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Glycine max NNL1 restricts symbiotic compatibility with widely distributed bradyrhizobia via root hair infection

A Publisher Correction to this article was published on 08 February 2021

This article has been updated


Symbiosis between soybean (Glycine max) and rhizobia is essential for efficient nitrogen fixation. Rhizobial effectors secreted through the type-III secretion system are key for mediating the interactions between plants and rhizobia, but the molecular mechanism remains largely unknown. Here, our genome-wide association study for nodule number identified G. max Nodule Number Locus 1 (GmNNL1), which encodes a new R protein. GmNNL1 directly interacts with the nodulation outer protein P (NopP) effector from Bradyrhizobium USDA110 to trigger immunity and inhibit nodulation through root hair infection. The insertion of a 179 bp short interspersed nuclear element (SINE)-like transposon into GmNNL1 leads to the loss of function of GmNNL1, enabling bradyrhizobia to successfully nodulate soybeans through the root hair infection route and enhancing nitrogen fixation. Our findings provide important insights into the coevolution of soybean–bradyrhizobia compatibility and offer a way to design new legume–rhizobia interactions for efficient symbiotic nitrogen fixation.

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Fig. 1: Natural variation of Glyma.02G076900.
Fig. 2: GmNNL1HT1 inhibits nodule formation in soybean.
Fig. 3: Crack infection is the main mode for B. diazoefficiens USDA110 invading roots of soybean accessions with GmNNL1HT1 to form nodules.
Fig. 4: GmNNL1HT1 recognizes NopP to inhibit nodulation.
Fig. 5: The evolution of GmNNL1 HTs and their compatibility with the natural variants of the bradyrhizobial effector protein NopP.
Fig. 6: The model for GmNNL1–NopP regulating nodulation in soybean.

Data availability

The gene-sequencing data of NopP and the 16S rRNA in Bradyrhizobium were uploaded to the NCBI website, and a list of the accession numbers is provided in Supplementary Table 5. VCF files for SNPs and indels for GWAS are available from the corresponding authors on request. The sequence of Glyma.02G076900 can be downloaded from the Soybase website ( The nucleotide or amino acid sequences of NopP in Bradyrhizobium species were retrieved from various databases (NCBI,; Rhizobase, Source data are provided with this paper.

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We thank H. Liao (Fujian University of Agriculture and Forestry Science and Technology) and J. Zhao (Anhui Agriculture University) for providing some accessions of soybeans for the GWAS experiments and evolution analysis; G. Stacey (University of Missouri) for providing GUS-tagged USDA110; H. Liao (Fujian University of Agriculture and Forestry Science and Technology) for providing A. rhizogenes K599; and X. Yao (Huazhong Agriculture University) for providing the GV3101 strain with the ER marker gene OFP-HDEL. This work was supported by grant 2016YFD0100700 of The National Key Research and Development Program of China (to B.Z. and Y.L.) and 2015CB910200 of The National Key Basic Research Foundation of China (to X.W.), grants 31870257, 91535104 and 31430046 of The National Natural Science Foundation of China (to X.W.), grant 31471522 of The National Natural Science Foundation of China (to M.Z.) and grant CARS-004-PS06 of China Agriculture Research System (to C.Y.).

Author information




X.W. and Y.L. conceived the study and managed the projects; B.Z., M.W., Z.Z., J.C., S.C., X.C., W.F., Y.P., K.T., S.W. and Hong Wang performed the GWAS experiments. X.W., B.Z., M.W., C.L. and L.Z. performed data analysis. B.Z., M.W., Y.P., Y.S., P.Z., H. Wu, Haijiao Wang, J.S., S.D., K.Q., M.H. and Y.W. performed the functional studies of the genes. B.Z., X.H., F.D., Q.S. and X.W. performed the gene evolution analysis. X.W., M.Z., C.Y., C.Q. and B.Z. collected most of the soybean accessions used for GWAS. B.Z., X.W. and Y.L. wrote and revised the article.

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Correspondence to Youguo Li or Xuelu Wang.

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Zhang, B., Wang, M., Sun, Y. et al. Glycine max NNL1 restricts symbiotic compatibility with widely distributed bradyrhizobia via root hair infection. Nat. Plants 7, 73–86 (2021).

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