A Select and Resequence Approach Reveals Strain-Specific Effects of <i>Medicago</i> Nodule-Specific PLAT-Domain Genes

Burghardt, Liana T.; Trujillo, Diana; Epstein, Brendan; Tiffin, Peter; Young, Nevin D.

doi:10.1104/pp.19.00831

Cited by 14 publications

(16 citation statements)

References 33 publications

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“…By continuing the evolution experiment and its genetic analysis, future work should address the evolution of late stages of symbiosis, such as the acquisition of persistence, nitrogen fixation and mutualism and should provide a better understanding of these poorly known symbiotic stages. EE including a single selection cycle also proved to be very useful in understanding the bacterial genetic bases of incompatible symbiotic interactions [47,166,167] and to analyze plant-mediated selection acting on rhizobial communities [168,169]. Complementary to synthetic biology and classical genetic approaches, EE will undoubtedly become an indispensable tool to select efficient, host-adapted microsymbionts in the perspective of optimizing current symbiotic associations or transferring N 2 -fixation in crops [170,171].…”

Section: Discussionmentioning

confidence: 99%

Experimental Evolution of Legume Symbionts: What Have We Learnt?

Moura

Remigi

Masson‐Boivin

et al. 2020

Genes

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Rhizobia, the nitrogen-fixing symbionts of legumes, are polyphyletic bacteria distributed in many alpha- and beta-proteobacterial genera. They likely emerged and diversified through independent horizontal transfers of key symbiotic genes. To replay the evolution of a new rhizobium genus under laboratory conditions, the symbiotic plasmid of Cupriavidus taiwanensis was introduced in the plant pathogen Ralstonia solanacearum, and the generated proto-rhizobium was submitted to repeated inoculations to the C. taiwanensis host, Mimosa pudica L. This experiment validated a two-step evolutionary scenario of key symbiotic gene acquisition followed by genome remodeling under plant selection. Nodulation and nodule cell infection were obtained and optimized mainly via the rewiring of regulatory circuits of the recipient bacterium. Symbiotic adaptation was shown to be accelerated by the activity of a mutagenesis cassette conserved in most rhizobia. Investigating mutated genes led us to identify new components of R. solanacearum virulence and C. taiwanensis symbiosis. Nitrogen fixation was not acquired in our short experiment. However, we showed that post-infection sanctions allowed the increase in frequency of nitrogen-fixing variants among a non-fixing population in the M. pudica–C. taiwanensis system and likely allowed the spread of this trait in natura. Experimental evolution thus provided new insights into rhizobium biology and evolution.

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Section: Discussionmentioning

confidence: 99%

Experimental Evolution of Legume Symbionts: What Have We Learnt?

Moura

Remigi

Masson‐Boivin

et al. 2020

Genes

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“…More recently, greenhouse studies have directly demonstrated the influence of GxG interactions on the fitness of both the plant and rhizobium partners (28)(29)(30)(31). The newly developed select-and-resequence approach is providing a high-throughput approach to uncover the genetic basis underlying GxG interactions for fitness in rhizobium-legume symbioses as well as a way to screen for strain-specific effects of individual genes (32,33). To date, GxG interaction studies have largely focused on measurements of fitness as a holistic measure of the entire symbiotic process.…”

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confidence: 99%

Nonadditive Transcriptomic Signatures of Genotype-by-Genotype Interactions during the Initiation of Plant-Rhizobium Symbiosis

et al. 2021

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Rhizobia are ecologically important, facultative plant-symbiotic microbes. In nature, there is a large variability in the association of rhizobial strains and host plants of the same species. Here, we evaluated whether plant and rhizobial genotypes influence the initial transcriptional response of rhizobium following perception of a host plant. RNA sequencing of the model rhizobium Sinorhizobium meliloti exposed to root exudates or luteolin (an inducer of nod genes, involved in the early steps of symbiotic interaction) was performed on a combination of three S. meliloti strains and three alfalfa varieties as host plants. The response to root exudates involved hundreds of changes in the rhizobium transcriptome. Of the differentially expressed genes, 35% were influenced by the strain genotype, 16% were influenced by the plant genotype, and 29% were influenced by strain-by-host plant genotype interactions. We also examined the response of a hybrid S. meliloti strain in which the symbiotic megaplasmid (∼20% of the genome) was mobilized between two of the above-mentioned strains. Dozens of genes were upregulated in the hybrid strain, indicative of nonadditive variation in the transcriptome. In conclusion, this study demonstrated that transcriptional responses of rhizobia upon perception of legumes are influenced by the genotypes of both symbiotic partners and their interaction, suggesting a wide spectrum of genetic determinants involved in the phenotypic variation of plant-rhizobium symbiosis. IMPORTANCE A sustainable way for meeting the need of an increased global food demand should be based on a holobiont perspective, viewing crop plants as intimately associated with their microbiome, which helps improve plant nutrition, tolerance to pests, and adverse climate conditions. However, the genetic repertoire needed for efficient association with plants by the microbial symbionts is still poorly understood. The rhizobia are an exemplary model of facultative plant symbiotic microbes. Here, we evaluated whether genotype-by-genotype interactions could be identified in the initial transcriptional response of rhizobium perception of a host plant. We performed an RNA sequencing study to analyze the transcriptomes of different rhizobial strains elicited by root exudates of three alfalfa varieties as a proxy of an early step of the symbiotic interaction. The results indicated strain- and plant variety-dependent variability in the observed transcriptional changes, providing fundamentally novel insights into the genetic basis of rhizobium-plant interactions. Our results provide genetic insights and perspective to aid in the exploitation of natural rhizobium variation for improvement of legume growth in agricultural ecosystems.

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“…However, most of the studies involved model strains and plants and their respective mutants, with only a limited evaluation of the genetic bases of the somewhat large phenotypic variation in the symbiotic phenotype due to natural genotype variation. Early studies in the alfalfa rhizobial symbiont Sinorhizobium meliloti showed that plant variety exerts a detectable effect on the recruitment of native soil rhizobial population (Carelli et al, 2000;Paffetti et al, s.d.). Clearly, the fitness advantage of the symbiosis (Burghardt, 2020) is influenced by GxG interactions between the two (or more) partners (Heath, 2008).…”

Section: The Role Of Genotype X Genotype Interactions In Shaping the Symbiotic Partnershipmentioning

confidence: 99%

Legume tasters: symbiotic rhizobia host preference and smart inoculant formulations

Cangioli

Checcucci

Mengoni

et al. 2021

BioComm

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Mutualistic interactions have great importance in ecology, with genetic information that takes shape through interactions within the symbiotic partners and between the partners and the environment. It is known that variation of the host-associated microbiome contributes to buffer adaptation challenges of the host’s physiology when facing varying environmental conditions. In agriculture, pivotal examples are symbiotic nitrogen-fixing rhizobia, known to contribute greatly to host (legume plants) adaptation and host productivity. A holistic view of increasing crop yield and resistance to biotic and abiotic stresses is that of microbiome engineering, the exploitation of a host-associated microbiome through its rationally designed manipulation with synthetic microbial communities. However, several studies highlighted that the expression of the desired phenotype in the host resides in species-specific, even genotype-specific interactions between the symbiotic partners. Consequently, there is a need to dissect such an intimate level of interaction, aiming to identify the main genetic components in both partners playing a role in symbiotic differences/host preferences. In the present paper, while briefly reviewing the knowledge and the challenges in plant–microbe interaction and rhizobial studies, we aim to promote research on genotype x genotype interaction between rhizobia and host plants for a rational design of synthetic symbiotic nitrogen-fixing microbial communities to be used for sustainably improving leguminous plants yield.

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A Select and Resequence Approach Reveals Strain-Specific Effects of Medicago Nodule-Specific PLAT-Domain Genes

Cited by 14 publications

References 33 publications

Experimental Evolution of Legume Symbionts: What Have We Learnt?

Experimental Evolution of Legume Symbionts: What Have We Learnt?

Nonadditive Transcriptomic Signatures of Genotype-by-Genotype Interactions during the Initiation of Plant-Rhizobium Symbiosis

Legume tasters: symbiotic rhizobia host preference and smart inoculant formulations

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