Lineage-Specific Rewiring of Core Pathways Predating Innovation of Legume Nodules Shapes Symbiotic Efficiency

ABSTRACT The interkingdom coevolution innovated the rhizobium-legume symbiosis. The application of this nitrogen-fixing system in sustainable agriculture is usually impeded by incompatible interactions between partners. However, the progressive evolution of rhizobium-legume compatibility remains elu...

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Autores principales:	Wen-Jing Cui, Biliang Zhang, Ran Zhao, Li-Xue Liu, Jian Jiao, Ziding Zhang, Chang-Fu Tian
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	adaptation immunity mutualism pangenome legume Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/974b4734ae2c49b2b6cb1d141f4de7e4
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spelling	oai:doaj.org-article:974b4734ae2c49b2b6cb1d141f4de7e42021-12-02T19:36:40ZLineage-Specific Rewiring of Core Pathways Predating Innovation of Legume Nodules Shapes Symbiotic Efficiency10.1128/mSystems.01299-202379-5077https://doaj.org/article/974b4734ae2c49b2b6cb1d141f4de7e42021-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.01299-20https://doaj.org/toc/2379-5077ABSTRACT The interkingdom coevolution innovated the rhizobium-legume symbiosis. The application of this nitrogen-fixing system in sustainable agriculture is usually impeded by incompatible interactions between partners. However, the progressive evolution of rhizobium-legume compatibility remains elusive. In this work, deletions of rhcV encoding a structural component of the type three secretion system allow related Sinorhizobium strains to nodulate a previously incompatible soybean cultivar (Glycine max). These rhcV mutants show low to medium to high symbiotic efficiency on the same cultivated soybean while being indistinguishable on wild soybean plants (Glycine soja). The dual pantranscriptomics reveals nodule-specific activation of core symbiosis genes of Sinorhizobium and Glycine genes associated with genome duplication events along the chronogram. Unexpectedly, symbiotic efficiency is in line with lineage-dependent transcriptional profiles of core pathways which predate the diversification of Fabaceae and Sinorhizobium. This is supported by further physiological and biochemical experiments. Particularly, low-efficiency nodules show disordered antioxidant activity and low-energy status, which restrict nitrogen fixation activity. Collectively, the ancient core pathways play a crucial role in optimizing the function of later-evolved mutualistic arsenals in the rhizobium-legume coevolution. IMPORTANCE Significant roles of complex extracellular microbiota in environmental adaptation of eukaryotes in ever-changing circumstances have been revealed. Given the intracellular infection ability, facultative endosymbionts can be considered pioneers within complex extracellular microbiota and are ideal organisms for understanding the early stage of interkingdom adaptation. This work reveals that the later innovation of key symbiotic arsenals and the lineage-specific network rewiring in ancient core pathways, predating the divergence of legumes and rhizobia, underline the progressive evolution of rhizobium-legume compatibility. This insight not only is significant for improving the application benefits of rhizobial inoculants in sustainable agriculture but also advances our general understanding of the interkingdom coevolution which is theoretically explored by all host-microbiota interactions.Wen-Jing CuiBiliang ZhangRan ZhaoLi-Xue LiuJian JiaoZiding ZhangChang-Fu TianAmerican Society for MicrobiologyarticleadaptationimmunitymutualismpangenomelegumeMicrobiologyQR1-502ENmSystems, Vol 6, Iss 2 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	adaptation immunity mutualism pangenome legume Microbiology QR1-502
spellingShingle	adaptation immunity mutualism pangenome legume Microbiology QR1-502 Wen-Jing Cui Biliang Zhang Ran Zhao Li-Xue Liu Jian Jiao Ziding Zhang Chang-Fu Tian Lineage-Specific Rewiring of Core Pathways Predating Innovation of Legume Nodules Shapes Symbiotic Efficiency
description	ABSTRACT The interkingdom coevolution innovated the rhizobium-legume symbiosis. The application of this nitrogen-fixing system in sustainable agriculture is usually impeded by incompatible interactions between partners. However, the progressive evolution of rhizobium-legume compatibility remains elusive. In this work, deletions of rhcV encoding a structural component of the type three secretion system allow related Sinorhizobium strains to nodulate a previously incompatible soybean cultivar (Glycine max). These rhcV mutants show low to medium to high symbiotic efficiency on the same cultivated soybean while being indistinguishable on wild soybean plants (Glycine soja). The dual pantranscriptomics reveals nodule-specific activation of core symbiosis genes of Sinorhizobium and Glycine genes associated with genome duplication events along the chronogram. Unexpectedly, symbiotic efficiency is in line with lineage-dependent transcriptional profiles of core pathways which predate the diversification of Fabaceae and Sinorhizobium. This is supported by further physiological and biochemical experiments. Particularly, low-efficiency nodules show disordered antioxidant activity and low-energy status, which restrict nitrogen fixation activity. Collectively, the ancient core pathways play a crucial role in optimizing the function of later-evolved mutualistic arsenals in the rhizobium-legume coevolution. IMPORTANCE Significant roles of complex extracellular microbiota in environmental adaptation of eukaryotes in ever-changing circumstances have been revealed. Given the intracellular infection ability, facultative endosymbionts can be considered pioneers within complex extracellular microbiota and are ideal organisms for understanding the early stage of interkingdom adaptation. This work reveals that the later innovation of key symbiotic arsenals and the lineage-specific network rewiring in ancient core pathways, predating the divergence of legumes and rhizobia, underline the progressive evolution of rhizobium-legume compatibility. This insight not only is significant for improving the application benefits of rhizobial inoculants in sustainable agriculture but also advances our general understanding of the interkingdom coevolution which is theoretically explored by all host-microbiota interactions.
format	article
author	Wen-Jing Cui Biliang Zhang Ran Zhao Li-Xue Liu Jian Jiao Ziding Zhang Chang-Fu Tian
author_facet	Wen-Jing Cui Biliang Zhang Ran Zhao Li-Xue Liu Jian Jiao Ziding Zhang Chang-Fu Tian
author_sort	Wen-Jing Cui
title	Lineage-Specific Rewiring of Core Pathways Predating Innovation of Legume Nodules Shapes Symbiotic Efficiency
title_short	Lineage-Specific Rewiring of Core Pathways Predating Innovation of Legume Nodules Shapes Symbiotic Efficiency
title_full	Lineage-Specific Rewiring of Core Pathways Predating Innovation of Legume Nodules Shapes Symbiotic Efficiency
title_fullStr	Lineage-Specific Rewiring of Core Pathways Predating Innovation of Legume Nodules Shapes Symbiotic Efficiency
title_full_unstemmed	Lineage-Specific Rewiring of Core Pathways Predating Innovation of Legume Nodules Shapes Symbiotic Efficiency
title_sort	lineage-specific rewiring of core pathways predating innovation of legume nodules shapes symbiotic efficiency
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/974b4734ae2c49b2b6cb1d141f4de7e4
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Lineage-Specific Rewiring of Core Pathways Predating Innovation of Legume Nodules Shapes Symbiotic Efficiency

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