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Sigma factor binding protein 1 (CsSIB1) is a putative candidate of the major-effect QTL dm5.3 for downy mildew resistance in cucumber (Cucumis sativus)

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Abstract

Key message

The dm5.3 major-effect QTL in cucumber encodes a homolog of Arabidopsis sigma factor binding protein 1 (CsSIB1). CsSIB1 positively regulates defense responses against downy mildew in cucumber through the salicylic acid (SA) biosynthesis/signaling pathway.

Abstract

Downy mildew (DM) caused by the oomycete pathogen Pseudoperonospora cubensis is an important disease of cucumber and other cucurbits. Our knowledge on molecular mechanisms of DM resistance is still limited. In this study, we reported identification and functional characterization of the candidate gene for the major-effect QTL, dm5.3 for DM resistance originated from PI 197088. The dm5.3 QTL was Modelized through marker-assisted development of near isogenic lines (NILs). NIL-derived segregating populations were used for fine mapping which narrowed the dm5.3 locus down to a 144 kb region. Based on multiple lines of evidence, we show that CsSIB1 (CsGy5G027140) that encodes the VQ motif-containing sigma factor binding protein 1 as the most likely candidate for dm5.3. Local association analysis identified a haplotype consisting of 7 SNPs inside the coding and promoter region of CsSIB1 that was associated with DM resistance. Expression of CsSIB1 was up-regulated with P. cubensis infection. Transcriptome profiling of NILs in response to P. cubensis inoculation revealed key players and associated gene networks in which increased expression of CsSIB1 antagonistically promoted salicylic acid (SA) but suppressed jasmonic acid (JA) biosynthesis/signaling pathways. Our work provides novel insights into the function of CsSIB1/dm5.3 as a disease resistance (R) gene. The roles of sigma factor binding protein genes in pathogen defense in cucumber were also discussed.

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Data and materials availability

All data pertinent to the reported work have been provided in the manuscript or in the supplemental online materials. The complete raw reads data for RNA-Seq reported in this study have been deposited to NCBI under BioProject accession PRJNA853345. The DNA sequences for the cucumber CsSIB1 genes have been deposited under NCBI GenBank accession numbers ON911570 and ON911570.

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Acknowledgements

The authors are grateful to Dr. Todd Wehner of North Carolina State University (Raleigh, NC), and Dr. Peter Kraan (Nunhems Netherlands BV) for help screen downy mildew resistances. We also thank Ashley Seufzer (USDA-ARS, Madison, WI) for technical help. USDA is an equal opportunity employer.

Funding

This study was supported by the National Institute of Food and Agriculture, US Department of Agriculture, under award numbers 2017–67013-26195 and 2020–51181-32139.

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Authors and Affiliations

  1. Horticulture Department, University of Wisconsin, Madison, WI, 53706, USA

    Junyi Tan, Yuhui Wang, Ronald Dymerski, Zhiming Wu & Yiqun Weng

  2. Institute of Cash Crops, Hebei Academy of Agriculture & Forestry Sciences, Shijiazhuang, 050051, Hebei, China

    Zhiming Wu

  3. USDA-ARS Vegetable Crops Research Unit, Madison, WI, 53706, USA

    Yiqun Weng

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Contributions

JT conducted majority of the reported work. YHW and ZW participated in NIL development, and screening tests for downy mildew resistances. RD contributed to association analysis in natural populations. YQW conceived and supervised the study and wrote the manuscript with JT. All authors reviewed and approved this submission.

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Correspondence to Yiqun Weng.

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Tan, J., Wang, Y., Dymerski, R. et al. Sigma factor binding protein 1 (CsSIB1) is a putative candidate of the major-effect QTL dm5.3 for downy mildew resistance in cucumber (Cucumis sativus). Theor Appl Genet 135, 4197–4215 (2022). https://doi.org/10.1007/s00122-022-04212-x

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