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Characterization of caffeoyl shikimate esterase gene family identifies CsCSE5 as a positive regulator of Podosphaera xanthii and Corynespora cassiicola pathogen resistance in cucumber

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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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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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Correspondence to Xiangnan Meng or Haiyan Fan.

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Communicated by Haitao Shi.

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Supplementary Information

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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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Supplementary file7 (XLSX 10 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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