CsLAC4, regulated by CsmiR397a, confers drought tolerance to the tea plant by enhancing lignin biosynthesis

Hongbin Yang, Linxuan Xia, Jingshan Li, Xiaoyu Jia, Xinyue Jia, Yuying Qi, Youben Yu, Weidong Wang

Stress Biology ›› 2024, Vol. 4 ›› Issue (1) : 50.

Stress Biology ›› 2024, Vol. 4 ›› Issue (1) : 50. DOI: 10.1007/s44154-024-00199-1
Original Paper

CsLAC4, regulated by CsmiR397a, confers drought tolerance to the tea plant by enhancing lignin biosynthesis

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Abstract

Drought is a prevalent abiotic stress that commonly affects the quality and yield of tea. Although numerous studies have shown that lignin accumulation holds significant importance in conferring drought tolerance to tea plants, the underlying molecular regulatory mechanisms governing the tea plant's response to drought remain largely elusive. LACCASEs (LACs), which belong to the class of plant copper-containing polyphenol oxidases, have been widely reported to participate in lignin biosynthesis in plants and are implicated in numerous plant life processes, especially in the context of adverse conditions. In this study, we detected the upregulation of CsLAC4 in response to drought induction. Remarkably, the overexpression of CsLAC4 not only substantially increased the lignin content of transgenic Arabidopsis thaliana but also simulated the development of vascular tissues, consequently leading to a significant enhancement in drought tolerance. Moreover, via dual-luciferase assays and transient overexpression in tea leaves, we revealed that CsLAC4 was negatively regulated by the upstream CsmiR397a. Interestingly, the expression of CsmiR397a was downregulated during drought stress in tea plants. Arabidopsis thaliana overexpressing CsmiR397a showed increased sensitivity to drought stress. By transient overexpression of CsmiR397a and CsLAC4 in tea plant leaves, we verified that CsLAC4, which is regulated by CsmiR397a, conferred drought tolerance to tea plants by enhancing lignin biosynthesis. These findings enhance our understanding of the molecular regulatory mechanisms underlying the response of tea plants to drought stress.

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Hongbin Yang, Linxuan Xia, Jingshan Li, Xiaoyu Jia, Xinyue Jia, Yuying Qi, Youben Yu, Weidong Wang. CsLAC4, regulated by CsmiR397a, confers drought tolerance to the tea plant by enhancing lignin biosynthesis. Stress Biology, 2024, 4(1): 50 https://doi.org/10.1007/s44154-024-00199-1

References

[]
Bai H, Chen J, Gao T, Tang Z, Li H, Gong S et al (2023) A Na+/H+ antiporter localized on the Golgi-to-vacuole transport system from Camellia sinensis, CsNHX6, plays a positive role in salt tolerance. Sci Hortic 309:111704. https://doi.org/10.1016/j.scienta.2022.111704
[]
Bang SW, Choi S, Jin X, Jung SE, Choi JW, Seo JS et al (2022) Transcriptional activation of rice CINNAMOYL-CoA REDUCTASE 10 by OsNAC5, contributes to drought tolerance by modulating lignin accumulation in roots. Plant Biotechnol J 20(4):736–747. https://doi.org/10.1111/pbi.13752
[]
Blaschek L, Murozuka E, Serk H, Menard D, Pesquet E (2023) Different combinations of laccase paralogs nonredundantly control the amount and composition of lignin in specific cell types and cell wall layers in Arabidopsis. Plant Cell 35(2):889–909. https://doi.org/10.1093/plcell/koac344
[]
Cheng L, Liu H, Zhao J, Dong Y, Xu Q, Yu Y (2021) Hormone orchestrates a hierarchical transcriptional cascade that regulates Al-induced de novo root regeneration in tea nodal cutting. J Agric Food Chem 69(21):5858–5870. https://doi.org/10.1021/acs.jafc.1c01100
[]
Choi SJ, Lee Z, Kim S, Jeong E, Shim JS (2023) Modulation of lignin biosynthesis for drought tolerance in plants. Front Plant Sci 14:1116426. https://doi.org/10.3389/fpls.2023.1116426
[]
Gaddam SR, Sharma A, Trivedi PK (2024) miR397b-LAC2 module regulates cadmium stress response by coordinating root lignification and copper homeostasis in Arabidopsis thaliana. J Hazard Mater 465:133100. https://doi.org/10.1016/j.jhazmat.2023.133100
[]
Geng D, Chen P, Shen X, Zhang Y, Li X, Jiang L et al (2018) MdMYB88 and MdMYB124 enhance drought tolerance by modulating root vessels and cell walls in apple. Plant Physiol 178(3):1296–1309. https://doi.org/10.1104/pp.18.00502
[]
Hou N, Li C, He J, Liu Y, Yu S, Malnoy M et al (2022) MdMTA-mediated m6A modification enhances drought tolerance by promoting mRNA stability and translation efficiency of genes involved in lignin deposition and oxidative stress. New Phytol 234(4):1294–1314. https://doi.org/10.1111/nph.18069
[]
Huang S, Zhou J, Gao L, Tang Y (2021) Plant miR397 and its functions. Funct Plant Biol 48(4):361–370. https://doi.org/10.1071/fp20342
[]
Huang JH, Zhang LY, Lin XJ, Gao Y, Zhang J, Huang WL et al (2022) CsiLAC4 modulates boron flow in Arabidopsis and Citrus via high-boron-dependent lignification of cell walls. New Phytol 233(3):1257–1273. https://doi.org/10.1111/nph.17861
[]
Janusz G, Pawlik A, Swiderska-Burek U, Polak J, Sulej J, Jarosz-Wilkolazka A et al (2020) Laccase properties, physiological functions, and evolution. Int J Mol Sci 21:966. https://doi.org/10.3390/ijms21030966
[]
Khandal H, Singh AP, Chattopadhyay D (2020) The microRNA397b-LACCASE2 module regulates root lignification under water and phosphate deficiency. Plant Physiol 182(3):1387–1403. https://doi.org/10.1104/pp.19.00921
[]
Li L, Yang K, Wang S, Lou Y, Zhu C, Gao Z (2020) Genome-wide analysis of laccase genes in moso bamboo highlights PeLAC10 involved in lignin biosynthesis and in response to abiotic stresses. Plant Cell Rep 39(6):751–763. https://doi.org/10.1007/s00299-020-02528-w
[]
Li D, Yang J, Pak S, Zeng M, Sun J, Yu S et al (2022a) PuC3H35 confers drought tolerance by enhancing lignin and proanthocyanidin biosynthesis in the roots of Populus ussuriensis. New Phytol 233(1):390–408. https://doi.org/10.1111/nph.17799
[]
Li P, Fu J, Xu Y, Shen Y, Zhang Y, Ye Z et al (2022b) CsMYB1 integrates the regulation of trichome development and catechins biosynthesis in tea plant domestication. New Phytol 234(3):902–917. https://doi.org/10.1111/nph.18026
[]
Li X, Ma Z, Song Y, Shen W, Yue Q, Khan A et al (2023) Insights into the molecular mechanisms underlying responses of apple trees to abiotic stresses. Hortic Res 10(8):uhad144. https://doi.org/10.1093/hr/uhad144
[]
Li J, Ren J, Lei X, Fan W, Tang L, Zhang Q et al (2024) CsREV-CsTCP4-CsVND7 module shapes xylem patterns differentially between stem and leaf to enhance tea plant tolerance to drought. Cell Rep 43(4):113987. https://doi.org/10.1016/j.celrep.2024.113987
[]
Liu W, Jiang Y, Jin Y, Wang C, Yang J, Qi H (2021) Drought-induced ABA, H2O2 and JA positively regulate CmCAD genes and lignin synthesis in melon stems. BMC Plant Biol 21(1):83. https://doi.org/10.1016/j.celrep.2024.113987
[]
Menard D, Blaschek L, Kriechbaum K, Lee CC, Serk H, Zhu C et al (2022) Plant biomechanics and resilience to environmental changes are controlled by specific lignin chemistries in each vascular cell type and morphotype. Plant Cell 34(12):4877–4896. https://doi.org/10.1093/plcell/koac284
[]
Niu Z, Li G, Hu H, Lv J, Zheng Q, Liu J et al (2021) A gene that underwent adaptive evolution, LAC2 (LACCASE), in Populus euphratica improves drought tolerance by improving water transport capacity. Hortic Res 8(1):88. https://doi.org/10.1038/s41438-021-00518-x
[]
Pan C, Zhang M, Chen J, Lu H, Zhao X, Chen X et al (2024) MiR397 regulates cadmium stress response by coordinating lignin polymerization in the root exodermis in Kandelia obovata. J Hazard Mater 471:134313. https://doi.org/10.1016/j.jhazmat.2024.134313
[]
Qin R, Hu Y, Chen H, Du Q, Yang J, Li WX (2023) MicroRNA408 negatively regulates salt tolerance by affecting secondary cell wall development in maize. Plant Physiol 192(2):1569–1583. https://doi.org/10.1093/plphys/kiad135
[]
Qin XL, Zhao YQ, Zhang DJ, Wang KY, Chen WH, Tang ZZ et al (2024) Three species of rape responded to cadmium and melatonin alleviating Cd-toxicity in species-specific strategy. Environ Pollut 354:124178. https://doi.org/10.1016/j.envpol.2024.124178
[]
Shao C, Chen J, Lv Z, Gao X, Guo S, Xu R et al (2023) Staged and repeated drought-induced regulation of phenylpropanoid synthesis confers tolerance to a water deficit environment in Camellia sinensis. Ind Crops Prod 201:116843. https://doi.org/10.1016/j.indcrop.2023.116843
[]
Sharma NK, Gupta SK, Dwivedi V, Chattopadhyay D (2020) Lignin deposition in chickpea root xylem under drought. Plant Signal Behav 15(6):1754621. https://doi.org/10.1080/15592324.2020.1754621
[]
Sharma NK, Yadav S, Gupta SK, Irulappan V, Francis A, Senthil-Kumar M et al (2023) MicroRNA397 regulates tolerance to drought and fungal infection by regulating lignin deposition in chickpea root. Plant Cell Environ 46(11):3501–3517. https://doi.org/10.1111/pce.14666
[]
Shen Y, Li X, Ma G, Zhao Y, Jiang X, Gao L et al (2022) Roles of YABBY transcription factors in the regulation of leaf development and abiotic stress responses in Camellia sinensis. Beverage Plant Res 2(1):4. https://doi.org/10.48130/BPR-2022-0004
[]
Sun Q, Liu X, Yang J, Liu W, Du Q, Wang H et al (2018) MicroRNA528 Affects lodging resistance of maize by regulating lignin biosynthesis under nitrogen-luxury conditions. Mol Plant 11(6):806–814. https://doi.org/10.1016/j.molp.2018.03.013
[]
Tang Y, Lu L, Sheng Z, Zhao D, Tao J (2023) An R2R3-MYB network modulates stem strength by regulating lignin biosynthesis and secondary cell wall thickening in herbaceous peony. Plant J 113(6):1237–1258. https://doi.org/10.1111/tpj.16107
[]
Wang W (2016) Transcriptome analysis and functional characterisation of Histone H1 gene in the tea plant under high temperature and drought stress. Dissertation, Nanjing Agricultural University
[]
Wang W, Xin H, Wang M, Ma Q, Wang L, Kaleri NA et al (2016) Transcriptomic analysis reveals the molecular mechanisms of drought-stress-induced decreases in Camellia sinensis leaf quality. Front Plant Sci 7:385. https://doi.org/10.3389/fpls.2016.00385
[]
Wang Y, Wang Q, Zhang F, Han C, Li W, Ren M et al (2024) PbARF19-mediated auxin signaling regulates lignification in pear fruit stone cells. Plant Sci 344:112103. https://doi.org/10.1016/j.plantsci.2024.112103
[]
Wei T, Tang Y, Jia P, Zeng Y, Wang B, Wu P et al (2021) A Cotton Lignin Biosynthesis Gene, GhLAC4, Fine-tuned by ghr-miR397 modulates plant resistance against Verticillium dahliae. Front Plant Sci 12:743795. https://doi.org/10.3389/fpls.2021.743795
[]
Xiao Y, Dong Y, Zhang Y, Zhang Y, Liu L, Liu P et al (2023) Two galactinol synthases contribute to the drought response of Camellia sinensis. Planta 258(5):84. https://doi.org/10.1007/s00425-023-04238-5
[]
Xie J, Cao B, Xu K (2024) Uncovering the dominant role of root lignin accumulation in silicon-induced resistance to drought in tomato. Int J Biol Macromol 259(1):129075. https://doi.org/10.1016/j.ijbiomac.2023.129075
[]
Xu X, Zhang Y, Liang M, Kong W, Liu J (2022) The citrus laccase gene CsLAC18 contributes to cold tolerance. Int J Mol Sci 23:14509. https://doi.org/10.3390/ijms232314509
[]
Yan Y, Wang P, Lu Y, Bai Y, Wei Y, Liu G et al (2021) MeRAV5 promotes drought stress resistance in cassava by modulating hydrogen peroxide and lignin accumulation. Plant J 107(3):847–860. https://doi.org/10.1111/tpj.15350
[]
Yang Y, He Y, Lv S, Zhu H, Wang T, Wang G et al (2023) The PcMYB44-mediated miR397-PcLACs module regulates defence-induced lignification in pear resistance to fungal disease. Mol Plant Pathol 24(9):1107–1125. https://doi.org/10.1111/mpp.13357
[]
Yang H, Jia X, Gao T, Gong S, Xia L, Zhang P et al (2024) The CsmiR397a-CsLAC17 module regulates lignin biosynthesis to balance the tenderness and gray blight resistance in young tea shoots. Hortic Res 11(5):uhae085. https://doi.org/10.1093/hr/uhae085
[]
Yu Y, Xing Y, Liu F, Zhang X, Li X, Zhang J et al (2021) The laccase gene family mediate multi-perspective trade-offs during tea plant (Camellia sinensis) development and defense processes. Int J Mol Sci 22:12554. https://doi.org/10.3390/ijms222212554
[]
Zhang Y, He J, Xiao Y, Zhang Y, Liu Y, Wan S et al (2021) CsGSTU8, a glutathione S-transferase from Camellia sinensis, is regulated by CsWRKY48 and plays a positive role in drought tolerance. Front Plant Sci 12:795919. https://doi.org/10.3389/fpls.2021.795919
[]
Zhang Y, Shan X, Zhao Q, Shi F (2022a) The microRNA397a-LACCASE17 module regulates lignin biosynthesis in Medicago ruthenica (L.). Front Plant Sci 13:978515. https://doi.org/10.3389/fpls.2022.978515
[]
Zhang Y, Xiao Y, Zhang Y, Dong Y, Liu Y, Liu L et al (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. https://doi.org/10.1021/acs.jafc.2c04892
[]
Zhang H, Shang X, Zhou N, Han Z, Zhang C, Ma Y et al (2023) The effective role of CsTCP5 and CsTCP18 transcription factors from Camellia sinensis (L.) O. Kuntze under drought and low-temperature. Beverage Plant Res 3(1):29. https://doi.org/10.48130/BPR-2023-0029
[]
Zhao D, Luan Y, Shi W, Zhang X, Meng J, Tao J (2021) A Paeonia ostii caffeoyl-CoA O-methyltransferase confers drought stress tolerance by promoting lignin synthesis and ROS scavenging. Plant Sci 303:110765. https://doi.org/10.1016/j.plantsci.2020.110765
[]
Zhou Y, Zhang Y, Wang X, Han X, An Y, Lin S et al (2020) Root-specific NF-Y family transcription factor, PdNF-YB21, positively regulates root growth and drought resistance by abscisic acid-mediated indoylacetic acid transport in populus. New Phytol 227(2):407–426. https://doi.org/10.1111/nph.16524
[]
Zhou C, Tian C, Zhu C, Lai Z, Lin Y, Guo Y (2022) Hidden players in the regulation of secondary metabolism in tea plant: focus on non-coding RNAs. Beverage Plant Res 2(1):19. https://doi.org/10.48130/BPR-2022-0019
[]
Zhou C, Yang N, Tian C, Wen S, Zhang C, Zheng A et al (2024) The miR166 targets CsHDZ3 genes to negatively regulate drought tolerance in tea plant (Camellia sinensis). Int J Biol Macromol 264(2):130735. https://doi.org/10.1016/j.ijbiomac.2024.130735
[]
Zhu J, Zhang H, Huang K, Guo R, Zhao J, Xie H et al (2023) Comprehensive analysis of the laccase gene family in tea plant highlights its roles in development and stress responses. BMC Plant Biol 23(1):129. https://doi.org/10.1186/s12870-023-04134-w

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