1. Experimental-Evolution-Driven Identification of Arabidopsis Rhizosphere Competence Genes in Pseudomonas protegens
- Author
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Li, Erqin, Zhang, Hao, Jiang, Henan, Pieterse, Corné M J, Jousset, Alexandre, Bakker, Peter A H M, de Jonge, Ronnie, Sub Plant-Microbe Interactions, Sub Ecology and Biodiversity, Plant Microbe Interactions, Ecology and Biodiversity, Sub Plant-Microbe Interactions, Sub Ecology and Biodiversity, Plant Microbe Interactions, and Ecology and Biodiversity more...
- Subjects
Siderophore ,Arabidopsis ,Microbial genomics ,Beneficial microorganisms ,Computational biology ,Plant Roots ,Microbiology ,03 medical and health sciences ,Pseudomonas protegens ,500 Naturwissenschaften und Mathematik::580 Pflanzen (Botanik)::580 Pflanzen (Botanik) ,Pseudomonas ,Virology ,Arabidopsis thaliana ,Evolutionary dynamics ,Soil Microbiology ,030304 developmental biology ,0303 health sciences ,Rhizosphere ,Experimental evolution ,biology ,030306 microbiology ,fungi ,food and beverages ,biology.organism_classification ,QR1-502 ,Genes, Bacterial ,Mutation ,Rhizosphere-inhabiting microbes ,Directed Molecular Evolution ,Adaptation ,Genome, Bacterial ,Research Article - Abstract
Beneficial plant root-associated microorganisms carry out a range of functions that are essential for plant performance. Establishment of a bacterium on plant roots, however, requires overcoming several challenges, including competition with neighboring microorganisms and host immunity. Forward and reverse genetics have led to the identification of mechanisms that are used by beneficial microorganisms to overcome these challenges, such as the production of iron-chelating compounds, the formation of strong biofilms, or the concealment of characteristic microbial molecular patterns that trigger the host immune system. However, how such mechanisms arose from an evolutionary perspective is much less understood. To study bacterial adaptation in the rhizosphere, we employed experimental evolution to track the physiological and genetic dynamics of root-dwelling Pseudomonas protegens in the Arabidopsis thaliana rhizosphere under axenic conditions. This simplified binary one plant/one bacterium system allows for the amplification of key adaptive mechanisms for bacterial rhizosphere colonization. We identified 35 mutations, including single-nucleotide polymorphisms, insertions, and deletions, distributed over 28 genes. We found that mutations in genes encoding global regulators and in genes for siderophore production, cell surface decoration, attachment, and motility accumulated in parallel, underlining the finding that bacterial adaptation to the rhizosphere follows multiple strategies. Notably, we observed that motility increased in parallel across multiple independent evolutionary lines. All together, these results underscore the strength of experimental evolution in identifying key genes, pathways, and processes for bacterial rhizosphere colonization and a methodology for the development of elite beneficial microorganisms with enhanced root-colonizing capacities that can support sustainable agriculture in the future. IMPORTANCE Beneficial root-associated microorganisms carry out many functions that are essential for plant performance. Establishment of a bacterium on plant roots, however, requires overcoming many challenges. Previously, diverse mechanisms that are used by beneficial microorganisms to overcome these challenges were identified. However, how such mechanisms have developed from an evolutionary perspective is much less understood. Here, we employed experimental evolution to track the evolutionary dynamics of a root-dwelling pseudomonad on the root of Arabidopsis. We found that mutations in global regulators, as well as in genes for siderophore production, cell surface decoration, attachment, and motility, accumulate in parallel, emphasizing these strategies for bacterial adaptation to the rhizosphere. We identified 35 mutations distributed over 28 genes. All together, our results demonstrate the power of experimental evolution in identifying key pathways for rhizosphere colonization and a methodology for the development of elite beneficial microorganisms that can support sustainable agriculture. more...
- Published
- 2021
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