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Enhanced resistance to soybean cyst nematode in transgenic soybean via host-induced silencing of vital Heterodera glycines genes

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Abstract

Soybean cyst nematode (SCN, Heterodera glycines Ichinohe) is the most economically damaging pathogen affecting soybean production worldwide. Host-induced gene silencing provides a promising approach to confer resistance to plant parasitic nematodes. In the present study, we produced stable transgenic soybean plants individually harboring the inverted repeats of three essential H. glycines genes, Hg-rps23, Hg-snb1, and Hg-cpn1, and evaluated their resistance to SCN infection. Molecular characterization confirmed the stable integration of the hairpin double stranded (ds) RNA in host plants. Inoculation assays with SCN race 3 showed significant reduction of female index (FI, 11.84 ~ 17.47%) on the roots of T4 transgenic plants, with 73.29 ~ 81.90% reduction for the three RNA interference (RNAi) constructs, compared to non-transformed plants (NT, 65.43%). Enhanced resistance to SCN race 3 was further confirmed in subsequent generations (T5) of transgenic soybean. Moreover, when inoculated with SCN race 4 which was considered highly virulent to most of soybean germplasms and varieties, transgenic soybean plants also exhibited reduced FIs (9.96 ~ 23.67%) and increased resistance, relative to the NT plants (46.46%). Consistently, significant down-regulation in transcript levels of the Hg-rps23, Hg-snb1, Hg-cpn1 genes were observed in the nematodes feeding on the transgenic roots, suggesting a broad-spectrum resistance mediated by the host-mediated silencing of vital H. glycines genes. There were no significant differences in morphological traits between transgenic and NT soybean plants under conditions with negligible SCN infection. In summary, our results demonstrate the effectiveness of host-induced silencing of essential H. glycines genes to enhance broad-spectrum SCN resistance in stable transgenic soybean plants, without negative consequences on the agronomic performance.

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Acknowledgements

This research was supported by grants from Jilin Provincial Agricultural Science & Technology Innovation Project (KYJF2021ZR021, CXGC2021TD015), National Natural Science Foundation of China (31701448) and China National Novel Transgenic Organisms Breeding Project (2016ZX08004-004). We thank Editage (www.editage.cn) for English language editing.

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  1. Yuanyu Zhang, Qianqian Zhao and Jinhua Zhang equally contributed to this article.

Authors and Affiliations

  1. Jilin Provincial Key Laboratory of Agricultural Biotechnology, Jilin Academy of Agricultural Sciences, Changchun, 130033, China

    Yuanyu Zhang, Qianqian Zhao, Jinhua Zhang, Lu Niu, Jing Yang, Xiaomei Liu, Guojie Xing, Xiaofang Zhong & Xiangdong Yang

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  1. Yuanyu Zhang
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  2. Qianqian Zhao
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Contributions

YX and ZX designed the experiments. ZY and ZQ conducted on molecular experiments and drafted the manuscript. NL, XG, and YJ conducted on Agrobacterium-mediated transformation. ZJ and LX conducted on SCN inoculation bioassay. All authors participated in the manuscript revision.

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Correspondence to Xiaofang Zhong or Xiangdong Yang.

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Zhang, Y., Zhao, Q., Zhang, J. et al. Enhanced resistance to soybean cyst nematode in transgenic soybean via host-induced silencing of vital Heterodera glycines genes. Transgenic Res 31, 239–248 (2022). https://doi.org/10.1007/s11248-022-00298-7

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