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GmSABP2-1 encodes methyl salicylate esterase and functions in soybean defense against soybean cyst nematode

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Abstract

Key message

The soybean gene GmSABP2-1 encodes methyl salicylate esterase and its overexpression led to significant reduction in development of pathogenic soybean cyst nematode.

Abstract

Soybean cyst nematode (SCN, Heterodera glycines) is one of the most devastating pests of soybean (Glycine max L. Merr.). In searching for SCN-defense genes, a soybean gene of the methylesterase (MES) family was found to be upregulated in an SCN-resistant soybean line and downregulated in an SCN-susceptible line upon SCN infection. This gene was designated as GmSABP2-1. Here, we report on biochemical and overexpression studies of GmSABP2-1 to examine its possible function in SCN resistance. The protein encoded by GmSABP2-1 is closely related to known methyl salicylate esterases. To determine the biochemical function of GmSABP2-1, a full-length cDNA of GmSABP2-1 was cloned into a protein expression vector and expressed in Escherichia coli. The resulting recombinant GmSABP2-1 was demonstrated to catalyze the demethylation of methyl salicylate. The biochemical properties of GmSABP2-1 were determined. Its apparent Km value was 46.2 ± 2.2 μM for methyl salicylate, comparable to those of the known methyl salicylate esterases. To explore the biological significance of GmSABP2-1 in soybean defense against SCN, we first overexpressed GmSABP2-1 in transgenic hairy roots of an SCN-susceptible soybean line. When infected with SCN, GmSABP2-1-overexpressing hairy roots showed 84.5% reduction in the development of SCN beyond J2 stage. To provide further genetic evidence for the role of GmSABP2-1 in SCN resistance, stable transgenic soybean plants overexpressing GmSABP2-1 were produced. Analysis of the GmSABP2-1-overexpressing lines showed a significant reduction in SCN development compared to non-transgenic plants. In conclusion, we demonstrated that GmSABP2-1 encodes methyl salicylate esterase and functions as a resistance-related gene against SCN.

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Data availability

The data supporting the findings of this study are available within the article and its Supplementary Materials. GenBank accession of GmSABP2-1 is PP438656.

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Acknowledgements

The authors would like to thank Dr. Prakash R. Arelli, Dana Pekarchick and Susan Thomas (USDA-ARS, Jackson, TN) for assistance with maintaining the SCN cultures.

Funding

Tennessee Soybean Promotion Board grant to MM, TH, CNS, and FC. USDA Hatch funds to FC, VP, TH, and CNS.

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Author notes

  1. Jingyu Lin and Weijiao Wang have contributed equally to this work.

Authors and Affiliations

  1. Department of Plant Sciences, University of Tennessee, Knoxville, TN, USA

    Jingyu Lin, Weijiao Wang, Mitra Mazarei, Nan Zhao, Xinlu Chen, Vincent R. Pantalone, Tarek Hewezi, Charles Neal Stewart Jr & Feng Chen

  2. Center for Agricultural Synthetic Biology, University of Tennessee, Knoxville, TN, USA

    Mitra Mazarei & Charles Neal Stewart Jr

Authors
  1. Jingyu Lin
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  2. Weijiao Wang
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  5. Xinlu Chen
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  9. Feng Chen
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Contributions

FC, CNS, VP, TH, MM, and JL conceived and designed the research. JL, WW, MM, NZ, and XC performed the experiments. All authors contributed to data analysis and interpretation. JL, WW, and FC wrote the manuscript with inputs from all authors. All authors read and approved the final manuscript.

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Correspondence to Feng Chen.

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The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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Communicated by Baochun Li.

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Lin, J., Wang, W., Mazarei, M. et al. GmSABP2-1 encodes methyl salicylate esterase and functions in soybean defense against soybean cyst nematode. Plant Cell Rep 43, 138 (2024). https://doi.org/10.1007/s00299-024-03224-9

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