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A Germin-Like Protein GLP1 of Legumes Mediates Symbiotic Nodulation by Interacting with an Outer Membrane Protein of Rhizobia

Rhizobia can infect legumes and induce the coordinated expression of symbiosis and defense genes for the establishment of mutualistic symbiosis. Numerous studies have elucidated the molecular interactions between rhizobia and host plants, which are associated with Nod factor, exopolysaccharide, and...

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Autores principales: Zeng, Xiaobo, Li, Dongzhi, Lv, Yanfei, Lu, Yao, Mei, Lingli, Zhou, Donglai, Chen, Dasong, Xie, Fuli, Lin, Hui, Li, Youguo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9927233/
https://www.ncbi.nlm.nih.gov/pubmed/36633436
http://dx.doi.org/10.1128/spectrum.03350-22
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author Zeng, Xiaobo
Li, Dongzhi
Lv, Yanfei
Lu, Yao
Mei, Lingli
Zhou, Donglai
Chen, Dasong
Xie, Fuli
Lin, Hui
Li, Youguo
author_facet Zeng, Xiaobo
Li, Dongzhi
Lv, Yanfei
Lu, Yao
Mei, Lingli
Zhou, Donglai
Chen, Dasong
Xie, Fuli
Lin, Hui
Li, Youguo
author_sort Zeng, Xiaobo
collection PubMed
description Rhizobia can infect legumes and induce the coordinated expression of symbiosis and defense genes for the establishment of mutualistic symbiosis. Numerous studies have elucidated the molecular interactions between rhizobia and host plants, which are associated with Nod factor, exopolysaccharide, and T3SS effector proteins. However, there have been relatively few reports about how the host plant recognizes the outer membrane proteins (OMPs) of rhizobia to mediate symbiotic nodulation. In our previous work, a gene (Mhopa22) encoding an OMP was identified in Mesorhizobium huakuii 7653R, whose homologous genes are widely distributed in Rhizobiales. In this study, a germin-like protein GLP1 interacting with Mhopa22 was identified in Astragalus sinicus. RNA interference of AsGLP1 resulted in a decrease in nodule number, whereas overexpression of AsGLP1 increased the number of nodules in the hairy roots of A. sinicus. Consistent symbiotic phenotypes were identified in Medicago truncatula with MtGLPx (refer to medtr7g111240.1, the isogeny of AsGLP1) overexpression or Tnt1 mutant (glpx-1) in symbiosis with Sinorhizobium meliloti 1021. The glpx-1 mutant displayed hyperinfection and the formation of more infection threads but a decrease in root nodules. RNA sequencing analysis showed that many differentially expressed genes were involved in hormone signaling and symbiosis. Taken together, AsGLP1 and its homology play an essential role in mediating the early symbiotic process through interacting with the OMPs of rhizobia. IMPORTANCE This study is the first report to characterize a legume host plant protein to sense and interact with an outer membrane protein (OMP) of rhizobia. It can be speculated that GLP1 plays an essential role to mediate early symbiotic process through interacting with OMPs of rhizobia. The results provide deeper understanding and novel insights into the molecular interactive mechanism of a legume symbiosis signaling pathway in recognition with rhizobial OMPs. Our findings may also provide a new perspective to improve the symbiotic compatibility and nodulation of legume.
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spelling pubmed-99272332023-02-15 A Germin-Like Protein GLP1 of Legumes Mediates Symbiotic Nodulation by Interacting with an Outer Membrane Protein of Rhizobia Zeng, Xiaobo Li, Dongzhi Lv, Yanfei Lu, Yao Mei, Lingli Zhou, Donglai Chen, Dasong Xie, Fuli Lin, Hui Li, Youguo Microbiol Spectr Research Article Rhizobia can infect legumes and induce the coordinated expression of symbiosis and defense genes for the establishment of mutualistic symbiosis. Numerous studies have elucidated the molecular interactions between rhizobia and host plants, which are associated with Nod factor, exopolysaccharide, and T3SS effector proteins. However, there have been relatively few reports about how the host plant recognizes the outer membrane proteins (OMPs) of rhizobia to mediate symbiotic nodulation. In our previous work, a gene (Mhopa22) encoding an OMP was identified in Mesorhizobium huakuii 7653R, whose homologous genes are widely distributed in Rhizobiales. In this study, a germin-like protein GLP1 interacting with Mhopa22 was identified in Astragalus sinicus. RNA interference of AsGLP1 resulted in a decrease in nodule number, whereas overexpression of AsGLP1 increased the number of nodules in the hairy roots of A. sinicus. Consistent symbiotic phenotypes were identified in Medicago truncatula with MtGLPx (refer to medtr7g111240.1, the isogeny of AsGLP1) overexpression or Tnt1 mutant (glpx-1) in symbiosis with Sinorhizobium meliloti 1021. The glpx-1 mutant displayed hyperinfection and the formation of more infection threads but a decrease in root nodules. RNA sequencing analysis showed that many differentially expressed genes were involved in hormone signaling and symbiosis. Taken together, AsGLP1 and its homology play an essential role in mediating the early symbiotic process through interacting with the OMPs of rhizobia. IMPORTANCE This study is the first report to characterize a legume host plant protein to sense and interact with an outer membrane protein (OMP) of rhizobia. It can be speculated that GLP1 plays an essential role to mediate early symbiotic process through interacting with OMPs of rhizobia. The results provide deeper understanding and novel insights into the molecular interactive mechanism of a legume symbiosis signaling pathway in recognition with rhizobial OMPs. Our findings may also provide a new perspective to improve the symbiotic compatibility and nodulation of legume. American Society for Microbiology 2023-01-12 /pmc/articles/PMC9927233/ /pubmed/36633436 http://dx.doi.org/10.1128/spectrum.03350-22 Text en Copyright © 2023 Zeng et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Zeng, Xiaobo
Li, Dongzhi
Lv, Yanfei
Lu, Yao
Mei, Lingli
Zhou, Donglai
Chen, Dasong
Xie, Fuli
Lin, Hui
Li, Youguo
A Germin-Like Protein GLP1 of Legumes Mediates Symbiotic Nodulation by Interacting with an Outer Membrane Protein of Rhizobia
title A Germin-Like Protein GLP1 of Legumes Mediates Symbiotic Nodulation by Interacting with an Outer Membrane Protein of Rhizobia
title_full A Germin-Like Protein GLP1 of Legumes Mediates Symbiotic Nodulation by Interacting with an Outer Membrane Protein of Rhizobia
title_fullStr A Germin-Like Protein GLP1 of Legumes Mediates Symbiotic Nodulation by Interacting with an Outer Membrane Protein of Rhizobia
title_full_unstemmed A Germin-Like Protein GLP1 of Legumes Mediates Symbiotic Nodulation by Interacting with an Outer Membrane Protein of Rhizobia
title_short A Germin-Like Protein GLP1 of Legumes Mediates Symbiotic Nodulation by Interacting with an Outer Membrane Protein of Rhizobia
title_sort germin-like protein glp1 of legumes mediates symbiotic nodulation by interacting with an outer membrane protein of rhizobia
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9927233/
https://www.ncbi.nlm.nih.gov/pubmed/36633436
http://dx.doi.org/10.1128/spectrum.03350-22
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