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A new NLR gene for resistance to Tomato spotted wilt virus in tomato (Solanum lycopersicum)

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Abstract

Key message

A typical NLR gene, Sl5R-1 , which regulates Tomato spotted wilt virus resistance, was fine mapped to a region less than 145 kb in the tomato genome.

Abstract

Tomato spotted wilt is a viral disease caused by Tomato spotted wilt virus (TSWV), which is a devastating disease that affects tomato (Solanum lycopersicum) production worldwide, and the resistance provided by the Sw-5 gene has broken down in some cases. In order to identify additional genes that confer resistance to TSWV, the F2 population was mapped using susceptible (M82) and resistant (H149) tomato lines. After 3 years of mapping, the main quantitative trait locus on chromosome 05 was narrowed to a genomic region of 145 kb and was subsequently identified by the F2 population, with 1971 plants in 2020. This region encompassed 14 candidate genes, and in it was found a gene cluster consisting of three genes (Sl5R-1, Sl5R-2, and Sl5R-3) that code for NBS-LRR proteins. The qRT-PCR and virus-induced gene silencing approach results confirmed that Sl5R-1 is a functional resistance gene for TSWV. Analysis of the Sl5R-1 promoter region revealed that there is a SlTGA9 transcription factor binding site caused by a base deletion in resistant plants, and its expression level was significantly up-regulated in infected resistant plants. Analysis of salicylic acid (SA) and jasmonic acid (JA) levels and the expression of SA- and JA-regulated genes suggest that SlTGA9 interacts or positively regulates Sl5R-1 to affect the SA- and JA-signaling pathways to resist TSWV. These results demonstrate that the identified Sl5R-1 gene regulates TSWV resistance by its own promoter interacting with the transcription factor SlTGA9.

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Data availability statement

The data used to support the findings of this study are available from the corresponding author upon request.

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Acknowledgements

We greatly appreciate the experimental suggestions provided by Dr. Yan Liang and Xiangqiang Zhan. We thank Dr. Xiangqiang Zhan and Dr. Fei Zhang for their technical support.

Funding

This work was supported by the National Key Research and Development Program of China (2016YFD0101703) and Key Research and Development Program of Shaanxi Province (2019ZDLNY03-05) to YL (Yan Liang).

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Authors and Affiliations

  1. College of Horticulture, Northwest A&F University, Xianyang, 712100, Shaanxi, China

    Shiming Qi, Yuanbo Shen, Xinyu Wang, Shijie Zhang, Yushun Li, Md. Monirul Islam, Jin Wang, Pan Zhao, Xiangqiang Zhan, Fei Zhang & Yan Liang

  2. State Agriculture Ministry Laboratory of Northwest Horticultural Plant Germplasm Resources and Genetic Improvement, Northwest A&F University, Xianyang, 712100, Shaanxi, China

    Shiming Qi, Yuanbo Shen, Xinyu Wang, Shijie Zhang, Yushun Li, Md. Monirul Islam, Jin Wang, Pan Zhao & Yan Liang

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  1. Shiming Qi
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  2. Yuanbo Shen
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Contributions

SQ engaged in all the experimental processes, data analyses, and interpretation of the experimental results. YS, XW, SZ, YL, IMM, JW, and PZ were involved in the TSWV inoculation of F2 population and the resistance evaluation. YS, XW, SZ, and YL were involved in the analysis of the mapping populations. All authors participated in the discussions on the experimental designs and the result evaluations. SQ wrote the manuscripts. YL, FZ, and XZ conceptualized the research, designed the experiments, and received funding. All authors reviewed and approved the manuscript.

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Correspondence to Yan Liang.

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Communicated by Reem Aboukhaddour.

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Qi, S., Shen, Y., Wang, X. et al. A new NLR gene for resistance to Tomato spotted wilt virus in tomato (Solanum lycopersicum). Theor Appl Genet 135, 1493–1509 (2022). https://doi.org/10.1007/s00122-022-04049-4

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