Abstract
Key message
CsCSE genes might be involved in the tolerance of cucumber to pathogens. Silencing of the CsCSE5 gene resulted in attenuated resistance of cucumber to Podosphaera xanthii and Corynespora cassiicola.
Abstract
Caffeoyl shikimate esterase (CSE), a key enzyme in the lignin biosynthetic pathway, has recently been characterized to play a key role in defense against pathogenic infection in plants. However, a systematic analysis of the CSE gene family in cucumber (Cucumis sativus) has not yet been conducted. Here, we identified eight CsCSE genes from the cucumber genome via bioinformatic analyses, and these genes were unevenly distributed on chromosomes 1, 3, 4, and 5. Results from multiple sequence alignment indicated that the CsCSE proteins had domains required for CSE activity. Phylogenetic analysis of gene structure and protein motifs revealed the conservation and diversity of the CsCSE gene family. Collinearity analysis showed that CsCSE genes had high homology with CSE genes in wax gourd (Benincasa hispida). Cis-acting element analysis of the promoters suggested that CsCSE genes might play important roles in growth, development, and stress tolerance. Expression pattern analysis indicated that CsCSE5 might be involved in regulating the resistance of cucumber to pathogens. Functional verification data confirmed that CsCSE5 positively regulates the resistance of cucumber to powdery mildew pathogen Podosphaera xanthii and target leaf spot pathogen Corynespora cassiicola. The results of our study provide information that will aid the genetic improvement of resistant cucumber varieties.
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References
Bacete L, Méelida H, Miedes E, Molina A (2018) Plant cell wall-mediated immunity: cell wall changes trigger disease resistance responses. Plant J 93:614–636
Cao Y, Yan X, Ran S, Ralph J, Smith RA, Chen X, Qu C, Li J, Liu L (2022) Knockout of the lignin pathway gene BnF5H decreases the S/G lignin compositional ratio and improves Sclerotinia sclerotiorum resistance in Brassica napus. Plant Cell Environ 45:248–261
Cesarino I (2019) Structural features and regulation of lignin deposited upon biotic and abiotic stresses. Curr Opin Biotechnol 56:209–214
Dong NQ, Lin HX (2021) Contribution of phenylpropanoid metabolism to plant development and plant-environment interactions. J Integr Plant Biol 63:180–209
Engelsdorf T, Kjaer L, Gigli-Bisceglia N, Vaahtera L, Bauer S, Miedes E, Wormit A, James L, Chairam I, Molina A, Hamann T (2019) Functional characterization of genes mediating cell wall metabolism and responses to plant cell wall integrity impairment. BMC Plant Biol 19:320
Eynck C, Séguin-Swartz G, Clarke WE, Parkin IAP (2012) Monolignol biosynthesis is associated with resistance to Sclerotinia sclerotiorum in Camelina sativa. Mol Plant Pathol 13:887–899
Gao W, Li HY, Xiao S, Chye ML (2010) Acyl-CoA-binding protein 2 binds lysophospholipase 2 and lysoPC to promote tolerance to cadmium-induced oxidative stress in transgenic Arabidopsis. Plant J 62:989–1003
Ha CM, Escamilla-Trevino L, Yarce JCS, Kim H, Ralph J, Chen F, Dixon RA (2016) An essential role of caffeoyl shikimate esterase in monolignol biosynthesis in Medicago truncatula. Plant J 86:363–375
Höch K, Koopmann B, von Tiedemann A (2021) Lignin composition and timing of cell wall lignification are involved in Brassica napus resistance to stem rot caused by Sclerotinia sclerotiorum. Phytopathology 111:1438–1448
Jang HA, Bae EK, Kim MH, Park SJ, Choi NY, Pyo SW, Lee C, Jeong HY, Lee H, Choi YI, Ko JH (2021) CRISPR-knockout of CSE gene improves saccharification efficiency by reducing lignin content in hybrid poplar. Int J Mol Sci 22:9750
Lee MH, Jeon HS, Kim SH, Chung JH, Roppolo D, Lee HJ, Cho HJ, Tobimatsu Y, Ralph J, Park OK (2019) Lignin-based barrier restricts pathogens to the infection site and confers resistance in plants. EMBO J 38:e101948
Liu Q, Luo L, Zheng L (2018) Lignins: biosynthesis and biological functions in plants. Int J Mol Sci 19:335
Liu M, Liang Z, Aranda MA, Hong N, Liu L, Kang B, Gu Q (2020) A cucumber green mottle mosaic virus vector for virus-induced gene silencing in cucurbit plants. Plant Methods 16:9
Ma QH, Zhu HH, Qiao MY (2018) Contribution of both lignin content and sinapyl monomer to disease resistance in tobacco. Plant Pathol 67:642–650
Meng XN, Yu Y, Zhao JY, Cui N, Song TF, Yang Y, Fan HY (2018) The two translationally controlled tumor protein genes, CsTCTP1 and CsTCTP2, are negative modulators in the Cucumis sativus defense response to Sphaerotheca fuliginea. Front Plant Sci 9:544
Molina A, Miedes E, Bacete L, Rodríguez T, Mélida H, Denancé N, Sánchez-Vallet A, Riviére MP, López G, Freydier A, Barlet X, Pattathil S, Hahn M, Goffner D (2021) Arabidopsis cell wall composition determines disease resistance specificity and fitness. Proc Natl Acad Sci USA 118:e2010243118
Moura JC, Bonine CA, de Oliveira Fernandes Viana J, Dornelas MC, Mazzafera P (2010) Abiotic and biotic stresses and changes in the lignin content and composition in plants. J Integr Plant Biol 52:360–376
Nie J, Wang Y, He H, Guo C, Zhu W, Pan J, Li D, Lian H, Pan J, Cai R (2015) Loss-of-function mutations in CsMLO1 confer durable powdery mildew resistance in cucumber (Cucumis sativus L.). Front Plant Sci 6:1155
Ozparpucu M, Gierlinger N, Cesarino I, Burgert I, Boerjan W, Rüggeberg M (2019) Significant influence of lignin on axial elastic modulus of poplar wood at low microfibril angles under wet conditions. J Exp Bot 70:4039–4047
Ralph J, Lundquist K, Brunow G, Lu F, Kim H, Schatz PF, Marita JM, Hatfield RD, Ralph SA, Christensen JH (2004) Lignins: natural polymers from oxidative coupling of 4-hydroxyphenyl-propanoids. Phytochem Rev 3:29–60
Ren HM (2011) Inhibitive mechanisms of chrysophanol against Sphaerotheca Fuliginea. Dissertation, Agricultural University of Hebei
Saleme MDLS, Cesarino I, Vargas L, Kim H, Vanholme R, Goeminne G, Acker RV, Fonseca FCDA, Pallidis A, Voorend W, Junior JN, Padmakshan D, Doorsselaere JV, Ralph J, Boerjan W (2017) Silencing CAFFEOYL SHIKIMATE ESTERASE affects lignification and improves saccharification in poplar. Plant Physiol 175:1040–1057
Swarbreck D, Wilks C, Lamesch P, Berardini TZ, Garcia-Hernandez M, Foerster H, Li D, Meyer T, Muller R, Ploetz L, Radenbaugh A, Singh S, Swing V, Tissier C, Zhang P, Huala E (2008) The Arabidopsis information resource (TAIR): gene structure and function annotation. Nucleic Acids Res 36:D1009–D1014
Vanholme R, Cesarino I, Rataj K, Xiao Y, Sundin L, Goeminne G, Kim H, Cross J, Morreel K, Araujo P, Welsh L, Haustraete J, McClellan C, Vanholme B, Ralph J, Simpson GG, Halpin C, Boerjan W (2013) Caffeoyl shikimate esterase (CSE) is an enzyme in the lignin biosynthetic pathway in Arabidopsis. Science 341:1103–1106
Vanholme R, De Meester B, Ralph J, Boerjan W (2019) Lignin biosynthesis and its integration into metabolism. Curr Opin Biotechnol 56:230–239
Vargas L, Cesarino I, Vanholme R, Voorend W, de Lyra Soriano Saleme M, Morreel K, Boerjan W (2016) Improving total saccharification yield of Arabidopsis plants by vessel-specific complementation of caffeoyl shikimate esterase (cse) mutants. Biotechnol Biofuels 9:139
Vijayaraj P, Jashal CB, Vijayakumar A, Rani SH, Venkata Rao DK, Rajasekharan R (2012) A bifunctional enzyme that has both monoacylglycerol acyltransferase and acyl hydrolase activities. Plant Physiol 160:667–683
Vries LD, Brouckaert M, Chanoca A, Kim H, Regner MR, Timokhin VI, Sun Y, Meester BD, Doorsselaere JV, Goeminne G, Chiang VL, Wang JP, Ralph J, Morreel K, Vanholme R, Boerjan W (2021) CRISPR-Cas9 editing of CAFFEOYL SHIKIMATE ESTERASE 1 and 2 shows their importance and partial redundancy in lignification in Populus tremula × P. alba. Plant Biotechnol J 19:2221–2234
Walther D, Brunnemann R, Selbig J (2007) The regulatory code for transcriptional response diversity and its relation to genome structural properties in A. thaliana. PLoS Genet 3:e11
Wang A, Loo R, Chen Z, Dennis EA (1997) Regiospecificity and catalytic triad of lysophospholipase I. J Biol Chem 272:22030–22036
Wang X, Zhang D, Cui Na Yu, Yang YuG, Fan H (2018) Transcriptome and miRNA analyses of the response to Corynespora cassiicola in cucumber. Sci Rep 8:7798
Wang JP, Liu B, Sun Y, Chiang VL, Sederoff RR (2019) Enzyme-enzyme interactions in monolignol biosynthesis. Front Plant Sci 9:1942
Wang X, Chao N, Zhang A, Kang J, Jiang X, Gai Y (2021a) Systematic analysis and biochemical characterization of the caffeoyl shikimate esterase gene family in poplar. Int J Mol Sci 22:13366
Wang X, Chen Q, Huang J, Meng X, Cui N, Yu Y, Fan H (2021b) Nucleotide-binding leucine-rich repeat genes CsRSF1 and CsRSF2 are positive modulators in the Cucumis sativus defense response to Sphaerotheca fuliginea. Int J Mol Sci 22:3986
Xia L, He X, Huang X, Yu H, Lu T, Xie X, Zeng X, Zhu J, Luo C (2022) Genome-wide identification and expression analysis of the 14–3–3 gene family in mango (Mangifera indica L.). Int J Mol Sci 23:1593
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
Xiong XP, Sun SC, Zhu QH, Zhang XY, Li YJ, Liu F, Xue F, Sun J (2021) The cotton lignin biosynthetic gene Gh4CL30 regulates lignification and phenolic content and contributes to Verticillium wilt resistance. Mol Plant Microbe Interact 34:240–254
Xu J, Tao X, Xie Z, Gong X, Qi K, Zhang S, Shiratake K, Tao S (2021) PbCSE1 promotes lignification during stone cell development in pear (Pyrus bretschneideri) fruit. Sci Rep 11:9450
Yang C, Liu R, Pang J, Ren B, Zhou H, Wang G, Wang E, Liu J (2021) Poaceae-specific cell wall-derived oligosaccharides activate plant immunity via OsCERK1 during Magnaporthe oryzae infection in rice. Nat Commun 12:2178
Yao Y, Zhao H, Sun L, Wu W, Li C, Wu Q (2022) Genome-wide identification of MAPK gene family members in Fagopyrum tataricum and their expression during development and stress responses. BMC Genomics 23:96
Yu Y, Yu Y, Cui N, Ma L, Tao R, Ma Z, Meng X, Fan H (2022) Lignin biosynthesis regulated by CsCSE1 is required for Cucumis sativus defence to Podosphaera xanthii. Plant Physiol Biochem 186:88–98
Zhang Y, Wu L, Wang X, Chen B, Zhao J, Cui J, Li Z, Yang J, Wu L, Wu J, Zhang G, Ma Z (2019) The cotton laccase gene GhLAC15 enhances Verticillium wilt resistance via an increase in defence-induced lignification and lignin components in the cell walls of plants. Mol Plant Pathol 20:309–322
Zhang P, Zhu YQ, Zhou SJ (2021) Comparative analysis of powdery mildew resistant and susceptible cultivated cucumber (Cucumis sativus L.) varieties to reveal the metabolic responses to Sphaerotheca fuliginea infection. BMC Plant Biol 21:24
Zhou X, Liao H, Chern M, Yin J, Chen Y, Wang J, Zhu X, Chen Z, Yuan C, Zhao W, Wang J, Li W, He M, Ma B, Wang J, Qin P, Chen W, Wang Y, Liu J, Qian Y, Wang W, Wu X, Li P, Zhu L, Li S, Ronald PC, Chen X (2018) Loss of function of a rice TPR-domain RNA-binding protein confers broad-spectrum disease resistance. Proc Natl Acad Sci USA 115:3174–3179
Zhu X, Rong W, Wang K, Guo W, Zhou M, Wu J, Ye X, Wei X, Zhang Z (2021) Overexpression of TaSTT3b-2B improves resistance to sharp eyespot and increases grain weight in wheat. Plant Biotechnol J 20:777–793
Zhu Y, Hu X, Wang P, Wang H, Ge X, Li F, Hou Y (2022) GhODO1, an R2R3-type MYB transcription factor, positively regulates cotton resistance to Verticillium dahliae via the lignin biosynthesis and jasmonic acid signaling pathway. Int J Biol Macromol 201:580–591
Acknowledgements
We thank Qinsheng Gu (Professor of Zhengzhou Fruit Research Institute) for providing vectors, and Tiefeng Song (Researcher of Liaoning Academy of Agricultural Sciences) for the support of breeding technology.
Funding
This research was funded by the National Natural Science Foundation of China (32102366), the Natural Science Foundation of Liaoning Province of China (2020-BS-138) and the Initiative Grant of Shenyang Agricultural University (880419022).
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XM and HF designed the experiments. LL directed the experiments. YY, JH and HZ conducted the experimental operation. YY performed the data analysis and manuscript writing. MZ and JH revised the manuscript. All the authors have read and agreed to the published version of the manuscript.
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Communicated by Haitao Shi.
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299_2023_3074_MOESM1_ESM.tiff
Supplementary file1 Supplementary Fig. 1 Domain analysis of CsCSE proteins. Different domains are labeled with different color boxes (TIFF 225981 kb)
299_2023_3074_MOESM2_ESM.tiff
Supplementary file2 Supplementary Fig. 2 Chromosome distribution and duplication events of CsCSE genes. Partial circles with different colors represent different cucumber chromosomes, which are labeled CsChr1 to CsChr7. Eight CsCSE genes are mapped on the corresponding chromosomes according to their physical locations. The color bars in chromosomes indicate gene density. The gray lines indicate collinear blocks within the cucumber genome (TIFF 297648 kb)
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Yu, Y., He, J., Liu, L. et al. Characterization of caffeoyl shikimate esterase gene family identifies CsCSE5 as a positive regulator of Podosphaera xanthii and Corynespora cassiicola pathogen resistance in cucumber. Plant Cell Rep 42, 1937–1950 (2023). https://doi.org/10.1007/s00299-023-03074-x
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DOI: https://doi.org/10.1007/s00299-023-03074-x