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Ancestral acquisitions, gene flow and multiple evolutionary trajectories of the type three secretion system and effectors in Xanthomonas plant pathogens

Abstract :

Deciphering the evolutionary history and transmission patterns of virulence determinants
is necessary to understand the emergence of novel pathogens. The main virulence
determinant of most pathogenic proteobacteria is the type three secretion
system (T3SS). The Xanthomonas genus includes bacteria responsible for numerous
epidemics in agroecosystems worldwide and represents a major threat to plant
health. The main virulence factor of Xanthomonas is the Hrp2 family T3SS; however,
this system is not conserved in all strains and it has not been previously determined
whether the distribution of T3SS in this bacterial genus has resulted from losses or
independent acquisitions. Based on comparative genomics of 82 genome sequences
representing the diversity of the genus, we have inferred three ancestral acquisitions
of the Hrp2 cluster during Xanthomonas evolution followed by subsequent
losses in some commensal strains and re-acquisition in some species. While mutation
was the main force driving polymorphism at the gene level, interspecies homologous
recombination of large fragments expanding through several genes shaped
Hrp2 cluster polymorphism. Horizontal gene transfer of the entire Hrp2 cluster also
occurred. A reduced core effectome composed of xopF1, xopM, avrBs2 and xopR
was identified that may allow commensal strains overcoming plant basal immunity.
In contrast, stepwise accumulation of numerous type 3 effector genes was shown in
successful pathogens responsible for epidemics. Our data suggest that capacity to
intimately interact with plants through T3SS would be an ancestral trait of xanthomonads.
Since its acquisition, T3SS has experienced a highly dynamic evolutionary
history characterized by intense gene flux between species that may reflect its
role in host adaptation.

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Contributor : Okina Université d'Angers <>
Submitted on : Friday, October 26, 2018 - 3:11:25 PM
Last modification on : Tuesday, September 8, 2020 - 3:01:18 AM
Long-term archiving on: : Sunday, January 27, 2019 - 2:55:23 PM

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Déborah Merda, Martial Briand, Eran Bosis, Céline Rousseau, Perrine Portier, et al.. Ancestral acquisitions, gene flow and multiple evolutionary trajectories of the type three secretion system and effectors in Xanthomonas plant pathogens. Molecular Ecology, Wiley, 2017, 26 (21), pp.1-14. ⟨10.1111/mec.14343⟩. ⟨hal-01904571⟩

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