doi.org/10.1007/s44154-022-00048-z
Huala, E. (2001) The Arabidopsis information resource (TAIR): a comprehensive database and web-based information retrieval, analysis, and visualization system for a model plant. Nucleic Acids Research, 29, 102–105. Available from: https://doi.org/10.1093/nar/29.1.102
Huang, J., Chen, Q., Rong, Y., Tang, B., Zhu, L., Ren, R. et al. (2021) Transcriptome analysis revealed gene regulatory network involved in PEG-induced drought stress in Tartary buckwheat (Fagopyrum tararicum). PeerJ, 9, e11136. Available from: https://doi.org/10.7717/peerj.11136
Huang, Y., Du, B., Yu, M., Cao, Y., Liang, K. & Zhang, L. (2024) Picea wilsonii NAC31 and DREB2A cooperatively activate ERD1 to modulate drought resistance in transgenic Arabidopsis. International Journal of Molecular Sciences, 25, 2037. Available from: https://doi.org/10.3390/ijms25042037
Jha, R., Zhang, K., He, Y., Mendler-Drienyovszki, N., Magyar-Tábori, K., Quinet, M. et al. (2024) Global nutritional challenges and opportunities: buckwheat, a potential bridge between nutrient deficiency and food security. Trends in Food Science and Technology, 145, 104365. Available from: https://doi.org/10.1016/j.tifs.2024.104365
Jing, R., Li, H.Q., HU, C.L., Jiang, Y.P., Qin, L.P. & Zheng, C.J. (2016) Phytochemical and pharmacological profiles of three fagopyrum buckwheats. International Journal of Molecular Sciences, 17, 589. Available from: https://doi.org/10.3390/ijms17040589
Jogawat, A., Yadav, B., Chhaya, Lakra,., NSingh, A.K. & Narayan, O.P. (2021) Crosstalk between phytohormones and secondary metabolites in the drought stress tolerance of crop plants: a review. Physiologia Plantarum, 172, 1106–1132. Available from: https://doi.org/10.1111/ppl.13328
Karki, A., Horvath, D.P. & Sutton, F. (2013) Induction of DREB2A pathway with repression of E2F, jasmonic acid biosynthetic and photosynthesis pathways in cold acclimation-specific freeze-resistant wheat crown. Functional & Integrative Genomics, 13, 57–65. Available from: https://doi.org/10.1007/s10142-012-0303-2
Khan, S.A., Li, M.Z., Wang, S.M. & Yin, H.J. (2018) Revisiting the role of plant transcription factors in the battle against abiotic stress. International Journal of Molecular Sciences, 19, 1634. Available from: https://doi.org/10.3390/ijms19061634
Kershaw, K.A. & Levitt, J. (1973) Responses of plants to environmental stresses. The Bryologist, 76, 328. Available from: https://doi.org/10.2307/3241344
Kidokoro, S., Konoura, I., Soma, F., Suzuki, T., Miyakawa, T., Tanokura, M. et al. (2023) Clock-regulated coactivators selectively control gene expression in response to different temperature stress conditions in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 120, e2216183120. Available from: https://doi.org/10.1073/pnas.2216183120
Kim, S., Kang, J.Y., Cho, D.I., Park, J.H. & Kim, S.Y. (2004) ABF2, an ABRE-binding bZIP factor, is an essential component of glucose signaling and its overexpression affects multiple stress tolerance. The Plant Journal, 40, 75–87. Available from: https://doi.org/10.1111/j.1365-313X.2004.02192.x
Kizis, D. & Pagès, M. (2002) Maize DRE-binding proteins DBF1 and DBF2 are involved in rab17 regulation through the drought-responsive element in an ABA-dependent pathway. The Plant Journal, 30, 679–689. Available from: https://doi.org/10.1046/j.1365-313X.2002.01325.x
Kumar, S., Muthuvel, J., Sadhukhan, A., Kobayashi, Y., Koyama, H. & Sahoo, L. (2022) Enhanced osmotic adjustment, antioxidant defense, and photosynthesis efficiency under drought and heat stress of transgenic cowpea overexpressing an engineered DREB transcription factor. Plant Physiology and Biochemistry, 193, 1–13. Available from: https://doi.org/10.1016/j.plaphy.2022.09.028
La, V.H., Tran, D.H., Han, V.-C., Nguyen, T.D., Duong, V.C., Nguyen, V.H. et al. (2023) Drought stress-responsive abscisic acid and salicylic acid crosstalk with the phenylpropanoid pathway in soybean seeds. Physiologia Plantarum, 175, e14050. Available from: https://doi.org/10.1111/ppl.14050
Lai, D., Zhang, K., He, Y., Fan, Y., Li, W., Shi, Y. et al. (2024) Multi-omics identification of a key glycosyl hydrolase gene FtGH1 involved in rutin hydrolysis in Tartary buckwheat (Fagopyrum tataricum). Plant Biotechnology Journal, 22, 1206–1223. Available from: https://doi.org/10.1111/pbi.14259
Langfelder, P. & Horvath, S. (2008) WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics, 9, 559. Available from: https://doi.org/10.1186/1471-2105-9-559
Lata, C. & Prasad, M. (2011) Role of DREBs in regulation of abiotic stress responses in plants. Journal of Experimental Botany, 62, 4731–4748. Available from: https://doi.org/10.1093/jxb/err210
Lee, B.-R., Park, S.-H., Muchlas, M., La, V.H., Al Mamun, M., Bae, D.-W. et al. (2023) Differential response of phenylpropanoid pathway as linked to hormonal change in two Brassica napus cultivars contrasting drought tolerance. Physiologia Plantarum, 175, e14115. Available from: https://doi.org/10.1111/ppl.14115
Li, J., Zhang, K., Meng, Y., Li, Q., Ding, M. & Zhou, M. (2019) FtMYB16 interacts with Ftimportin-α1 to regulate rutin biosynthesis in tartary buckwheat. Plant Biotechnology Journal, 17, 1479–1481. Available from: https://doi.org/10.1111/pbi.13121
Li, M., Yao, T., Lin, W., Hinckley, W.E., Galli, M., Muchero, W. et al. (2023) Double DAP-seq uncovered synergistic DNA binding of interacting bZIP transcription factors. Nature Communications, 14, 2600. Available from: https://doi.org/10.1038/s41467-023-38096-2
Li, X., Qi, S., Meng, L., Su, P., Sun, Y., Li, N. et al. (2025) Genome-wide identification of the wall-associated kinase gene family and their expression patterns under various abiotic stresses in soybean (Glycine max (L.) Merr). Frontiers in Plant Science, 15, 1511681. Available from: https://doi.org/10.3389/fpls.2024.1511681
Li, X.-L., Meng, D., Li, M.-J., Zhou, J., Yang, Y.-Z., Zhou, B.-B. et al. (2023) Transcription factors MhDREB2A/MhZAT10 play a role in drought and cold stress response crosstalk in apple. Plant Physiology, 192, 2203–2220. Available from: https://doi.org/10.1093/plphys/kiad147
Li, Y., Zheng, Y.P., Zhou, X.H., Yang, X.M., He, X.R., Feng, Q. et al. (2021) Rice miR1432 fine-tunes the balance of yield and blast disease resistance via different modules. Rice, 14, 87. Available from: https://doi.org/10.1186/s12284-021-00529-1
Liang, Z. & Schnable, J.C. (2018) Functional divergence between subgenomes and gene pairs after whole genome duplications. Molecular Plant, 11, 388–397. Available from: https://doi.org/10.1016/j.molp.2017.12.010
Lin, H., Yao, Y.J., Sun, P.C., Feng, L.D., Wang, S., Ren, Y.M. et al. (2023) Haplotype-resolved genomes of two buckwheat crops provide insights into their contrasted rutin concentrations and reproductive systems. BMC Plant Biology, 21, 87. Available from: https://doi.org/10.1186/s12915-023-01587-1
Liu, M., Sun, W., Ma, Z., Zheng, T., Huang, L., Wu, Q. et al. (2019) Genome-wide investigation of the AP2/ERF gene family in Tartary buckwheat (Fagopyum tataricum). BMC Plant Biology, 19, 84. Available from: https://doi.org/10.1186/s12870-019-1681-6
Liu, Q., Kasuga, M., Sakuma, Y., Abe, H., Miura, S., Yamaguchi-Shinozaki, K. et al. (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell, 10, 1391–1406. Available from: https://doi.org/10.1105/tpc.10.8.1391
Liu, Y., Zhu, Q. & Zhu, N. (2008) Recent duplication and positive selection of the GAGE gene family. Genetica, 133, 31–35. Available from: https://doi.org/10.1007/s10709-007-9179-9
Magadum, S., Banerjee, U., Murugan, P., Gangapur, D. & Ravikesavan, R. (2013) Gene duplication as a major force in evolution. Journal of Genetics, 92, 155–161. Available from: https://doi.org/10.1007/s12041-013-0212-8
Májeková, M., Martínková, J. & Hájek, T. (2019) Grassland plants show no relationship between leaf drought tolerance and soil moisture affinity, but rapidly adjust to changes in soil moisture. Functional Ecology, 33, 774–785. Available from: https://doi.org/10.1111/1365-2435.13312
Marinho, J.P., Coutinho, I.D., da Fonseca Lameiro, R., Marin, S.R.R., Colnago, L.A., Nakashima, K. et al. (2019) Metabolic alterations in conventional and genetically modified soybean plants with GmDREB2A;2 FL and GmDREB2A;2 CA transcription factors during water deficit. Plant Physiology and Biochemistry, 140, 122–135. Available from: https://doi.org/10.1016/j.plaphy.2019.04.040
Meena, R.P., Ghosh, G., Vishwakarma, H. & Padaria, J.C. (2022) Expression of a Pennisetum glaucum gene DREB2A confers enhanced heat, drought and salinity tolerance in transgenic Arabidopsis. Molecular Biology Reports, 49, 7347–7358. Available from: https://doi.org/10.1007/s11033-022-07527-6
Mei, F., Chen, B., Du, L., Li, S., Zhu, D., Chen, N. et al. (2022) A gain-of-function allele of a DREB transcription factor gene ameliorates drought tolerance in wheat. Plant Cell, 34, 4472–4494. Available from: https://doi.org/10.1093/plcell/koac248
Metz, J., Lampei, C., Bäumler, L., Bocherens, H., Dittberner, H., Henneberg, L. et al. (2020) Rapid adaptive evolution to drought in a subset of plant traits in a large-scale climate change experiment. Ecology Letters, 23, 1643–1653. Available from: https://doi.org/10.1111/ele.13596
Mittler, R. & Zilinskas, B.A. (1994) Regulation of pea cytosolic ascorbate peroxidase and other antioxidant enzymes during the progression of drought stress and following recovery from drought. The Plant Journal, 5, 397–405. Available from: https://doi.org/10.1111/j.1365-313x.1994.00397.x
Morran, S., Eini, O., Pyvovarenko, T., Parent, B., Singh, R., Ismagul, A. et al. (2011) Improvement of stress tolerance of wheat and barley by modulation of expression of DREB/CBF factors. Plant Biotechnology Journal, 9, 230–249. Available from: https://doi.org/10.1111/j.1467-7652.2010.00547.x
Nakabayashi, R., Yonekura-Sakakibara, K., Urano, K., Suzuki, M., Yamada, Y., Nishizawa, T. et al. (2014) Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids. The Plant Journal, 77, 367–379. Available from: https://doi.org/10.1111/tpj.12388
Ober, D. (2005) Seeing double: gene duplication and diversification in plant secondary metabolism. Trends in Plant Science, 10, 444–449. Available from: https://doi.org/10.1016/j.tplants.2005.07.007
Oksana, S., Marek, K., Marian, B. & Marek, Z. (2023) Cultivar-dependent and drought-induced modulation of secondary metabolites, adaptative defense in Fagopyrum esculentum L. Physiology and Molecular Biology of Plants, 29, 1605–1618. Available from: https://doi.org/10.1007/s12298-023-01376-8
Otekunrin, O.A. (2021) Is Africa ready for the SDG 2 (zero hunger) target by 2030? Current Agriculture Research Journal, 9. Available from: https://doi.org/10.12944/CARJ.9.1.01
Panchy, N., Lehti-Shiu, M. & Shiu, S.-H. (2016) Evolution of gene duplication inplants. Plant Physiology, 171, 2294–2316. Available from: https://doi.org/10.1104/pp.16.00523
Qin, F., Kakimoto, M., Sakuma, Y., Maruyama, K., Osakabe, Y., Tran, L.-S.P. et al. (2007) Regulation and functional analysis of ZmDREB2A in response to drought and heat stresses in Zea mays L. The Plant Journal, 50, 54–69. Available from: https://doi.org/10.1111/j.1365-313X.2007.03034.x
Qin, F., Sakuma, Y., Tran, L.-S.P., Maruyama, K., Kidokoro, S., Fujita, Y. et al. (2008) Arabidopsis DREB2A-interacting proteins function as RING E3 ligases and negatively regulate plant drought stress-responsive gene expression. Plant Cell, 20, 1693–1707. Available from: https://doi.org/10.1105/tpc.107.057380
Quinlan, A.R. & Hall, I.M. (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics, 26, 841–842. Available from: https://doi.org/10.1093/bioinformatics/btq033
Rauschkolb, R., Li, Z., Godefroid, S., Dixon, L., Durka, W., Májeková, M. et al. (2022) Evolution of plant drought strategies and herbivore tolerance after two decades of climate change. The New Phytologist, 235, 773–785. Available from: https://doi.org/10.1111/nph.18125
Reis, R.R., Brito, A.D., da Cunha, B., Martins, P.K., Martins, M.T.B., Alekcevetch, J.C. et al. (2014) Induced over-expression of AtDREB2A CA improves drought tolerance in sugarcane. Plant Science, 221–222, 59–68. Available from: https://doi.org/10.1016/j.plantsci.2014.02.003
Ren, M., Wang, Z., Xue, M., Wang, X., Zhang, F., Zhang, Y. et al. (2019) Constitutive expression of an A-5 subgroup member in the DREB transcription factor subfamily from Ammopiptanthus mongolicus enhanced abiotic stress tolerance and anthocyanin accumulation in transgenic Arabidopsis. PLoS One, 14, e0224296. Available from: https://doi.org/10.1371/journal.pone.0224296
Ren, Y., Zhang, S., Zhao, Q., Wu, Y. & Li, H. (2023) The CsMYB123 and CsbHLH111 are involved in drought stress-induced anthocyanin biosynthesis in Chaenomeles speciosa. Molecular Horticulture, 3, 25. Available from: https://doi.org/10.1186/s43897-023-00071-2
Riechmann, J.L. & Meyerowitz, E.M. (1998) The AP2/EREBP family of plant transcription factors. Biological Chemistry, 379, 633–654. Available from: https://doi.org/10.1515/bchm.1998.379.6.633
Sadhukhan, A., Panda, S.K. & Sahoo, L. (2014) The cowpea RING ubiquitin ligase VuDRIP interacts with transcription factor VuDREB2A for regulating abiotic stress responses. Plant Physiology and Biochemistry, 83, 51–56. Available from: https://doi.org/10.1016/j.plaphy.2014.07.007
Sakuma, Y., Maruyama, K., Qin, F., Osakabe, Y., Shinozaki, K. & Yamaguchi-Shinozaki, K. (2006) Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proceedings of the National Academy of Sciences of the United States of America, 103, 18822–18827. Available from: https://doi.org/10.1073/pnas.0605639103
Santiago, J., Rodrigues, A., Saez, A., Rubio, S., Antoni, R., Dupeux, F. et al. (2009) Modulation of drought resistance by the abscisic acid receptor PYL5 through inhibition of clade a PP2Cs. The Plant Journal, 60, 575–588. Available from: https://doi.org/10.1111/j.1365-313X.2009.03981.x
Sarkar, T., Thankappan, R., Mishra, G.P. & Nawade, B.D. (2019) Advances in the development and use of DREB for improved abiotic stress tolerance in transgenic crop plants. Physiology and Molecular Biology of Plants, 25, 1323–1334. Available from: https://doi.org/10.1007/s12298-019-00711-2
Seth, P. & Sebastian, J. (2024) Plants and global warming: challenges and strategies for a warming world. Plant Cell Reports, 43, 27. Available from: https://doi.org/10.1007/s00299-023-03083-w
Sharma, H., Chawla, N. & Dhatt, A.S. (2022) Role of phenylalanine/tyrosine ammonia lyase and anthocyanidin synthase enzymes for anthocyanin biosynthesis in developing Solanum melongena L. genotypes. Physiologia Plantarum, 174, e13756. Available from: https://doi.org/10.1111/ppl.13756
Shi, D., Jouannet, V., Agustí, J., Kaul, V., Levitsky, V., Sanchez, P. et al. (2021) Tissue-specific transcriptome profiling of the Arabidopsis inflorescence stem reveals local cellular signatures. The Plant Cell, 33, 200–223. Available from: https://doi.org/10.1093/plcell/koaa019
Song, T., Huo, Q., Li, C., Wang, Q., Cheng, L., Qi, W. et al. (2024) The biosynthesis of storage reserves and auxin is coordinated by a hierarchical regulatory network in maize endosperm. The New Phytologist, 243, 1855–1869. Available from: https://doi.org/10.1111/nph.19949
Sun, W., Xu, Z., Song, C. & Chen, S. (2022) Herbgenomics: decipher molecular genetics of medicinal plants. The Innovation, 3, 100322. Available from: https://doi.org/10.1016/j.xinn.2022.100322
Tarolli, P. & Zhao, W. (2023) Drought in agriculture: preservation, adaptation, migration. The Innovation Geoscience, 1, 100002. Available from: https://doi.org/10.59717/j.xinn-geo.2023.100002
Tiedge, K., Li, X., Merrill, A.T., Davisson, D., Chen, Y., Yu, P. et al. (2022) Comparative transcriptomics and metabolomics reveal specialized metabolite drought stress responses in switchgrass (Panicum virgatum). The New Phytologist, 236, 1393–1408. Available from: https://doi.org/10.1111/nph.18443
Vonapartis, E., Mohamed, D., Li, J., Pan, W., Wu, J. & Gazzarrini, S. (2022) CBF4/DREB1D represses XERICO to attenuate ABA, osmotic and drought stress responses in Arabidopsis. The Plant Journal, 110, 961–977. Available from: https://doi.org/10.1111/tpj.15713
Wang, A., Liu, Y., Li, Q., Li, X., Zhang, X., Kong, J. et al. (2023) FlbZIP12 gene enhances drought tolerance via modulating flavonoid biosynthesis in Fagopyrum leptopodum. Frontiers in Plant Science, 14, 1279468. Available from: https://doi.org/10.3389/fpls.2023.1279468
Wang, F., Harindintwali, J.D., Wei, K., Shan, Y., Mi, Z., Costello, M.J. et al. (2023) Climate change: strategies for mitigation and adaptation. Innovative Geosciences, 1, 100015–100037. Available from: https://doi.org/10.59717/j.xinn-geo.2023.100015
Wang, Q., Guan, Y., Wu, Y., Chen, H., Chen, F. & Chu, C. (2008) Overexpression of a rice OsDREB1F gene increases salt, drought, and low temperature tolerance in both Arabidopsis and rice. Plant Molecular Biology, 67, 589–602. Available from: https://doi.org/10.1007/s11103-008-9340-6
Wang, Z., Yung, W.-S., Gao, Y., Huang, C., Zhao, X., Chen, Y. et al. (2024) From phenotyping to genetic mapping: identifying water-stress adaptations in legume root traits. BMC Plant Biology, 24, 749. Available from: https://doi.org/10.1186/s12870-024-05477-8
Wei, H., Wang, X., Wang, K., Tang, X., Zhang, N. & Si, H. (2024) Transcription factors as molecular switches regulating plant responses to drought stress. Physiologia Plantarum, 176, e14366. Available from: https://doi.org/10.1111/ppl.14366
Wei, T., Deng, K., Liu, D., Gao, Y., Liu, Y., Yang, M. et al. (2016) Ectopic expression of DREB transcription factor, AtDREB1A, confers tolerance to drought in transgenic Salvia miltiorrhiza. Plant & Cell Physiology, 57, 1593–1609. Available from: https://doi.org/10.1093/pcp/pcw084
Wen, W., Li, Z., Shao, J., Tang, Y., Zhao, Z., Yang, J. et al. (2021) The distribution and sustainable utilization of buckwheat resources under climate change in China. Plants, 10, 2081. Available from: https://doi.org/10.3390/plants10102081
Wu, Z., Liu, S., Zhao, J., Wang, F., Du, Y., Zou, S. et al. (2017) Comparative responses to silicon and selenium in relation to antioxidant enzyme system and the glutathione-ascorbate cycle in flowering Chinese cabbage (Brassica campestris L. ssp. chinensis var. utilis) under cadmium stress. Environmental and Experimental Botany, 133, 1–11. Available from: https://doi.org/10.1016/j.envexpbot.2016.09.005
Xu, Y., Hu, W., Song, S., Ye, X., Ding, Z., Liu, J. et al. (2023) MaDREB1F confers cold and drought stress resistance through common regulation of hormone synthesis and protectant metabolite contents in banana. Horticultural Research, 10, uhac275. Available from: https://doi.org/10.1093/hr/uhac275
Yang, Q., Zhang, Y., Qu, X., Wu, F., Li, X., Ren, M. et al. (2023) Genome-wide analysis of UDP-glycosyltransferases family and identification of UGT genes involved in abiotic stress and flavonol biosynthesis in Nicotiana tabacum. BMC Plant Biology, 23, 204. Available from: https://doi.org/10.1186/s12870-023-04208-9
Yang, X., Zhu, X., Wei, J., Li, W., Wang, H., Xu, Y. et al. (2022) Primary root response to combined drought and heat stress is regulated via salicylic acid metabolism in maize. BMC Plant Biology, 22, 417. Available from: https://doi.org/10.1186/s12870-022-03805-4
Yaschenko, A.E., Fenech, M., Mazzoni-Putman, S., Alonso, J.M. & Stepanova, A.N. (2022) Deciphering the molecular basis of tissue-specific gene expression in plants: can synthetic biology help? Current Opinion in Plant Biology, 68, 102241. Available from: https://doi.org/10.1016/j.pbi.2022.102241
Yin, J. & Slater, L. (2023) Understanding heatwave-drought compound hazards and impacts on socio-ecosystems. The Innovation Geoscience, 1, 100042–3. Available from: https://doi.org/10.59717/j.xinn-geo.2023.100042
Yu, G., Wang, L.G. & He, Q.Y. (2015) ChIPseeker: an R/Bioconductor package for ChIP peak annotation, comparison and visualization. Bioinformatics, 31, 2382–2383. Available from: https://doi.org/10.1093/bioinformatics/btv145
Zhang, H., Zhao, Y. & Zhu, J.K. (2020) Thriving under stress: how plants balance growth and the stress response. Developmental Cell, 55, 529–543. Available from: https://doi.org/10.1016/j.devcel.2020.10.012
Zhang, K., He, M., Fan, Y., Zhao, H., Gao, B., Yang, K. et al. (2021) Resequencing of global Tartary buckwheat accessions reveals multiple domestication events and key loci associated with agronomic traits. Genome Biology, 22(1), 23. Available from: https://doi.org/10.1186/s13059-020-02217-7
Zhang, K., He, Y., Lu, X., Shi, Y., Zhao, H., Li, X. et al. (2023) Comparative and population genomics of buckwheat species reveal key determinants of flavor and fertility. Molecular Plant, 16, 1427–1444. Available from: https://doi.org/10.1016/j.molp.2023.08.013
Zhang, K., Logacheva, M.D., Meng, Y., Hu, J., Wan, D., Li, L. et al. (2018) Jasmonate-responsive MYB factors spatially repress rutin biosynthesis in Fagopyrum tataricum. Journal of Experimental Botany, 69, 1955–1966. Available from: https://doi.org/10.1093/jxb/ery032
Zhang, L., Li, X., Ma, B., Gao, Q., Du, H., Han, Y. et al. (2017) The Tartary buckwheat genome provides insights into rutin biosynthesis and abiotic stress tolerance. Molecular Plant, 10, 1224–1237. Available from: https://doi.org/10.1016/j.molp.2017.08.013
Zhang, T.T., Lin, Y.J., Liu, H.F., Liu, Y.Q., Zeng, Z.F., Lu, X.Y. et al. (2024) The AP2/ERF transcription factor MdDREB2A regulates nitrogen utilisation and sucrose transport under drought stress. Plant, Cell & Environment, 47, 1668–1684. Available from: https://doi.org/10.1111/pce.14834
Zhang, X., He, Y., Li, L., Liu, H. & Hong, G. (2021) Involvement of the R2R3-MYB transcription factor MYB21 and its homologs in regulating flavonol accumulation in Arabidopsis stamen. Journal of Experimental Botany, 72, 4319–4332. Available from: https://doi.org/10.1093/jxb/erab156
Zhang, Y., Liu, T., Meyer, C.A., Eeckhoute, J., Johnson, D.S., Bernstein, B.E. et al. (2008) Model-based analysis of ChIP-Seq (MACS). Genome Biology, 9, R137. Available from: https://doi.org/10.1186/gb-2008-9-9-r137
Zhao, C., Liu, X., Gong, Q., Cao, J., Shen, W., Yin, X. et al. (2021) Three AP2/ERF family members modulate flavonoid synthesis by regulating type IV chalcone isomerase in citrus. Plant Biotechnology Journal, 19, 671–688. Available from: https://doi.org/10.1111/pbi.13494
Zhao, H., He, Y., Zhang, K., Li, S., Chen, Y., He, M. et al. (2023) Rewiring of the seed metabolome during Tartary buckwheat domestication. Plant Biotechnology Journal, 21, 150–164. Available from: https://doi.org/10.1111/pbi.13932
Zhou, Y., Chen, M., Guo, J., Wang, Y., Min, D., Jiang, Q. et al. (2020) Overexpression of soybean DREB1 enhances drought stress tolerance of transgenic wheat in the field. Journal of Experimental Botany, 71, 1842–1857. Available from: https://doi.org/10.1093/jxb/erz569
Zhu, J.K. (2016) Abiotic stress signaling and responses in plants. Cell, 167, 313–324. Available from: https://doi.org/10.1016/j.cell.2016.08.029
