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New Insight into the Evolution of Symbiotic Genes in Black Locust-Associated Rhizobia.

ABSTRACT: Nitrogen fixation in legumes occurs via symbiosis with rhizobia. This process involves packages of symbiotic genes on mobile genetic elements that are readily transferred within or between rhizobial species, furnishing the recipient with the ability to interact with plant hosts. However, it remains elusive whether plant host migration has played a role in shaping the current distribution of genetic variation in symbiotic genes. Herein, we examined the genetic structure and phylogeographic pattern of symbiotic genes in 286 symbiotic strains of Mesorhizobium nodulating black locust (Robinia pseudoacacia), a cross-continental invasive legume species that is native to North America. We conducted detailed phylogeographic analysis and approximate Bayesian computation to unravel the complex demographic history of five key symbiotic genes. The sequencing results indicate an origin of symbiotic genes in Germany rather than North America. Our findings provide strong evidence of prehistoric lineage splitting and spatial expansion events resulting in multiple radiations of descendent clones from founding sequence types worldwide. Estimates of the timescale of divergence in North American and Chinese subclades suggest that black locust-specific symbiotic genes have been present in these continent many thousands of years before recent migration of plant host. Although numerous crop plants, including legumes, have found their centers of origin as centers of evolution and diversity, the number of legume-specific symbiotic genes with a known geographic origin is limited. This work sheds light on the coevolution of legumes and rhizobia.

SUBMITTER: Liu Z

PROVIDER: S-EPMC6698633 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Ethylene plays an important role in regulating the rhizobial nodulation process. Consequently, numerous strains of rhizobia possess the ability to decrease plant ethylene levels by the expression of the enzyme 1-aminocyclopropane-1-carboxylate (ACC) deaminase or via the production of rhizobitoxine, thus, leading to an increased ability to nodulate leguminous plants. Nevertheless, not much is understood about the prevalence of these ethylene modulation genes in different rhizobial groups nor their role in the evolution of the symbiotic process. In this work, we analyze the prevalence and evolution of the enzymes ACC deaminase (AcdS) and dihydrorhizobitoxine desaturase (RtxC) in 395 NodC+ genomes from different rhizobial strains isolated from a wide range of locations and plant hosts, and discuss their importance in the evolution of the symbiotic process. The obtained results show that AcdS and RtxC are differentially prevalent in rhizobial groups, indicating the existence of several selection mechanisms governed by the rhizobial strain itself and its evolutionary origin, the environment, and, importantly, the leguminous plant host (co-evolution). Moreover, it was found that the prevalence of AcdS and RtxC is increased in Bradyrhizobium and Paraburkholderia, and lower in other groups. Data obtained from phylogenetic, evolutionary as well as gene localization analysis support the previous hypotheses regarding the ancient origin of the nodulation abilities in Bradyrhizobium and Paraburkholderia, and brings a new perspective for the importance of ethylene modulation genes in the development of the symbiotic process. The acquisition of AcdS by horizontal gene transfer and a positive selection in other rhizobial groups indicates that this enzyme plays an important role in the nodulation process of many rhizobia. On the other hand, RtxC is negatively selected in most symbioses. Understanding the evolution of ethylene modulation genes in rhizobia may be the key to the development of new strategies aiming for an increased nodulation and nitrogen fixation process.

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New Insight into the Evolution of Symbiotic Genes in Black Locust-Associated Rhizobia.

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