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Two galactinol synthases contribute to the drought response of Camellia sinensis

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Abstract

Main conclusion

CsGolS2-1 and CsGolS2-2 are involved in the transcriptional mechanism and play an important role in the drought response of tea plants.

Abstract

GolS is critical for the biosynthesis of galactinol and has been suggested to contribute to drought tolerance in various plants. However, whether GolS plays a role in drought response and the underlying transcriptional mechanism of GolS genes in response to drought stress in tea plants is still unclear. In this study, we found that drought stress promotes the accumulation of galactinol in tea leaves and that the expression of CsGolS2-1 and CsGolS2-2, which encode proteins capable of catalyzing galactinol biosynthesis, is continuously and dramatically induced by drought stress. Moreover, transgenic Arabidopsis plants expressing CsGolS2-1 and CsGolS2-2 were more drought-tolerant than WT plants, as evidenced by increased cell membrane stability. In addition, the drought-responsive transcription factor CsWRKY2 has been shown to positively regulate the expression of CsGolS2-1 and CsGolS2-2 by directly binding to their promoters. Furthermore, CsVQ9 was found to interact with CsWRKY2 and promote its transcriptional function to activate CsGolS2-1 and CsGolS2-2 expression. Taken together, our findings provide insights not only into the positive role played by CsGolS2-1 and CsGolS2-2 in the drought response of tea plants but also into the transcriptional mechanisms involved.

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Data availability

All of the data are represented in the manuscript and Supplementary Materials.

Abbreviations

ROS:

Reactive oxygen species

GolS:

Galactinol synthases

UDP-Gal:

UDP-galactose

TFs:

Transcription factors

MDA:

Malondialdehyde

WGCNA:

Weighted gene co-expression network analysis

References

  • Chen J, Wang H, Li Y, Pan J, Hu Y, Yu D (2018) Arabidopsis VQ10 interacts with WRKY8 to modulate basal defense against Botrytis cinerea. J Integr Plant Biol 60(10):956–969

    Article  CAS  PubMed  Google Scholar 

  • Chen Q, Hu T, Li X, Song CP, Zhu JK, Chen L, Zhao Y (2022a) Phosphorylation of SWEET sucrose transporters regulates plant root: shoot ratio under drought. Nat Plants 8(1):68–77

    Article  CAS  PubMed  Google Scholar 

  • Chen S, Cao H, Huang B, Zheng X, Liang K, Wang GL, Sun X (2022b) The WRKY10-VQ8 module safely and effectively regulates rice thermotolerance. Plant Cell Environ 45(7):2126–2144

    Article  CAS  PubMed  Google Scholar 

  • Chi Y, Yang Y, Zhou Y, Zhou J, Fan B, Yu JQ, Chen Z (2013) Protein-protein interactions in the regulation of WRKY transcription factors. Mol Plant 6(2):287–300

    Article  CAS  PubMed  Google Scholar 

  • Cui LH, Byun MY, Oh HG, Kim SJ, Lee J, Park H, Lee H, Kim WT (2020) Poaceae type II galactinol synthase 2 from antarctic flowering plant Deschampsia antarctica and rice improves cold and drought tolerance by accumulation of raffinose family oligosaccharides in transgenic rice plants. Plant Cell Physiol 61(1):88–104

    Article  CAS  PubMed  Google Scholar 

  • Dong Q, Zhao S, Duan D, Tian Y, Wang Y, Mao K, Zhou Z, Ma F (2018) Structural and functional analyses of genes encoding VQ proteins in apple. Plant Sci 272:208–219

    Article  CAS  PubMed  Google Scholar 

  • dos Santos TB, Vieira LGE (2020) Involvement of the galactinol synthase gene in abiotic and biotic stress responses: a review on current knowledge. Plant Gene 24:100258

    Article  Google Scholar 

  • Draper HH, Squires EJ, Mahmoodi H, Wu J, Agarwal S, Hadley M (1993) A comparative evaluation of thiobarbituric acid methods for the determination of malondialdehyde in biological materials. Free Radic Biol Med 15(4):353–363

    Article  CAS  PubMed  Google Scholar 

  • ElSayed AI, Rafudeen MS, Golldack D (2014) Physiological aspects of raffinose family oligosaccharides in plants: protection against abiotic stress. Plant Biol 16(1):1–8

    Article  CAS  PubMed  Google Scholar 

  • Filiz E, Ozyigit II, Vatansever R (2015) Genome-wide identification of galactinol synthase (GolS) genes in Solanum lycopersicum and Brachypodium distachyon. Comput Biol Chem 58:149–157

    Article  CAS  PubMed  Google Scholar 

  • Gu L, Zhang Y, Zhang M, Li T, Dirk LM, Downie B, Zhao T (2016) ZmGOLS2, a target of transcription factor ZmDREB2A, offers similar protection against abiotic stress as ZmDREB2A. Plant Mol Biol 90(1–2):157–170

    Article  CAS  PubMed  Google Scholar 

  • Gu L, Jiang T, Zhang C, Li X, Wang C, Zhang Y, Li T, Dirk LMA, Downie AB, Zhao T (2019) Maize HSFA2 and HSBP2 antagonistically modulate raffinose biosynthesis and heat tolerance in Arabidopsis. Plant J 100(1):128–142

    Article  CAS  PubMed  Google Scholar 

  • Lai Z, Li Y, Wang F, Cheng Y, Fan B, Yu JQ, Chen Z (2011) Arabidopsis sigma factor binding proteins are activators of the WRKY33 transcription factor in plant defense. Plant Cell 23(10):3824–3841

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Langfelder P, Horvath S (2008) WGCNA: an R package for weighted correlation network analysis. BMC Bioinform 9:559

    Article  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25(16):2078–2079

    Article  PubMed  PubMed Central  Google Scholar 

  • Li T, Zhang Y, Liu Y, Li X, Hao G, Han Q, Dirk LMA, Downie AB, Ruan YL, Wang J, Wang G, Zhao T (2020) Raffinose synthase enhances drought tolerance through raffinose synthesis or galactinol hydrolysis in maize and Arabidopsis plants. J Biol Chem 295(23):8064–8077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liao Y, Smyth GK, Shi W (2014) featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30(7):923–930

    Article  CAS  PubMed  Google Scholar 

  • Liu SC, Jin JQ, Ma JQ, Yao MZ, Ma CL, Li CF, Ding ZT, Chen L (2016) Transcriptomic analysis of tea plant responding to drought stress and recovery. PLoS ONE 11(1):e0147306

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu L, Wu X, Sun W, Yu X, Demura T, Li D, Zhuge Q (2021) Galactinol synthase confers salt-stress tolerance by regulating the synthesis of galactinol and raffinose family oligosaccharides in poplar. Ind Crops Prod 165:113432

    Article  CAS  Google Scholar 

  • Ma S, Sun L, Sui X, Li Y, Chang Y, Fan J, Zhang Z (2019) Phloem loading in cucumber: combined symplastic and apoplastic strategies. Plant J 98(3):391–404

    Article  CAS  PubMed  Google Scholar 

  • Ma S, Lv J, Li X, Ji T, Zhang Z, Gao L (2021) Galactinol synthase gene 4 (CsGolS4) increases cold and drought tolerance in Cucumis sativus L. by inducing RFO accumulation and ROS scavenging. Environ Exp Bot 185:104406

    Article  CAS  Google Scholar 

  • Mukherjee S, Sengupta S, Mukherjee A, Basak P, Majumder AL (2019) Abiotic stress regulates expression of galactinol synthase genes post-transcriptionally through intron retention in rice. Planta 249:891–912

    Article  CAS  PubMed  Google Scholar 

  • Ng’etich WK, Stephens W (2001) Responses of tea to environment in Kenya. 1. genotype × environment interactions for total dry matter production and yield. Exp Agric 37(3):333–342

    Article  Google Scholar 

  • Nishizawa A, Yabuta Y, Shigeoka S (2008) Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol 147(3):1251–1263

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Panda RK, Stephens W, Matthews R (2003) Modelling the influence of irrigation on the potential yield of tea (Camellia sinensis) in North-East India. Exp Agric 39(2):181–198

    Article  Google Scholar 

  • Qiu S, Zhang J, He J, Sha W, Li M, Zhao Y, Zhai Y (2020) Overexpression of GmGolS2-1, a soybean galactinol synthase gene, enhances transgenic tobacco drought tolerance. Plant Cell Tiss Organ Cult 143:507–516

    Article  CAS  Google Scholar 

  • Safaei Chaeikar S, Marzvan S, Jahangirzadeh Khiavi S, Rahimi M (2020) Changes in growth, biochemical, and chemical characteristics and alteration of the antioxidant defense system in the leaves of tea clones (Camellia sinensis L.) under drought stress. Sci Hortic 265:109257

    Article  CAS  Google Scholar 

  • Salvi P, Kamble NU, Majee M (2018) Stress-inducible galactinol synthase of chickpea (CaGolS) is implicated in heat and oxidative stress tolerance through reducing stress-induced excessive reactive oxygen species accumulation. Plant Cell Physiol 59(1):155–166

    Article  CAS  PubMed  Google Scholar 

  • Salvi P, Kamble NU, Majee M (2020) Ectopic over-expression of ABA-responsive Chickpea galactinol synthase (CaGolS) gene results in improved tolerance to dehydration stress by modulating ROS scavenging. Environ Exp Bot 171:103957

    Article  CAS  Google Scholar 

  • Selvaraj MG, Ishizaki T, Valencia M, Ogawa S, Dedicova B, Ogata T, Yoshiwara K, Maruyama K, Kusano M, Saito K, Takahashi F, Shinozaki K, Nakashima K, Ishitani M (2017) Overexpression of an Arabidopsis thaliana galactinol synthase gene improves drought tolerance in transgenic rice and increased grain yield in the field. Plant Biotechnol J 15(11):1465–1477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13(11):2498–2504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shao C, Chen J, Lv Z, Gao X, Guo S, Xu R, Deng Z, Yao S, Chen Z, Kang Y, Huang J, Liu Z, Shen C (2023) Staged and repeated drought-induced regulation of phenylpropanoid synthesis confers tolerance to a water deficit environment in Camellia sinensis. Ind Crops Prod 201:11683

    Article  Google Scholar 

  • Shen J, Wang S, Sun L, Wang Y, Fan K, Li C, Wang H, Bi C, Zhang F, Ding Z (2022) Dynamic changes in metabolic and lipidomic profiles of tea plants during drought stress and re-watering. Front Plant Sci 13:978531

    Article  PubMed  PubMed Central  Google Scholar 

  • Shi J, Fu XZ, Peng T, Huang XS, Fan QJ, Liu JH (2010) Spermine pretreatment confers dehydration tolerance of citrus in vitro plants via modulation of antioxidative capacity and stomatal response. Tree Physiol 30(7):914–922

    Article  CAS  PubMed  Google Scholar 

  • Song C, Chung WS, Lim CO (2016) Overexpression of heat shock factor gene HsfA3 increases galactinol levels and oxidative stress tolerance in Arabidopsis. Mol Cells 39(6):477–483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun Z, Qi X, Wang Z, Li P, Wu C, Zhang H, Zhao Y (2013) Overexpression of TsGOLS2, a galactinol synthase, in Arabidopsis thaliana enhances tolerance to high salinity and osmotic stresses. Plant Physiol Biochem 69:82–89

    Article  CAS  PubMed  Google Scholar 

  • Taji T, Ohsumi C, Iuchi S, Seki M, Kasuga M, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2002) Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J 29(4):417–426

    Article  CAS  PubMed  Google Scholar 

  • Taniguchi F, Kimura K, Saba T, Ogino A, Yamaguchi S, Tanaka J (2014) Worldwide core collections of tea (Camellia sinensis) based on SSR markers. Tree Genet Genom 10:1555–1565

    Article  Google Scholar 

  • Valluru R, Van den Ende W (2011) Myo-inositol and beyond–emerging networks under stress. Plant Sci 181(4):387–400

    Article  CAS  PubMed  Google Scholar 

  • Van den Ende W, Valluru R (2009) Sucrose, sucrosyl oligosaccharides, and oxidative stress: scavenging and salvaging? J Exp Bot 60(1):9–18

    Article  PubMed  Google Scholar 

  • Wang Z, Zhu Y, Wang L, Liu X, Liu Y, Phillips J, Deng X (2009) A WRKY transcription factor participates in dehydration tolerance in Boea hygrometrica by binding to the W-box elements of the galactinol synthase (BhGolS1) promoter. Planta 230(6):1155–1166

    Article  CAS  PubMed  Google Scholar 

  • Wang A, Garcia D, Zhang H, Feng K, Chaudhury A, Berger F, Peacock WJ, Dennis ES, Luo M (2010) The VQ motif protein IKU1 regulates endosperm growth and seed size in Arabidopsis. Plant J 63(4):670–679

    Article  CAS  PubMed  Google Scholar 

  • Wei C, Yang H, Wang S, Zhao J, Liu C, Gao L, Xia E, Lu Y, Tai Y, She G, Sun J, Cao H, Tong W, Gao Q, Li Y, Deng W, Jiang X, Wang W, Chen Q, Zhang S, Li H, Wu J, Wang P, Li P, Shi C, Zheng F, Jian J, Huang B, Shan D, Shi M, Fang C, Yue Y, Li F, Li D, Wei S, Han B, Jiang C, Yin Y, Xia T, Zhang Z, Bennetzen JL, Zhao S, Wan X (2018) Draft genome sequence of Camellia sinensis var. sinensis provides insights into the evolution of the tea genome and tea quality. Proc Natl Acad Sci USA 115(18):E4151–E4158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xia EH, Li FD, Tong W, Li PH, Wu Q, Zhao HJ, Ge RH, Li RP, Li YY, Zhang ZZ, Wei CL, Wan XC (2019) Tea Plant Information Archive: a comprehensive genomics and bioinformatics platform for tea plant. Plant Biotechnol J 17(10):1938–1953

    Article  PubMed  PubMed Central  Google Scholar 

  • You J, Wang Y, Zhang Y, Dossa K, Li D, Zhou R, Wang L, Zhang X (2018) Genome-wide identification and expression analyses of genes involved in raffinose accumulation in sesame. Sci Rep 8(1):4331

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Henriques R, Lin SS, Niu QW, Chua NH (2006) Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nat Protoc 1(2):641–646

    Article  CAS  PubMed  Google Scholar 

  • Zhang Q, Cai M, Yu X, Wang L, Guo C, Ming R, Zhang J (2017) Transcriptome dynamics of Camellia sinensis in response to continuous salinity and drought stress. Tree Genet Genom 13(4):78

    Article  Google Scholar 

  • Zhang H, Sun Z, Feng S, Zhang J, Zhang F, Wang W, Hu H, Zhang W, Bao M (2022a) The C2H2-type zinc finger protein PhZFP1 regulates cold stress tolerance by modulating galactinol synthesis in Petunia hybrida. J Exp Bot 73(18):6434–6448

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Xiao Y, Zhang Y, Dong Y, Liu Y, Liu L, Wan S, He J, Yu Y (2022b) Accumulation of galactinol and ABA is involved in exogenous EBR-induced drought tolerance in tea plants. J Agric Food Chem 70(41):13391–13403

    Article  CAS  PubMed  Google Scholar 

  • Zhao TY, Meeley RB, Downie B (2003) Aberrant processing of a maize GALACTINOL SYNTHASE transcript is caused by heat stress. Plant Sci 165(1):245–256

    Article  CAS  Google Scholar 

  • Zhou Y, Liu Y, Wang S, Shi C, Zhang R, Rao J, Wang X, Gu X, Wang Y, Li D, Wei C (2017) Molecular cloning and characterization of galactinol synthases in Camellia sinensis with different responses to biotic and abiotic stressors. J Agric Food Chem 65(13):2751–2759

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by the earmarked fund for Modern Agro-industry Technology Research System (CARS-19), the Agricultural Special Fund Project of Shaanxi Province (NYKJ-2022-YL(XN)37), the special fund for University-Supported Extension Model (TGZX2022-2), The science and technology Innovation Project of Shaanxi Academy of Forestry Sciences (SXLK2021-02-06).

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  1. Yezi Xiao and Yuan Dong contributed equally to this work.

Authors and Affiliations

  1. College of Horticulture, Northwest A&F University, Yangling, 712100, Shaanxi, China

    Yezi Xiao, Yuan Dong, Yongheng Zhang, Yingao Zhang, Lu Liu, Peiying Liu, Siqing Wan, Qingshan Xu & Youben Yu

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  1. Yezi Xiao
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Xiao, Y., Dong, Y., Zhang, Y. et al. Two galactinol synthases contribute to the drought response of Camellia sinensis. Planta 258, 84 (2023). https://doi.org/10.1007/s00425-023-04238-5

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