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

Authors: ZHANG, BAO - Huazhong Agricultural University; WANG, MENGDI - Huazhong Agricultural University; SUN, YIFANG - Huazhong Agricultural University; ZHAO, PENG - Huazhong Agricultural University; LIU, CHANG - Huazhong Agricultural University; QING, KE - Huazhong Agricultural University; HU, XIAOTONG - Huazhong Agricultural University; ZHONG, ZHEDONG - Huazhong Agricultural University; CHENG, JIALONG - Huazhong Agricultural University; WANG, HAIJIAO - Henan University; PEMG, YAQI - Henan University; SHI, JIAJIA - Henan University; ZHUANG, LILI - Henan University; DU, SI - Huazhong Agricultural University; HE, MIAO - Huazhong Agricultural University; WU, HUI - Huazhong Agricultural University; LIU, MIN - Huazhong Agricultural University; CHEN, SHENGCAI - Huazhong Agricultural University; WANG, HONG - Huazhong Agricultural University; CHEN, XU - Huazhong Agricultural University; FAN, WEI - Huazhong Agricultural University; TIAN, KEWEI - Huazhong Agricultural University; WANG, YIN - Huazhong Agricultural University; CHEN, QIANG - Hebei Academy Of Agriculture; WANG, SHIXIANG - Huazhong Agricultural University; DONG, FAMING - Hebei Academy Of Agriculture; YANG, CHUNYAN - Hebei Academy Of Agriculture; ZHANG, MENGCHEN - Hebei Academy Of Agriculture; Song, Qijian; LI, YOUGUO - Huazhong Agricultural University; WANG, XUELU - Henan Agricultural University

Submitted to: Nature Plants
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/8/2020
Publication Date: 1/15/2021
Citation: Zhang, B., Wang, M., Sun, Y., Zhao, P., Liu, C., Qing, K., Hu, X., Zhong, Z., Cheng, J., Wang, H., Pemg, Y., Shi, J., Zhuang, L., Du, S., He, M., Wu, H., Liu, M., Chen, S., Wang, H., Chen, X., Fan, W., Tian, K., Wang, Y., Chen, Q., Wang, S., Dong, F., Yang, C., Zhang, M., Song, Q., Li, Y., Wang, X. 2021. Glycine max NNL1 restricts symbiotic compatibility with widely distributed bradyrhizobia via root hair infection. Nature Plants. 7:73-86. https://doi.org/10.1038/s41477-020-00832-7.
DOI: https://doi.org/10.1038/s41477-020-00832-7

Interpretive Summary: Nitrogen is the most critical nutrient requirement for crop production. Legume crops like soybean can derive most, if not all, of the nitrogen required for optimal growth and yield by establishing a symbiosis with nitrogen-fixing bacteria known as rhizobia. Despite the knowledge of how rhizobia establish connections to form symbiotic root nodules in plants, scientists still do not know why this is possible. In this study, we analyzed the DNA genomes of soybean and found a gene, GmNNL1, that is responsible for the numbers of root nodules formed by rhizobia. The analysis revealed that soybeans containing a natural mutation in this gene by insertion of a transposable element makes GmNNL1 non-functional which allows for nodule formation. A non-mutated gene, however, triggers an immune response upon symbiosis which then limits nodulation numbers. These findings will be useful to soybean scientists and breeders at government agencies, universities, and private institutes who want to improve soybean-rhizobium symbiosis to provide for efficient soybean cultivation with less topical fertilizer application.

Technical Abstract: Symbiosis between soybean (Glycine max) and rhizobia is essential for efficient nitrogen fixation. Rhizobial effectors secreted via the type III secretion system are key to mediate the plant -rhizobia interaction, but the molecular mechanism remains largely unknown. Our genome-wide association study for nodule number identified Nodule Number Locus 1 (GmNNL1), encoding a novel R protein. GmNNL1 directly interacts with the nodulation outer protein P effector from Bradyrhizobium USDA110 to trigger immunity and inhibit nodulation through root hair infection. The insertion of a 179-bp SINE-like transposon into GmNNL1 leads to the loss of function of GmNNL1, allowing bradyrhizobia to successfully nodulate soybeans through the root hair infection route and enhancing nitrogen fixation. Our findings provide important insight into the co-evolution of soybean-bradyrhizobia compatibility and offer a new way to design novel legume -rhizobia interactions for efficient symbiotic nitrogen fixation.