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

Jinge Liu; Ting Wang; Qiulin Qin; Xiaocheng Yu; Shengming Yang; Randy D. Dinkins; Anett Kuczmog; Péter Putnoky; Artur Muszyński; Joel S. Griffitts; Attila Kereszt; Hongyan Zhu

doi:10.1073/pnas.2214703119

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

Jinge Liu, Ting Wang, Qiulin Qin, Xiaocheng Yu, Shengming Yang, Randy D. Dinkins, Anett Kuczmog, Péter Putnoky, Artur Muszyński, Joel S. Griffitts, Attila Kereszt, Hongyan Zhu

Plant and Soil Sciences

Research output: Contribution to journal › Article › peer-review

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 Nodulation Specificity 1 (NS1) 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.

Original language	English
Article number	e2214703119
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	119
Issue number	51
DOIs	https://doi.org/10.1073/pnas.2214703119
State	Published - Dec 20 2022

Bibliographical note

Funding Information:
We thank E. Kondorosi for helpful comments on the manuscript; and P. Tiffin (University of Minnesota), B. Scharf (Virginia Polytechnic Institute and State University), and A. Mengoni (University of Florence, Italy) for providing the rhizobial strains. This work was supported by US Department of Agriculture/National Institute of Food and Agriculture Grant 2014-67013-21573 (to H.Z.), US National Science Foundation Grant IOS-1758037 (to H.Z. and A.M.), US Department of Agriculture/Agricultural Research Service Non-Assistance Cooperative Agreement Grant 5850428003 (to H.Z.), Hungarian National Research, Development and Innovation Office Grants K128486 and K134841 (to A. Kereszt), and China Scholarship Council (to T.W.).

Funding Information:
ACKNOWLEDGMENTS. We thank E. Kondorosi for helpful comments on the manuscript; and P.Tiffin (University of Minnesota),B.Scharf (Virginia Polytechnic Institute and State University), and A. Mengoni (University of Florence, Italy) for providing the rhizobial strains. This work was supported by US Department of Agriculture/National Institute of Food and Agriculture Grant 2014-67013-21573 (to H.Z.), US National Science Foundation Grant IOS-1758037 (to H.Z. and A.M.), US Department of Agriculture/Agricultural Research Service Non-Assistance Cooperative Agreement Grant 5850428003 (to H.Z.), Hungarian National Research, Development and Innovation Office Grants K128486 and K134841 (to A. Kereszt), and China Scholarship Council (to T.W.).

Publisher Copyright:
Copyright © 2022 the Author(s). Published by PNAS.

Keywords

Medicago
nodulation
receptors
specificity
symbiosis

ASJC Scopus subject areas

General

Access to Document

10.1073/pnas.2214703119

Cite this

Liu, J., Wang, T., Qin, Q., Yu, X., Yang, S., Dinkins, R. D., Kuczmog, A., Putnoky, P., Muszyński, A., Griffitts, J. S., 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 of the United States of America, 119(51), [e2214703119]. https://doi.org/10.1073/pnas.2214703119

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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 Nodulation Specificity 1 (NS1) 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.",

keywords = "Medicago, nodulation, receptors, specificity, symbiosis",

author = "Jinge Liu and Ting Wang and Qiulin Qin and Xiaocheng Yu and Shengming Yang and Dinkins, {Randy D.} and Anett Kuczmog and P{\'e}ter Putnoky and Artur Muszy{\'n}ski and Griffitts, {Joel S.} and Attila Kereszt and Hongyan Zhu",

note = "Funding Information: We thank E. Kondorosi for helpful comments on the manuscript; and P. Tiffin (University of Minnesota), B. Scharf (Virginia Polytechnic Institute and State University), and A. Mengoni (University of Florence, Italy) for providing the rhizobial strains. This work was supported by US Department of Agriculture/National Institute of Food and Agriculture Grant 2014-67013-21573 (to H.Z.), US National Science Foundation Grant IOS-1758037 (to H.Z. and A.M.), US Department of Agriculture/Agricultural Research Service Non-Assistance Cooperative Agreement Grant 5850428003 (to H.Z.), Hungarian National Research, Development and Innovation Office Grants K128486 and K134841 (to A. Kereszt), and China Scholarship Council (to T.W.). Funding Information: ACKNOWLEDGMENTS. We thank E. Kondorosi for helpful comments on the manuscript; and P.Tiffin (University of Minnesota),B.Scharf (Virginia Polytechnic Institute and State University), and A. Mengoni (University of Florence, Italy) for providing the rhizobial strains. This work was supported by US Department of Agriculture/National Institute of Food and Agriculture Grant 2014-67013-21573 (to H.Z.), US National Science Foundation Grant IOS-1758037 (to H.Z. and A.M.), US Department of Agriculture/Agricultural Research Service Non-Assistance Cooperative Agreement Grant 5850428003 (to H.Z.), Hungarian National Research, Development and Innovation Office Grants K128486 and K134841 (to A. Kereszt), and China Scholarship Council (to T.W.). Publisher Copyright: Copyright {\textcopyright} 2022 the Author(s). Published by PNAS.",

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Liu, J, Wang, T, Qin, Q, Yu, X, Yang, S, Dinkins, RD, Kuczmog, A, Putnoky, P, Muszyński, A, Griffitts, JS, 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 of the United States of America, vol. 119, no. 51, e2214703119. https://doi.org/10.1073/pnas.2214703119

Paired Medicago receptors mediate broad-spectrum resistance to nodulation by Sinorhizobium meliloti carrying a species-specific gene. / Liu, Jinge; Wang, Ting; Qin, Qiulin et al.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 119, No. 51, e2214703119, 20.12.2022.

Research output: Contribution to journal › Article › peer-review

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AU - Liu, Jinge

AU - Wang, Ting

AU - Qin, Qiulin

AU - Yu, Xiaocheng

AU - Yang, Shengming

AU - Dinkins, Randy D.

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AU - Kereszt, Attila

AU - Zhu, Hongyan

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PY - 2022/12/20

Y1 - 2022/12/20

N2 - 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 Nodulation Specificity 1 (NS1) 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.

AB - 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 Nodulation Specificity 1 (NS1) 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.

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

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