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24-Epibrassinolide Enhances Resistance Against Colletotrichum fructicola by Promoting Lignin Biosynthesis in Camellia sinensis L.

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Abstract

Brassinosteroids (BRs) are steroid-type phytohormones that not only control growth and development but also responses to biotic and abiotic stressors in plants. However, little is known about the function of BRs in the protection of tea against the fungal pathogen Colletotrichum fructicola causing anthracnose disease. Here, we revealed that 24-epibrassinolide (EBR) could improve tea resistance against C. fructicola, which was linked to the EBR-induced accumulation of lignin in tea leaves. Time-course of the relative expression of ITS/Cs18SrDNA showed that its expression increased after the inoculation with C. fructicola; however, EBR pretreatment significantly decreased the ITS/Cs18SrDNA expression at 3, 24 and 96 h postinoculation. Following an initial increase in 3 h postinoculation, lignin content significantly decreased from 6 to 24 h postinoculation with C. fructicola. In contrast to inoculation with only C. fructicola, exogenous EBR pretreatment significantly increased lignin contents throughout the postinoculation period. According to the qRT-PCR assay, EBR and C. fructicola differentially regulated the expression of 14 genes involved in the phenylpropanoid and lignin-specific pathways. Moreover, the activity of peroxidase (POD), a central enzyme in the final phase of lignin biosynthesis increased significantly at 3 h postinoculation with EBR treatment. Gene expression analysis revealed that EBR induced CsMYB4-like expression possibly to activate the transcription of CsPOD5-like gene responsible for lignin biosynthesis in response to C. fructicola. These findings suggest that EBR plays a positive role in disease resistance by inducing lignin synthesis, which may have potential application for the prevention of C. fructicola in tea plants.

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References

  • Ahammed GJ, Yu JQ (2022) Brassinosteroids in plant developmental biology and stress tolerance. Elsevier, Amsterdam

    Google Scholar 

  • Ahammed GJ, Li X, Liu A, Chen S (2020) Brassinosteroids in plant tolerance to abiotic stress. J Plant Growth Regul 39:1451–1464

    Article  CAS  Google Scholar 

  • Ali SS, Gunupuru LR, Kumar GBS, Khan M, Scofield S, Nicholson P, Doohan FM (2014) Plant disease resistance is augmented in uzu barley lines modified in the brassinosteroid receptor BRI1. BMC Plant Biol 14:227

    Article  PubMed  PubMed Central  Google Scholar 

  • Chakraborty N, Mukherjee K, Sarkar A, Acharya K (2019) Interaction between bean and Colletotrichum gloeosporioides: understanding through a biochemical approach. Plants 8:345

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Silva DD, Crous PW, Ades PK, Hyde KD, Taylor PWJ (2017) Life styles of Colletotrichum species and implications for plant biosecurity. Fungal Biol Rev 31:155–168

    Article  Google Scholar 

  • Dong NQ, Lin HX (2021) Contribution of phenylpropanoid metabolism to plant development and plant-environment interactions. J Integr Plant Biol 63:180–209

    Article  CAS  PubMed  Google Scholar 

  • Eskandari S, Hofte H, Zhang T (2020) Foliar manganese spray induces the resistance of cucumber to Colletotrichum lagenarium. J Plant Physiol 246–247:153129

    Article  PubMed  Google Scholar 

  • Furio RN, Albornoz PL, Coll Y, Martínez Zamora GM, Salazar SM, Martos GG, Díaz Ricci JC (2018) Effect of natural and synthetic Brassinosteroids on strawberry immune response against Colletotrichum acutatum. Eur J Plant Pathol 153:167–181

    Article  Google Scholar 

  • Guo M, Pan YM, Dai YL, Gao ZM (2014) First report of brown blight disease caused by Colletotrichum gloeosporioides on Camellia sinensis in Anhui Province, China. Plant Dis 98:284–284

    Article  CAS  PubMed  Google Scholar 

  • Han W, Li X, Yan P, Zhang L, Jalal Ahammed G (2018) Tea cultivation under changing climatic conditions, pp 455–472

  • He S, Chen H, Wei Y, An T, Liu S (2020) Development of a DNA-based real-time PCR assay for the quantification of Colletotrichum Camelliae growth in tea (Camellia Sinensis). Plant Methods 16(1):1–11. https://doi.org/10.1186/s13007-020-00564-x

    Article  CAS  Google Scholar 

  • Hu M, Zhu Y, Liu G, Gao Z, Li M, Su Z, Zhang Z (2019) Inhibition on anthracnose and induction of defense response by nitric oxide in pitaya fruit. Sci Hortic 245:224–230

    Article  CAS  Google Scholar 

  • Janeczko A, Saja D, Dziurka M, Gullner G, Kornaś A, Skoczowski A, Gruszka D, Barna B (2019) Brassinosteroid deficiency caused by the mutation of the HvDWARF gene influences the reactions of barley to powdery mildew. Physiol Mol Plant Pathol 108:101438

    Article  CAS  Google Scholar 

  • Jeyaraj A, Elango T, Yu Y, Chen X, Zou Z, Ding Z, Zhao Z, Chen X, Li X, Chen L (2021) Impact of exogenous caffeine on regulatory networks of microRNAs in response to Colletotrichum gloeosporioides in tea plant. Sci Hortic 279:109914

    Article  CAS  Google Scholar 

  • Kour J, Kohli SK, Khanna K, Bakshi P, Sharma P, Singh AD, Ibrahim M, Devi K, Sharma N, Ohri P, Skalicky M, Brestic M, Bhardwaj R, Landi M, Sharma A (2021) Brassinosteroid signaling, crosstalk and physiological functions in plants under heavy metal stress. Front Plant Sci 12:608061

    Article  PubMed  PubMed Central  Google Scholar 

  • Li X, Ahammed GJ, Li Z, Tang M, Yan P, Han W (2016) Decreased biosynthesis of Jasmonic acid via lipoxygenase pathway compromised caffeine-induced resistance to Colletotrichum gloeosporioides under elevated CO2 in tea seedlings. Phytopathology 106:1270–1277

    Article  CAS  PubMed  Google Scholar 

  • Li G, Zhu S, Wu W, Zhang C, Peng Y, Wang Q, Shi J (2017) Exogenous nitric oxide induces disease resistance against Monilinia fructicola through activating the phenylpropanoid pathway in peach fruit. J Sci Food Agric 97:3030–3038

    Article  CAS  PubMed  Google Scholar 

  • Li X, Wei J-P, Ahammed GJ, Zhang L, Li Y, Yan P, Zhang L-P, Han W-Y (2018) Brassinosteroids attenuate moderate high temperature-caused decline in tea quality by enhancing theanine biosynthesis in Camellia sinensis L. Front Plant Sci 9:1016

    Article  PubMed  PubMed Central  Google Scholar 

  • Li X, Ahammed GJ, Zhang XN et al (2021) Melatonin-mediated regulation of anthocyanin biosynthesis and antioxidant defense confer tolerance to arsenic stress in Camellia sinensis L. J Hazard Mater 403:123922

    Article  CAS  PubMed  Google Scholar 

  • Lin SR, Yu SY, Chang TD, Lin YJ, Wen CJ, Lin YH (2020) First report of anthracnose caused by Colletotrichum fructicola on tea in Taiwan. Plant Dis 105:710

    Article  Google Scholar 

  • Liu X, Yang H, Wang Y, Zhu Z, Zhang W, Li J (2020) Comparative transcriptomic analysis to identify brassinosteroid response genes. Plant Physiol 184:1072–1082

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu Q, Wang Y, Li N, Ni D, Yang Y, Wang X (2018) Differences in the characteristics and pathogenicity of Colletotrichum camelliae and C. fructicola isolated from the tea plant [Camellia sinensis (L.) O. Kuntze]. Front Microbiol 9:3060

    Article  PubMed  PubMed Central  Google Scholar 

  • Novo M, Silvar C, Merino F, Martinez-Cortes T, Lu F, Ralph J, Pomar F (2017) Deciphering the role of the phenylpropanoid metabolism in the tolerance of Capsicum annuum L. to Verticillium dahliae Kleb. Plant Sci 258:12–20

    Article  CAS  PubMed  Google Scholar 

  • Ortiz-Morea FA, He P, Shan L, Russinova E (2020) It takes two to tango—molecular links between plant immunity and brassinosteroid signalling. J Cell Sci 133:jcs246728

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park P, Kurihara T, Nita M, Ikeda K, Inoue K, Ishii H (2019) Application of energy-filtering electron microscopy (EFEM) for analysis of hydrogen peroxide and lignin in epidermal walls of cucumber leaves triggered by acibenzolar-S-methyl treatment prior to inoculation with Colletotrichum orbiculare. Plant Pathol 68:1624–1634

    Article  CAS  Google Scholar 

  • Ren Y, Xue Y, Tian D, Zhang L, Xiao G, He J (2020) Improvement of postharvest anthracnose resistance in mango fruit by nitric oxide and the possible mechanisms involved. J Agric Food Chem 68:15460–15467

    Article  CAS  PubMed  Google Scholar 

  • Shi Y-N, Liu X-F, Li X, Dong W-C, Grierson D, Yin X-R, Chen K-S (2017) SIMYB1 and SIMYB2, two new MYB genes from tomato, transcriptionally regulate cellulose biosynthesis in tobacco. J Integr Agric 16:65–75

    Article  CAS  Google Scholar 

  • Suzuki S, Suzuki Y, Yamamoto N et al (2009) High-throughput determination of thioglycolic acid lignin from rice. Plant Biotechnol 26:337–340

    Article  CAS  Google Scholar 

  • Ullah C, Tsai CJ, Unsicker SB, Xue L, Reichelt M, Gershenzon J, Hammerbacher A (2018) Salicylic acid activates poplar defense against the biotrophic rust fungus Melampsora larici-populina via increased biosynthesis of catechin and proanthocyanidins. New Phytol 221:960–975

    Article  PubMed  PubMed Central  Google Scholar 

  • Velho AC, Mondino P, Stadnik MJ (2018) Extracellular enzymes of Colletotrichum fructicola isolates associated to Apple bitter rot and Glomerella leaf spot. Mycology 9:145–154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang YC, Hao XY, Wang L, Bin X, Wang XC, Yang YJ (2016a) Diverse Colletotrichum species cause anthracnose of tea plants (Camellia sinensis (L.) O. Kuntze) in China. Sci Rep 6:35287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang YC, Qian WJ, Li NN, Hao XY, Wang L, Xiao B, Wang XC, Yang YJ (2016b) Metabolic changes of caffeine in tea plant (Camellia sinensis (L.) O. Kuntze) as defense response to Colletotrichum fructicola. J Agric Food Chem 64:6685–6693

    Article  CAS  PubMed  Google Scholar 

  • Wei Y, Zhou D, Peng J, Pan L, Tu K (2017) Hot air treatment induces disease resistance through activating the phenylpropanoid metabolism in cherry tomato fruit. J Agric Food Chem 65:8003–8010

    Article  CAS  PubMed  Google Scholar 

  • Xie M, Zhang J, Tschaplinski TJ, Tuskan GA, Chen JG, Muchero W (2018) Regulation of Lignin biosynthesis and its role in growth-defense tradeoffs. Front Plant Sci 9:1427. https://doi.org/10.3389/fpls.2018.01427

    Article  PubMed  PubMed Central  Google Scholar 

  • Yogendra KN, Kumar A, Sarkar K, Li Y, Pushpa D, Mosa KA, Duggavathi R, Kushalappa AC (2015) Transcription factor StWRKY1 regulates phenylpropanoid metabolites conferring late blight resistance in potato. J Exp Bot 66:7377–7389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu M-H, Zhao Z-Z, He J-X (2018) Brassinosteroid signaling in plant-microbe interactions. Int J Mol Sci 19:4091

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang L, Ahammed GJ, Li X, Wei J-P, Li Y, Yan P, Zhang L-P, Han W-Y (2018) Exogenous brassinosteroid enhances plant defense against Colletotrichum gloeosporioides by activating phenylpropanoid pathway in Camellia sinensis L. J Plant Growth Regul 37:1235–1243

    Article  CAS  Google Scholar 

  • Zhang L, Jiang X, Liu Q, Ahammed GJ, Lin R, Wang L, Shao S, Yu J, Zhou Y (2020) The HY5 and MYB15 transcription factors positively regulate cold tolerance in tomato via the CBF pathway. Plant Cell Environ 43:2712–2726

    Article  CAS  PubMed  Google Scholar 

  • Zhong C, Tang Y, Pang B, Li X, Yang Y, Deng J, Feng C, Li L, Ren G, Wang Y, Peng J, Sun S, Liang S, Wang X (2020) The R2R3-MYB transcription factor GhMYB1a regulates flavonol and anthocyanin accumulation in Gerbera hybrida. Hortic Res 7:78

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou J, Lee C, Zhong R, Ye ZH (2009) MYB58 and MYB63 are transcriptional activators of the lignin biosynthetic pathway during secondary cell wall formation in Arabidopsis. Plant Cell 21:248–266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank the support of the Key Research and Development Program of Zhejiang Province (2021C02040); the Zhejiang Provincial Natural Science Foundation (LY19C160009); the National Key R&D Program of China (2020YFD10007; 2017YFE0107500); the Innovation Project of the Chinese Academy of Agricultural Sciences (CAAS-ASTIP-2019-TRICAAS); the National Natural Science Foundation of China (31950410555); Ministry of Science and Technology of the People’s Republic of China (QNJ20200226001, QNJ2021026001); Henan Engineering Technology Research Center for Horticultural Crop safety and Disease Control; and Henan International Joint Laboratory of Stress Resistance Regulation and Safe Production of Protected Vegetables.

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  1. Lan Zhang and Zheng Zhang contributed equally to this work.

Authors and Affiliations

  1. Key Laboratory of Tea Quality and Safety Control, Ministry of Agriculture, Tea Research Institute, Chinese Academy of Agricultural Sciences, Hangzhou, 310008, People’s Republic of China

    Lan Zhang, Zheng Zhang, Golam Jalal Ahammed, Peng Yan, Li-Ping Zhang, Shibei Ge, Jianyu Fu, Wen-Yan Han & Xin Li

  2. College of Horticulture and Plant Protection, Henan University of Science and Technology, Luoyang, 471023, People’s Republic of China

    Golam Jalal Ahammed

  3. School of Economics and Management, Hebei Institute of Architecture and Civil Engineering, Zhangjiakou, 075000, People’s Republic of China

    Xiaorong Wang

  4. Tea Science Research Institute in Kaihua Agricultural and Rural Affairs Bureau, Quzhou, 324000, People’s Republic of China

    Huihan Fang

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  1. Lan Zhang
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Contributions

XL and LZ conceived and designed the research; LZ, ZZ, GJA, XW, HF, L-PZ, PY, SG and JF performed the experiments and analyzed the data; XL, LZ, GJA, ZZ, XW, HF and W-YH discussed the data; LZ, GJA and XL wrote the manuscript with the contributions from the other authors.

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Correspondence to Golam Jalal Ahammed or Xin Li.

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Zhang, L., Zhang, Z., Ahammed, G.J. et al. 24-Epibrassinolide Enhances Resistance Against Colletotrichum fructicola by Promoting Lignin Biosynthesis in Camellia sinensis L.. J Plant Growth Regul 42, 1558–1566 (2023). https://doi.org/10.1007/s00344-022-10640-2

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