CsPHRs-CsJAZ3 incorporates phosphate signaling and jasmonate pathway to regulate catechin biosynthesis in Camellia sinensis

Linying Li , Xueying Zhang , Da Li , Hui Su , Yuqing He , Zelong Xu , Yao Zhao , Yiyi Hong , Qingsheng Li , Ping Xu , Gaojie Hong

Horticulture Research ›› 2024, Vol. 11 ›› Issue (8) : 178

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Horticulture Research ›› 2024, Vol. 11 ›› Issue (8) :178 DOI: 10.1093/hr/uhae178
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CsPHRs-CsJAZ3 incorporates phosphate signaling and jasmonate pathway to regulate catechin biosynthesis in Camellia sinensis
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Abstract

Catechins constitute abundant metabolites in tea and have potential health benefits and high economic value. Intensive study has shown that the biosynthesis of tea catechins is regulated by environmental factors and hormonal signals. However, little is known about the coordination of phosphate (Pi) signaling and the jasmonic acid (JA) pathway on biosynthesis of tea catechins. We found that Pi deficiency caused changes in the content of catechins and modulated the expression levels of genes involved in catechin biosynthesis. Herein, we identified two transcription factors of phosphate signaling in tea, named CsPHR1 and CsPHR2, respectively. Both regulated catechin biosynthesis by activating the transcription of CsANR1 and CsMYB5c. We further demonstrated CsSPX1, a Pi pathway repressor, suppressing the activation by CsPHR1/2 of CsANR1 and CsMYB5c. JA, one of the endogenous plant hormones, has been reported to be involved in the regulation of secondary metabolism. Our work demonstrated that the JA signaling repressor CsJAZ3 negatively regulated catechin biosynthesis via physical interaction with CsPHR1 and CsPHR2. Thus, the CsPHRs-CsJAZ3 module bridges the nutrition and hormone signals, contributing to targeted cultivation of high-quality tea cultivars with high fertilizer efficiency.

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Linying Li, Xueying Zhang, Da Li, Hui Su, Yuqing He, Zelong Xu, Yao Zhao, Yiyi Hong, Qingsheng Li, Ping Xu, Gaojie Hong. CsPHRs-CsJAZ3 incorporates phosphate signaling and jasmonate pathway to regulate catechin biosynthesis in Camellia sinensis. Horticulture Research, 2024, 11 (8) : 178 DOI:10.1093/hr/uhae178

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Acknowledgements

This research was supported by the Zhejiang Provincial Natural Science Foundation of China under Grant No. LQ23C020003 and LR22C020003, the National Natural Science Foundation of China under Grant No. 32272553, the Major Science and Technology Special Project of Variety Breeding of Zhejiang Province (2021C02067-7 and 2021C02064-6), and the State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products (2021DG700024-KF202102).

Author contributions

GJ.H. and LY.L. designed the project, analyzed the data, interpreted the results, and wrote the manuscript. LY.L., XY.Z., D.L., H.S., YQ.H., ZL.X., Y.Z., YY.H., QS.L., and P.X. performed the experiments. The article's submission was reviewed and approved by all authors.

Data availability

All the data supporting the findings of this study are available in the paper and supplementary data.

Conflict of interest

The authors declare no conflict of interest.

Supplementary data

Supplementary data are available at Horticulture Research online.

References

[1]

Fraga CG, Croft KD, Kennedy DO. et al. The effects of polyphenols and other bioactives on human health. Food Funct. 2019; 10: 514-28

[2]

Goya L, Roman RS, de Pascual-Teresa S. Polyphenols’ effect on cerebrovascular health. Curr Med Chem. 2022; 29: 1029-44

[3]

Veeraraghavan VP, Mony U, Renu K. et al. Effects of polyphenols on ncRNAs in cancer - an update. Clin Exp Pharmacol Physiol. 2022; 49:613-23

[4]

Roh E, Kim JE, Kwon JY. et al. Molecular mechanisms of green tea polyphenols with protective effects against skin photoaging. Crit Rev Food Sci Nutr. 2017; 57:1631-7

[5]

Zhang X, Liu Y, Gao K. et al. Characterisation of anthocyanidin reductase from Shuchazao green tea. J Sci Food Agric. 2012; 92: 1533-9

[6]

Fu JY, Liu Q, Wang C. et al. ZmWRKY79 positively regulates maize phytoalexin biosynthetic gene expression and is involved in stress response. J Exp Bot. 2018; 69:497-510

[7]

Eungwanichayapant PD, Popluechai S. Accumulation of catechins in tea in relation to accumulation of mRNA from genes involved in catechin biosynthesis. Plant Physiol Biochem. 2009; 47: 94-7

[8]

Kuhn BM, Geisler M, Bigler L. et al. Flavonols accumulate asymmetrically and affect auxin transport in Arabidopsis. Plant Physiol. 2011; 156:585-95

[9]

Jiang X, Huang K, Zheng G. et al. CsMYB5a and CsMYB5e from Camellia sinensis differentially regulate anthocyanin and proanthocyanidin biosynthesis. Plant Sci. 2018; 270:209-20

[10]

Zheng G, Fan C, Di S. et al. Ectopic expression of tea MYB genes alter spatial flavonoid accumulation in alfalfa (Medicago sativa). PLoS One. 2019; 14:e0218336

[11]

Wang P, Ma G, Zhang L. et al. A sucrose-induced MYB (SIMYB) transcription factor promoting proanthocyanidin accumulation in the tea plant (Camellia sinensis). J Agric Food Chem. 2019; 67: 1418-28

[12]

Liu Y, Hou H, Jiang X. et al. A WD 40 repeat protein from Camellia sinensis regulates anthocyanin and proanthocyanidin accumulation through the formation of MYB(-)bHLH(-)WD40 ternary complexes. Int J Mol Sci. 2018; 19:1686

[13]

Liu ZJ, Wu X, Wang E. et al. PHR1 positively regulates phosphate starvation-induced anthocyanin accumulation through direct upregulation of genes F3’H and LDOX in Arabidopsis. Planta. 2022; 256:42

[14]

Lin ZH, Chen LS, Chen RB. et al. Root release and metabolism of organic acids in tea plants in response to phosphorus supply. J Plant Physiol. 2011; 168:644-52

[15]

Kc S, Liu M, Zhang Q. et al. Metabolic changes of amino acids and flavonoids in tea plants in response to inorganic phosphate limitation. Int J Mol Sci. 2018; 19:3683

[16]

Lin ZH, Qi YP, Chen RB. et al. Effects of phosphorus supply on the quality of green tea. Food Chem. 2012; 130:908-14

[17]

Su H, Zhang X, He Y. et al. Transcriptomic analysis reveals the molecular adaptation of three major secondary metabolic pathways to multiple macronutrient starvation in tea (Camellia sinensis). Genes. 2020; 11:241

[18]

Guan Z, Zhang Q, Zhang Z. et al. Mechanistic insights into the regulation of plant phosphate homeostasis by the rice SPX2-PHR2 complex. Nat Commun. 2022; 13:1581

[19]

Wang Z, Ruan W, Shi J. et al. Rice SPX1 and SPX2 inhibit phosphate starvation responses through interacting with PHR2 in a phosphate-dependent manner. Proc Natl Acad Sci USA. 2014; 111: 14953-8

[20]

Liu F, Wang Z, Ren H. et al. OsSPX1 suppresses the function of OsPHR2 in the regulation of expression of OsPT2 and phosphate homeostasis in shoots of rice. Plant J. 2010; 62:508-17

[21]

Zhou J, Jiao F, Wu Z. et al. OsPHR2 is involved in phosphate-starvation signaling and excessive phosphate accumulation in shoots of plants. Plant Physiol. 2008; 146:1673-86

[22]

Wang P, Snijders R, Kohlen W. et al. Medicago SPX1 and SPX3 regulate phosphate homeostasis, mycorrhizal colonization, and arbuscule degradation. Plant Cell. 2021; 33:3470-86

[23]

Puga MI, Mateos I, Charukesi R. et al. SPX1 is a phosphate-dependent inhibitor of phosphate starvation response 1 in Arabidopsis. Proc Natl Acad Sci USA. 2014; 111:14947-52

[24]

Rubio V, Linhares F, Solano R. et al. A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev. 2001; 15: 2122-33

[25]

Bustos R, Castrillo G, Linhares F. et al. A central regulatory system largely controls transcriptional activation and repression responses to phosphate starvation in Arabidopsis. PLoS Genet. 2010; 6:e1001102

[26]

Bao H, Chen H, Chen M. et al. Transcriptome-wide identification and characterization of microRNAs responsive to phosphate starvation in Populus tomentosa. Funct Integr Genomics. 2019; 19: 953-72

[27]

Chen NN, Tong S, Yang J. et al. PtoWRKY 40 interacts with PtoPHR1-LIKE3 while regulating the phosphate starvation response in poplar. Plant Physiol. 2022; 190:2688-705

[28]

Li LY, He Y, Zhang X. et al. Alterations of rice (Oryza sativa L.) DNA methylation patterns associated with gene expression in response to rice black streaked dwarf virus. Int J Mol Sci. 2020; 21:5753

[29]

Ghorbel M, Brini F, Sharma A. et al. Role of jasmonic acid in plants: the molecular point of view. Plant Cell Rep. 2021; 40: 1471-94

[30]

Pandey BK, Verma L, Prusty A. et al. OsJAZ11 regulates phosphate starvation responses in rice. Planta. 2021; 254:8

[31]

Khan GA, Vogiatzaki E, Glauser G. et al. Phosphate deficiency induces the jasmonate pathway and enhances resistance to insect herbivory. Plant Physiol. 2016; 171:632-44

[32]

Shan X, Zhang Y, Peng W. et al. Molecular mechanism for jasmonate-induction of anthocyanin accumulation in Arabidopsis. J Exp Bot. 2009; 60:3849-60

[33]

Cai XT, Xu P, Zhao PX. et al. Arabidopsis ERF 109 mediates cross-talk between jasmonic acid and auxin biosynthesis during lateral root formation. Nat Commun. 2014; 5:5833

[34]

Wasternack C, Hause B. Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann Bot. 111:1021-58

[35]

Kazan K, Manners JM. JAZ repressors and the orchestration of phytohormone crosstalk. Trends Plant Sci. 2012; 17:22-31

[36]

Hou X, Lee LY, Xia K. et al. DELLAs modulate jasmonate signaling via competitive binding to JAZs. Dev Cell. 2010; 19:884-94

[37]

Kong YZ, Wang G, Chen X. et al. OsPHR2 modulates phosphate starvation-induced OsMYC2 signalling and resistance to Xanthomonas oryzae pv. oryzae. Plant Cell Environ. 2021; 44: 3432-44

[38]

Wang J, Sun J, Miao J. et al. A phosphate starvation response regulator Ta-PHR1 is involved in phosphate signalling and increases grain yield in wheat. Ann Bot. 2013; 111:1139-53

[39]

Wang HH, Hu J, Li L. et al. Involvement of PtPHR1 in phosphates starvation-induced alkaloid biosynthesis in Pinellia ternata (Thunb.) Breit. Front Plant Sci. 2022; 13:914648

[40]

Ren F, Guo QQ, Chang LL. et al. Brassica napus PHR1 gene encoding a MYB-like protein functions in response to phosphate starvation. PLoS One. 2012; 7:e44005

[41]

Lu S, Ye J, Zhu K. et al. A citrus phosphate starvation response factor CsPHL3 negatively regulates carotenoid metabolism. Plant Cell Physiol. 2021; 62:482-93

[42]

Zhang XY, He Y, He W. et al. Structural and functional insights into the LBD family involved in abiotic stress and flavonoid synthases in Camellia sinensis. Sci Rep. 2019; 9:15651

[43]

Shi JC, Zhao B, Zheng S. et al. A phosphate starvation response-centered network regulates mycorrhizal symbiosis. Cell. 2021; 184:5527-5540.e18

[44]

Wang X, Li Z, Policarpio L. et al. De novo biosynthesis of complex natural product sakuranetin using modular co-culture engineering. Appl Microbiol Biotechnol. 2020; 104:4849-61

[45]

Ju L, Jing Y, Shi P. et al. JAZ proteins modulate seed germination through interaction with ABI5 in bread wheat and Arabidopsis. New Phytol. 2019; 223:246-60

[46]

Shi J, Ma C, Qi D. et al. Transcriptional responses and flavor volatiles biosynthesis in methyl jasmonate-treated tea leaves. BMC Plant Biol. 2015; 15:233

[47]

Thines B, Katsir L, Melotto M. et al. JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature. 2007; 448:661-5

[48]

Luo XY, Li Z, Xiao S. et al. Phosphate deficiency enhances cotton resistance to Verticillium dahliae through activating jasmonic acid biosynthesis and phenylpropanoid pathway. Plant Sci. 2021; 302:110724

[49]

He YQ, Zhang X, Li L. et al. SPX4 interacts with both PHR1 and PAP1 to regulate critical steps in phosphorus-status-dependent anthocyanin biosynthesis. New Phytol. 2021; 230: 205-17

[50]

Tan HJ, Man C, Xie Y. et al. A crucial role of GA-regulated flavonol biosynthesis in root growth of Arabidopsis. Mol Plant. 2019; 12: 521-37

[51]

Zhang H, Li C, Wei K. et al. The reduction of tea quality caused by irrational phosphate application is associated with anthocyanin metabolism. Beverage Plant Res. 2023; 3:10

[52]

Ding Z, Jia S, Wang Y. et al. Phosphate stresses affect ionome and metabolome in tea plants. Plant Physiol Biochem. 2017; 120: 30-9

[53]

Kc S, Long L, Zhang Q. et al. Effect of interactions between phosphorus and light intensity on metabolite compositions in tea cultivar Longjing43. Int J Mol Sci. 2022; 23:15194

[54]

Yu S, Li P, Zhao X. et al. CsTCPs regulate shoot tip development and catechin biosynthesis in tea plant (Camellia sinensis). Hortic Res. 2021; 8:104

[55]

Luo Y, Yu S, Li J. et al. Molecular characterization of WRKY transcription factors that act as negative regulators of O-methylated catechins biosynthesis in tea plant (Camellia sinensis L.). J Agric Food Chem. 2018; 66:11234-43

[56]

Lv Q, Zhong Y, Wang Y. et al. SPX4 negatively regulates phosphate signaling and homeostasis through its interaction with PHR2 in rice. Plant Cell. 2014; 26:1586-97

[57]

Osorio MB, Ng S, Berkowitz O. et al. SPX4 acts on PHR1-dependent and -independent regulation of shoot phosphorus status in Arabidopsis. Plant Physiol. 2019; 181:332-52

[58]

Srivastava R, Roychowdhury A, Kumar R. Host SPX-PHR regulatory circuit: the molecular dynamo steering mycorrhization in plants. Plant Cell Rep. 2022; 41:1329-32

[59]

Zhao MY, Wang L, Wang J. et al. Induction of priming by cold stress via inducible volatile cues in neighboring tea plants. J Integr Plant Biol. 2020; 62:1461-8

[60]

He KR, du J, Han X. et al. PHOSPHATE STARVATION RESPONSE1 (PHR1) interacts with JASMONATE ZIM-DOMAIN (JAZ) and MYC2 to modulate phosphate deficiency-induced jasmonate signaling in Arabidopsis. Plant Cell. 2023; 35:2132-56

[61]

Yang M, Luo F, Zhang X. et al. Uptake, translocation, and metabolism of anthracene in tea plants. Sci Total Environ. 2022; 821:152905

[62]

Zhang XY, Li L, He Y. et al. The CsHSFA-CsJAZ6 module-mediated high temperature regulates flavonoid metabolism in Camellia sinensis. Plant Cell Environ. 2023; 46:2401-18

[63]

Hu C-J, Gao Y, Liu Y. et al. Studies on the mechanism of efficient extraction of tea components by aqueous ethanol. Food Chem. 2016; 194:312-8

[64]

Chen ST, Kong Y, Zhang X. et al. Structural and functional organization of the MYC transcriptional factors in Camellia sinensis. Planta. 2021; 253:93

[65]

Clough SJ, Bent AF. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J: Cell Mol Biol. 1998; 16:735-43

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