Combining GWAS and RNA-Seq approaches identifies the FtADH1 gene for drought resistance in Tartary buckwheat

doi:10.1016/j.jia.2024.11.009

Advanced Online Publication | Current Issue | Archive | Adv Search

Combining GWAS and RNA-Seq approaches identifies the FtADH1 gene for drought resistance in Tartary buckwheat

Jiayue He^1,^2*, Yanhua Chen^2*, Yanrong Hao², Dili Lai², Tanzim Jahan², Yaliang Shi², Hao Lin², Yuqi He², Md. Nurul Huda², Jianping Cheng¹, Kaixuan Zhang², Jinbo Li^3#, Jingjun Ruan^1#, Meiliang Zhou^2#

¹College of Agriculture, Guizhou University, Guiyang 550025, China

²Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China

³LuoYang Normal University, LuoYang 471934, China

Abstract
References

Download: PDF in ScienceDirect
Export: BibTeX | EndNote (RIS)

摘要

干旱严重制约了苦荞产业的发展，干旱灾害是影响苦荞幼苗生长、产量及品质的主要环境因素。然而，苦荞中与干旱耐受相关基因的分子机制目前仍较少被研究。乙醇脱氢酶基因（ADH）在植物中作为一个小的基因家族，在植物生长、发育及抵御逆境胁迫中发挥着重要的作用，但其在干旱胁迫中潜在的分子机制仍不清楚。本研究基于抗旱隶属函数值（MFVD）综合评价苦荞各个品种的抗旱性，通过全基因组关联研究(GWAS)并结合转录组数据分析，鉴定到苦荞抗旱基因FtADH1。研究结果表明，在拟南芥和苦荞毛状根中过表达FtADH1可以通过促进根系伸长和清除活性氧来增强其干旱耐受能力。此外，我们通过pull-down联合质谱分析发现与FtADH1相互作用的蛋白，揭示了苦荞FtADH1的与S-腺苷甲硫氨酸（SAM）合成酶蛋白FtSAMS1存在特异性相互作用。进一步的研究发现，在水分缺失胁迫处理下，过表达FtSAMS1可以显著增强苦荞毛状根中ADH酶活性和增加SAM含量。此外，FtSAMS1拟南芥和苦荞毛状根的过表达植物均表现出耐旱表型，这揭示了其FtADH1一致的生物学功能。进化变异分析表明，在荞麦属植物中，ADH1发生了基因重复和净化选择，这可能有助于提高该基因的适应性优势，如提高在栽培荞麦中的抗旱性。总之，我们的研究结果强调了的FtADH1在干旱胁迫下的重要功能，并且阐明了FtADH1和FtSAMS1在干旱条件下的相互作用机制，阐明了FtADH1与FtSAMS1之间的相互作用机制，并探讨了其在荞麦及其近缘种抗旱品种开发中的潜在应用价值。

Abstract

Drought is one of the major environmental constraints that significantly affects seedling emergence, yield, and quality of Tartary buckwheat, thereby hindering the development of its industry. However, the molecular mechanisms underlying drought tolerance genes in Tartary buckwheat remain largely unexplored. Alcohol dehydrogenase (ADH), one of the essential plant proteins, plays a crucial role in growth, development, and stress responses, but its specific role in drought resistance is still unclear. In this study, we identified an ADH gene FtADH1, using a membership function value of drought tolerance (MFVD) combined with a genome-wide association study (GWAS) and transcriptomic profiles that confers drought tolerance in Tartary buckwheat. Our findings demonstrated that the overexpression of FtADH1 in Arabidopsis and Tartary buckwheat hairy roots enhances drought tolerance by promoting root elongation and mitigating elevated levels of reactive oxygen species (ROS). Our findings demonstrated that FtADH1 can enhanced tolerance to drought stresses in both Tartary buckwheat and Arabidopsis. This study identifies the FtADH1 as a new player in affecting ROS level and the stress response of Tartary buckwheat by regulating protective enzyme activities at a high level to scavenge ROS and modulating root growth under drought stress. Further, we identified proteins interacting with FtADH1 through a prokaryotic expression pull-down assay combined with mass spectrometry, revealing that FtADH1 specifically interacts with the S-adenosyl-L-methionine (SAM) synthetase protein, FtSAMS1. Overexpression of FtSAMS1 was found to enhance ADH enzymatic activity, leading to increased SAM content in overexpressing Tartary buckwheat hairy roots under water-deficit conditions. Additionally, FtSAMS1 overexpression induced a drought-resistant phenotype in Arabidopsis and Tartary buckwheat hairy roots under drought stress, revealing the biological function of FtADH1. Evolutionary analysis indicates that ADH1 in Fagopyrum species has undergone significant evolutionary events, including duplication and purifying selection, which may contribute to functional diversification and adaptive advantages such as drought resistance in cultivated buckwheat. In summary, this study proposes that FtADH1 is a key contributor to drought tolerance, and its interaction with FtSAMS1 holds potential for the development of drought-resistant varieties in Tartary buckwheat and its relative species.

Keywords: Tartary buckwheat FtADH1 FtSAMS1 drought GWAS hairy roots

Online: 04 November 2024

Fund:

This research was supported by the National Natural Science Foundation of China (32372045), the Key Laboratory of Molecular Breeding for Grain and Oil Crops in Guizhou Provinc, China (Qiankehezhongyindi (2023) 008), the Key Laboratory of Functional Agriculture of Guizhou Provincial Higher Education Institutions, China (Qianjiaoji (2023) 007).

About author: #Correspondence Jinbo Li, E-mail: jinbo406@126.com; Jingjun Ruan, E-mail: 523131814@qq.com; Meiliang Zhou, E-mail: zhoumeiliang@caas.cn *These authors contributed equally to this work.

	Service
	E-mail this article
	Add to citation manager
	E-mail Alert
	RSS
	Articles by authors

Cite this article:

Jiayue He, Yanhua Chen, Yanrong Hao, Dili Lai, Tanzim Jahan, Yaliang Shi, Hao Lin, Yuqi He, Md. Nurul Huda, Jianping Cheng, Kaixuan Zhang, Jinbo Li, Jingjun Ruan, Meiliang Zhou . 2024. Combining GWAS and RNA-Seq approaches identifies the FtADH1 gene for drought resistance in Tartary buckwheat. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2024.11.009

Ahmed I M, Nadira U A, Qiu C W, Cao F, Chen Z-H, Vincze E, Wu F. 2020. The barley S-adenosylmethionine synthetase 3 gene HvSAMS3 positively regulates the tolerance to combined drought and salinity stress in Tibetan wild barley. Cells, 9, 1530.

Bailey-Serres J, Parker J E, Ainsworth E A, Oldroyd G E D, Schroeder J I. 2019. Genetic strategies for improving crop yields. Nature, 575, 109-118.

Betteridge D J. 2000. What is oxidative stress? Metabolism, 49, 3-8.

Bitencourt-Ferreira G, Pintro V O, de Azevedo W F, Jr. 2019. Docking with AutoDock4. Methods in Molecular Biology, 2053, 125-148.

Bocchini M, D’Amato R, Ciancaleoni S, Fontanella M C, Palmerini C A, Beone G M, Onofri A, Negri V, Marconi G, Albertini E, Businelli D. 2018. Soil selenium (Se) biofortification changes the physiological, biochemical and epigenetic responses to water stress in Zea mays L. by inducing a higher drought tolerance. Frontiers in Plant Science, 9, doi: 10.3389/fpls.2018.00389.

Boyer J S. 1982. Plant productivity and environment. Science, 218, 443-448.

Boyer J S, Silk W K, Watt M. 2010. Path of water for root growth. Functional Plant Biology, 37, doi: 10.1071/fp10108.

Cantoni G L. 1953. S-Adenosylmethionine; a new intermediate formed enzymatically from L-methionine and adenosinetriphosphate. Journal of Biological Chemistry, 204, 403-416.

Çelik A, Aktaş F. 2013. A new NADH-dependent, zinc containing alcohol dehydrogenase from Bacillus thuringiensis serovar israelensis involved in oxidations of short to medium chain primary alcohols. Journal of Molecular Catalysis B: Enzymatic, 89, 114-121.

Chen C, Wu Q, Yue J, Wang X, Wang C, Wei R, Li R, Jin G, Chen T, Chen P. 2024. A cyclic nucleotide-gated channel gene HcCNGC21 positively regulates salt and drought stress responses in kenaf (Hibiscus cannabinus L.). Plant Science, 345, doi: 10.1016/j.plantsci.2024.112111.

Chen C, Wu Y, Li J, Wang X, Zeng Z, Xu J, Liu Y, Feng J, Chen H, He Y, Xia R. 2023. TBtools-II: A "one for all, all for one" bioinformatics platform for biological big-data mining. Molecular Plant, 16, 1733-1742.

Choi H L, Seo J W, Hwang M H, Yu C Y, Seong E S. 2022. MsSAMS, a cold stress-responsive gene, provides resistance to environmental stress in T₂-generation transgenic plants. Transgenic Research, 31, 381-389.

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.

Comas L H, Becker S R, Cruz V M V, Byrne P F, Dierig D A. 2013. Root traits contributing to plant productivity under drought. Frontiers in Plant Science, 4, doi: 10.3389/fpls.2013.00442.

Cui M, Zhang W, Zhang Q, Xu Z, Zhu Z, Duan F, Wu R. 2011. Induced over-expression of the transcription factor OsDREB2A improves drought tolerance in rice. Plant Physiology and Biochemistry, 49, 1384-1391.

Dossa K, Li D, Zhou R, Yu J, Wang L, Zhang Y, You J, Liu A, Mmadi M A, Fonceka D, Diouf D, Cissé N, Wei X, Zhang X. 2019. The genetic basis of drought tolerance in the high oil crop Sesamum indicum. Plant Biotechnol J, 17, 1788-1803.

Garabagi F, Strommer J. 2004. Distinct genes produce the alcohol dehydrogenases of pollen and maternal tissues in Petunia hybrida. Biochemical Genetics, 42, 199-208.

Gautheron J, Elsayed S, Pistorio V, Lockhart S, Zammouri J, Auclair M, Koulman A, Meadows S R, Lhomme M, Ponnaiah M. 2024. ADH1B, the adipocyte-enriched alcohol dehydrogenase, plays an essential, cell-autonomous role in human adipogenesis. Proceedings of the National Academy of Sciences of the United States of America, 121, e2319301121.

Gaweł S, Wardas M, Niedworok E, Wardas P. 2004. Malondialdehyde (MDA) as a lipid peroxidation marker. Wiadomosci lekarskie (Warsaw, Poland: 1960), 57, 453-455.

Guo J, Li C, Zhang X, Li Y, Zhang D, Shi Y, Song Y, Li Y, Yang D, Wang T. 2020. Transcriptome and GWAS analyses reveal candidate gene for seminal root length of maize seedlings under drought stress. Plant Science, 292, 110380.

Guo Z, Yang W, Chang Y, Ma X, Tu H, Xiong F, Jiang N, Feng H, Huang C, Yang P, Zhao H, Chen G, Liu H, Luo L, Hu H, Liu Q, Xiong L. 2018. Genome-wide association studies of image traits reveal genetic architecture of drought resistance in rice. Molecular Plant, 11, 789-805.

Hareem M, Danish S, Obaid S A, Ansari M J, Datta R. 2024. Mitigation of drought stress in chili plants (Capsicum annuum L.) using mango fruit waste biochar, fulvic acid and cobalt. Scientific Reports, 14, 14270.

He M, He Y, Zhang K, Lu X, Zhang X, Gao B, Fan Y, Zhao H, Jha R, Huda M N. 2022. Comparison of buckwheat genomes reveals the genetic basis of metabolomic divergence and ecotype differentiation. New Phytologist, 235, 1927-1943.

He Y, Zhang K, Shi Y, Lin H, Huang X, Lu X, Wang Z, Li W, Feng X, Shi T, Chen Q, Wang J, Tang Y, Chapman M A, Germ M, Luthar Z, Kreft I, Janovská D, Meglič V, Woo S H, Quinet M, Fernie A R, Liu X, Zhou M. 2024. Genomic insight into the origin, domestication, dispersal, diversification and human selection of Tartary buckwheat. Genome Biology, 25, 61.

Hewedy O A, Elsheery N I, Karkour A M, Elhamouly N, Arafa R A, Mahmoud G A-E, Dawood M F A, Hussein W E, Mansour A, Amin D H, Allakhverdiev S I, Zivcak M, Brestic M. 2023. Jasmonic acid regulates plant development and orchestrates stress response during tough times. Environmental and Experimental Botany, 208, doi: 10.1016/j.envexpbot.2023.105260.

Huang J, Chen Q, Rong Y, Tang B, Zhu L, Ren R, Shi T, Chen Q. 2021. Transcriptome analysis revealed gene regulatory network involved in PEG-induced drought stress in Tartary buckwheat (Fagopyrum tararicum). PeerJ, 9, doi: 10.7717/peerj.11136.

Huang X, Zhao Y, Wei X, Li C, Wang A, Zhao Q, Li W, Guo Y, Deng L, Zhu C, Fan D, Lu Y, Weng Q, Liu K, Zhou T, Jing Y, Si L, Dong G, Huang T, Lu T, Feng Q, Qian Q, Li J, Han B. 2011. Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm. Nature Genetics, 44, 32-39.

Huda M N, Lu S, Jahan T, Ding M, Jha R, Zhang K, Zhang W, Georgiev M I, Park S U, Zhou M. 2021. Treasure from garden: Bioactive compounds of buckwheat. Food Chemistry, 335, 127653.

Jeong S, Lim C W, Lee S C. 2021. CaADIP1-dependent CaADIK1-kinase activation is required for abscisic acid signalling and drought stress response in Capsicum annuum. New Phytologist, 231, 2247-2261.

Käsbauer C L, Pathuri I P, Hensel G, Kumlehn J, Hückelhoven R, Proels R K. 2018. Barley ADH-1 modulates susceptibility to Bgh and is involved in chitin-induced systemic resistance. Plant Physiology and Biochemistry, 123, 281-287.

Kim S H, Kim S H, Palaniyandi S A, Yang S H, Suh J W. 2015. Expression of potato S-adenosyl-L-methionine synthase (SbSAMS) gene altered developmental characteristics and stress responses in transgenic Arabidopsis plants. Plant Physiology and Biochemistry, 87, 84-91.

Kreft I, Zhou M, Golob A, Germ M, Likar M, Dziedzic K, Luthar Z. 2020. Breeding buckwheat for nutritional quality. Breeding Science, 70, 67-73.

Kumar S, Sandell L L, Trainor P A, Koentgen F, Duester G. 2012. Alcohol and aldehyde dehydrogenases: Retinoid metabolic effects in mouse knockout models. Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, 1821, 198-205.

Lesk C, Rowhani P, Ramankutty N. 2016. Influence of extreme weather disasters on global crop production. Nature, 529, 84-87.

Li M X, Yeung J M, Cherny S S, Sham P C. 2012. Evaluating the effective numbers of independent tests and significant P-value thresholds in commercial genotyping arrays and public imputation reference datasets. Humam Genetics, 131, 747-756.

Li W, Han Y, Tao F, Chong K. 2011. Knockdown of SAMS genes encoding S-adenosyl-l-methionine synthetases causes methylation alterations of DNAs and histones and leads to late flowering in rice. Journal of Plant Physiology, 168, 1837-1843.

Li X, Tang Y, Li H, Luo W, Zhou C, Zhang L, Lv J. 2020. A wheat R2R3 MYB gene TaMpc1-D4 negatively regulates drought tolerance in transgenic Arabidopsis and wheat. Plant Science, 299, doi: 10.1016/j.plantsci.2020.110613.

Luan H, Li H, Li Y, Chen C, Li S, Wang Y, Yang J, Xu M, Shen H, Qiao H, Wang J. 2023. Transcriptome analysis of barley (Hordeum vulgare L.) under waterlogging stress, and overexpression of the HvADH4 gene confers waterlogging tolerance in transgenic Arabidopsis. BMC Plant Biology, 23, doi: 10.1186/s12870-023-04081-6.

Luo X, Wang B, Gao S, Zhang F, Terzaghi W, Dai M. 2019. Genome‐wide association study dissects the genetic bases of salt tolerance in maize seedlings. Journal of Integrative Plant Biology, 61, 658-674.

Lv A M, Su L T, Fan N N, Wen W W, Gao L, Mo X, You X K, Zhou P, An Y. 2024. The MsDHN1-MsPIP2;1-MsmMYB module orchestrates the trade-off between growth and survival of alfalfa in response to drought stress. Plant Biotechnology Journal, 22, 1132-1145.

Ma J, Du G, Li X, Zhang C, Guo J. 2015. A major locus controlling malondialdehyde content under water stress is associated with Fusarium crown rot resistance in wheat. Molecular Genetics and Genomics, 290, 1955-1962.

Meng H-L, Sun P-Y, Wang J-R, Sun X-Q, Zheng C-Z, Fan T, Chen Q-F, Li H-Y. 2022. Comparative physiological, transcriptomic, and WGCNA analyses reveal the key genes and regulatory pathways associated with drought tolerance in Tartary buckwheat. Frontiers in Plant Science, 13, doi: 10.3389/fpls.2022.985088.

Meng J, Wang L, Wang J, Zhao X, Cheng J, Yu W, Jin D, Li Q, Gong Z. 2018. METHIONINE ADENOSYLTRANSFERASE4 mediates DNA and histone methylation. Plant Physiology, 177, 652-670.

Mwadzingeni L, Shimelis H, Rees D J, Tsilo T J. 2017. Genome-wide association analysis of agronomic traits in wheat under drought-stressed and non-stressed conditions. PLoS ONE, 12, e0171692.

Nazir F, Peter P, Gupta R, Kumari S, Nawaz K, Khan M I R. 2024. Plant hormone ethylene: A leading edge in conferring drought stress tolerance. Physiologia Plantarum, 176, doi: 10.1111/ppl.14151.

Plapp B V, Lee A T-I, Khanna A, Pryor J M. 2013. Bradykinetic alcohol dehydrogenases make yeast fitter for growth in the presence of allyl alcohol. Chemico-Biological Interactions, 202, 104-110.

Pulla R K, Kim Y-J, Parvin S, Shim J-S, Lee J-H, Kim Y-J, In J-G, Senthil K S, Yang D-C. 2009. Isolation of S-adenosyl-L-methionine synthetase gene from Panax ginseng C.A. meyer and analysis of its response to abiotic stresses. Physiology and Molecular Biology of Plants, 15, 267-275.

Qi X, Li M-W, Xie M, Liu X, Ni M, Shao G, Song C, Kay-Yuen Yim A, Tao Y, Wong F-L. 2014. Identification of a novel salt tolerance gene in wild soybean by whole-genome sequencing. Nature Communications, 5, 4340.

Roje S. 2006. S-Adenosyl-l-methionine: Beyond the universal methyl group donor. Phytochemistry, 67, 1686-1698.

Senthil-Kumar M, Hema R, Suryachandra T R, Ramegowda H V, Gopalakrishna R, Rama N, Udayakumar M, Mysore K S. 2010. Functional characterization of three water deficit stress-induced genes in tobacco and Arabidopsis: An approach based on gene down regulation. Plant Physiology and Biochemistry, 48, 35-44. doi,10.1016/j.plaphy.2009.09.005.

Sequera-Mutiozabal M, Antoniou C, Tiburcio A F, Alcázar R, Fotopoulos V. 2017. Polyamines: emerging hubs promoting drought and salt stress tolerance in plants. Current Molecular Biology Reports, 3, 28-36.

Shaar-Moshe L, Hübner S, Peleg Z. 2015. Identification of conserved drought-adaptive genes using a cross-species meta-analysis approach. BMC Plant Biology, 15, doi: 10.1186/s12870-015-0493-6.

Shi H, Liu W, Yao Y, Wei Y, Chan Z. 2017. Alcohol dehydrogenase 1 (ADH1) confers both abiotic and biotic stress resistance in Arabidopsis. Plant Science, 262, 24-31.

Shohat H, Eliaz N I, Weiss D. 2021. Gibberellin in tomato: metabolism, signaling and role in drought responses. Molecular Horticulture, 1, 15.

Singh D, Laxmi A. 2015. Transcriptional regulation of drought response: a tortuous network of transcriptional factors. Frontiers in Plant Science, 6, doi: 10.3389/fpls.2015.00895.

Speirs J, Lee E, Holt K, Yong-Duk K, Steele Scott N, Loveys B, Schuch W. 1998. Genetic manipulation of alcohol dehydrogenase levels in ripening tomato fruit affects the balance of some flavor aldehydes and alcohols. Plant Physiology, 117, 1047-1058.

Strommer J. 2011. The plant ADH gene family. The Plant Journal, 66, 128-142.

Su W, Ren Y, Wang D, Su Y, Feng J, Zhang C, Tang H, Xu L, Muhammad K, Que Y. 2020. The alcohol dehydrogenase gene family in sugarcane and its involvement in cold stress regulation. BMC Genomics, 21, 521.

Tardieu F, Simonneau T, Muller B. 2018. The physiological basis of drought tolerance in crop plants: A scenario-dependent probabilistic approach. Annual Review of Plant Biology, 69, 733-759.

Thompson C E, Salzano F M, de Souza O N, Freitas L B. 2007. Sequence and structural aspects of the functional diversification of plant alcohol dehydrogenases. Gene, 396, 108-115.

Tougou M, Hashiguchi A, Yukawa K, Nanjo Y, Hiraga S, Nakamura T, Nishizawa K, Komatsu S. 2012. Responses to flooding stress in soybean seedlings with the alcohol dehydrogenase transgene. Plant Biotechnology, 29, 301-305.

Van Der Straeten D, Rodrigues Pousada R A, Gielen J, Van Montagu M. 2002. Tomato alcohol dehydrogenase. FEBS Letters, 295, 39-42.

Wang X, Li Q, Xie J, Huang M, Cai J, Zhou Q, Dai T, Jiang D. 2021. Abscisic acid and jasmonic acid are involved in drought priming-induced tolerance to drought in wheat. The Crop Journal, 9, 120-132.

Wang X, Wang H, Liu S, Ferjani A, Li J, Yan J, Yang X, Qin F. 2016. Genetic variation in ZmVPP1 contributes to drought tolerance in maize seedlings. Nature Genetics, 48, 1233-1241.

Wang Z, Wang F, Hong Y, Yao J, Ren Z, Shi H, Zhu J-K. 2018. The flowering repressor SVP confers drought resistance in Arabidopsis by regulating abscisic acid catabolism. Molecular Plant, 11, 1184-1197.

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.

Xiang D B, Wei W, Wan Y, Wu X Y, Ye X L, Peng L X, Zhong L Y, Wu Q, Zou L, Zhao G, Zhao J L. 2021. Polysaccharide elicitor from the endophyte Bionectria sp. Fat6 improves growth of Tartary buckwheat under drought stress. Phyton-International Journal of Experimental Botany, 90, 461-473.

Xiao J, Cheng H, Li X, Xiao J, Xu C, Wang S. 2013. Rice WRKY13 regulates cross talk between abiotic and biotic stress signaling pathways by selective binding to different cis-elements. Plant Physiology, 163, 1868-1882.

Yan H, Liu C, Zhao J, Ye X, Wu Q, Yao T, Peng L, Zou L, Zhao G. 2021. Genome-wide analysis of the NF-Y gene family and their roles in relation to fruit development in Tartary buckwheat (Fagopyrum tataricum). International Journal of Biological Macromolecules, 190, 487-498.

Yang H, Fang Y, Liang Z, Qin T, Liu J H, Liu T. 2024. Polyamines: pleiotropic molecules regulating plant development and enhancing crop yield and quality. Plant Biotechnology Journal, 22, 3194-3201.

Yi S Y, Ku S S, Sim H-J, Kim S-K, Park J H, Lyu J I, So E J, Choi S Y, Kim J, Ahn M S, Kim S W, Park H, Jeong W J, Lim Y P, Min S R, Liu J R. 2017. An alcohol dehydrogenase gene from Synechocystis sp. Confers salt tolerance in transgenic tobacco. Frontiers in Plant Science, 8, doi: 10.3389/fpls.2017.01965.

Yu L H, Wu S J, Peng Y S, Liu R N, Chen X, Zhao P, Xu P, Zhu J B, Jiao G L, Pei Y, Xiang C B. 2015. Arabidopsis EDT1/HDG11 improves drought and salt tolerance in cotton and poplar and increases cotton yield in the field. Plant Biotechnology Journal, 14, 72-84.

Zhang F, Rosental L, Ji B, Brotman Y, Dai M. 2024. Metabolite‐mediated adaptation of crops to drought and the acquisition of tolerance. The Plant Journal, 118, 626-644.

Zhang H, Zhang J, Xu Q, Wang D, Di H, Huang J, Yang X, Wang Z, Zhang L, Dong L. 2020a. Identification of candidate tolerance genes to low-temperature during maize germination by GWAS and RNA-seq approaches. BMC Plant Biology, 20, 1-17.

Zhang J, Huang D, Zhao X, Zhang M. 2021a. Evaluation of drought resistance and transcriptome analysis for the identification of drought-responsive genes in Iris germanica. Scientific Reports, 11, doi,10.1038/s41598-021-95633-z.

Zhang K, He M, Fan Y, Zhao H, Gao B, Yang K, Li F, Tang Y, Gao Q, Lin T. 2021b. Resequencing of global Tartary buckwheat accessions reveals multiple domestication events and key loci associated with agronomic traits. Genome Biology, 22, 1-17.

Zhang K, He Y, Lu X, Shi Y, Zhao H, Li X, Li J, Liu Y, Ouyang Y, Tang Y. 2023. Comparative and population genomics of buckwheat species reveal key determinants of flavor and fertility. Molecular Plant, 16, 1427-1444.

Zhang K, Logacheva M D, Meng Y, Hu J, Wan D, Li L, Janovská D, Wang Z, Georgiev M I, Yu Z. 2018. Jasmonate-responsive MYB factors spatially repress rutin biosynthesis in Fagopyrum tataricum. Journal of Experimental Botany, 69, 1955-1966.

Zhang X, Bao Z, Gong B, Shi Q. 2020b. S-adenosylmethionine synthetase 1 confers drought and salt tolerance in transgenic tomato. Environmental and Experimental Botany, 179, doi: 10.1016/j.envexpbot.2020.104226.

Zhang Z L, Zhou M L, Tang Y, Li F L, Tang Y X, Shao J R, Xue W T, Wu Y M. 2012. Bioactive compounds in functional buckwheat food. Food Research International, 49, 389-395.

Zhao W, Huang H, Wang J, Wang X, Xu B, Yao X, Sun L, Yang R, Wang J, Sun A. 2023. Jasmonic acid enhances osmotic stress responses by MYC2‐mediated inhibition of protein phosphatase 2C1 and response regulators 26 transcription factor in tomato. The Plant Journal, 113, 546-561.

Zhou M, Sun Z, Ding M, Logacheva M D, Kreft I, Wang D, Yan M, Shao J, Tang Y, Wu Y. 2017. FtSAD2 and FtJAZ1 regulate activity of the FtMYB11 transcription repressor of the phenylpropanoid pathway in Fagopyrum tataricum. New Phytologist, 216, 814-828.

Zhu F. 2016a. Chemical composition and health effects of Tartary buckwheat. Food Chemistry, 203, 231-245.

Zhu J K. 2016b. Abiotic stress signaling and responses in plants. Cell, 167, 313-324.

No related articles found!

No Suggested Reading articles found!

Viewed

Full text

Abstract

Cited

Shared

Discussed

Cite this article:

About JIA

Editorial board

For authors