Paired Medicago receptors mediate broad-spectrum resistance to nodulation by Sinorhizobium meliloti carrying a species-specific gene

Authors: LIU, JINGE - University Of Kentucky; WANG, TING - Institute Of Biochemistry Of The Romanian Academy; QIN, QIULIN - University Of Kentucky; YU, XIAOCHENG - University Of Kentucky; Yang, Shengming; Dinkins, Randy; KUCZMOG, ANETT - University Of Pecs; PUTNOKY, PETER - University Of Pecs; MUSZYNSKI, ARTUR - University Of Georgia; GRIFFITTS, JOEL - Brigham Young University; KERESZT, ATTILA - Hungarian Academy Of Sciences; ZHU, HONGYAN - University Of Kentucky

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/9/2022
Publication Date: 12/12/2022
Citation: Liu, J., Wang, T., Qin, Q., Yu, X., Yang, S., Dinkins, R.D., Kuczmog, A., Putnoky, P., Muszynski, A., Griffitts, J., Kereszt, A., Zhu, H. 2022. Paired Medicago receptors mediate broad-spectrum resistance to nodulation by Sinorhizobium meliloti carrying a species-specific gene. Proceedings of the National Academy of Sciences (PNAS). 119(51). https://doi.org/10.1073/pnas.2214703119.
DOI: https://doi.org/10.1073/pnas.2214703119

Interpretive Summary: Rhizobia are soil-inhabiting bacteria that form specialized structures, called nodules, on the roots of legume plants. Within the nodules, rhizobia can convert atmospheric nitrogen into ammonia that can be utilized by legumes. This process is termed root nodule symbiosis, which enables legumes to meet their own nitrogen needs in nitrogen-poor soils. The legume-rhizobia symbiotic association is highly specific, such that each legume plant establishes a symbiosis with only a limited set of rhizobia strains and vice versa. However, the molecular mechanisms underlying symbiotic specificity are less understood. In this study we have cloned and characterized the NS1a and NS1b receptors in the legume Medicago truncatula that restrict nodulation by many rhizobia strains. We also cloned a bacterial gene that is required for receptors-mediated nodulation restriction. Therefore, our discovery reveals a previously undescribed mechanism regulating specificity in legume-rhizobia symbiosis, and it provides knowledge and gene targets for both plant geneticists and microbiologists to broaden the legume-rhizobia symbiosis spectrum.

Technical Abstract: Plants have evolved the ability to distinguish between symbiotic and pathogenic microbial signals. However, potentially cooperative plant-microbe interactions often abort due to incompatible signaling. The NS1 (Nodulation Specificity 1) locus in the legume Medicago truncatula blocks tissue invasion and root nodule induction by many strains of the nitrogen-fixing symbiont Sinorhizobium meliloti. Controlling this strain-specific nodulation blockade are two genes at the NS1 locus, designated NS1a and NS1b, which encode malectin-like leucine-rich repeat receptor kinases. Expression of NS1a and NS1b is induced upon inoculation by both compatible and incompatible Sinorhizobium strains and is dependent on host perception of bacterial nodulation (Nod) factors. Both presence/absence and sequence polymorphisms of the paired receptors contribute to the evolution and functional diversification of the NS1 locus. A bacterial gene, designated rns1, is required for activation of NS1-mediated nodulation restriction. rns1 encodes a type I-secreted protein and is present in approximately 50% of the nearly 250 sequenced S. meliloti strains but not found in over 60 sequenced strains from the closely related species Sinorhizobium medicae. S. meliloti strains lacking functional rns1 are able to evade NS1-mediated nodulation blockade.