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Comparative Genomics of Xylella fastidiosa Explores Candidate Host-Specificity Determinants and Expands the Known Repertoire of Mobile Genetic Elements and Immunity Systems.

ABSTRACT: Xylella fastidiosa causes diseases in many plant species. Originally confined to the Americas, infecting mainly grapevine, citrus, and coffee, X. fastidiosa has spread to several plant species in Europe causing devastating diseases. Many pathogenicity and virulence factors have been identified, which enable the various X. fastidiosa strains to successfully colonize the xylem tissue and cause disease in specific plant hosts, but the mechanisms by which this happens have not been fully elucidated. Here we present thorough comparative analyses of 94 whole-genome sequences of X. fastidiosa strains from diverse plant hosts and geographic regions. Core-genome phylogeny revealed clades with members sharing mostly a geographic region rather than a host plant of origin. Phylogenetic trees for 1605 orthologous CDSs were explored for potential candidates related to host specificity using a score of mapping metrics. However, no candidate host-specificity determinants were strongly supported using this approach. We also show that X. fastidiosa accessory genome is represented by an abundant and heterogeneous mobilome, including a diversity of prophage regions. Our findings provide a better understanding of the diversity of phylogenetically close genomes and expand the knowledge of X. fastidiosa mobile genetic elements and immunity systems.

SUBMITTER: Uceda-Campos G

PROVIDER: S-EPMC9148166 | biostudies-literature | 2022 Apr

REPOSITORIES: biostudies-literature

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Comparative Genomics of Xylella fastidiosa Explores Candidate Host-Specificity Determinants and Expands the Known Repertoire of Mobile Genetic Elements and Immunity Systems.

Uceda-Campos Guillermo G Feitosa-Junior Oseias R OR Santiago Caio R N CRN Pierry Paulo M PM Zaini Paulo A PA de Santana Wesley O WO Martins-Junior Joaquim J Barbosa Deibs D Digiampietri Luciano A LA Setubal João C JC da Silva Aline M AM

Microorganisms 20220427 5

Xylella fastidiosa causes diseases in many plant species. Originally confined to the Americas, infecting mainly grapevine, citrus, and coffee, X. fastidiosa has spread to several plant species in Europe causing devastating diseases. Many pathogenicity and virulence factors have been identified, which enable the various X. fastidiosa strains to successfully colonize the xylem tissue and cause disease in specific plant hosts, but the mechanisms by which this happens have not b ...[more]

PMID: 35630358

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Project description:Xylella fastidiosa is an economically important bacterial plant pathogen. With insights gained from 72 genomes, this study investigated differences among the three main subspecies, which have allopatric origins: X. fastidiosa subsp. fastidiosa, multiplex, and pauca The origin of recombinogenic X. fastidiosa subsp. morus and sandyi was also assessed. The evolutionary rate of the 622 genes of the species core genome was estimated at the scale of an X. fastidiosa subsp. pauca subclade (7.62 × 10-7 substitutions per site per year), which was subsequently used to estimate divergence time for the subspecies and introduction events. The study characterized genes present in the accessory genome of each of the three subspecies and investigated the core genome to detect genes potentially under positive selection. Recombination is recognized to be the major driver of diversity in X. fastidiosa, potentially facilitating shifts to novel plant hosts. The relative effect of recombination in comparison to point mutation was calculated (r/m = 2.259). Evidence of recombination was uncovered in the core genome alignment; X. fastidiosa subsp. fastidiosa in the United States was less prone to recombination, with an average of 3.22 of the 622 core genes identified as recombining regions, whereas a specific clade of X. fastidiosa subsp. multiplex was found to have on average 9.60 recombining genes, 93.2% of which originated from X. fastidiosa subsp. fastidiosa Interestingly, for X. fastidiosa subsp. morus, which was initially thought to be the outcome of genome-wide recombination between X. fastidiosa subsp. fastidiosa and X. fastidiosa subsp. multiplex, intersubspecies homologous recombination levels reached 15.30% in the core genome. Finally, there is evidence of X. fastidiosa subsp. pauca strains from citrus containing genetic elements acquired from strains infecting coffee plants as well as genetic elements from both X. fastidiosa subsp. fastidiosa and X. fastidiosa subsp. multiplex In summary, our data provide new insights into the evolution and epidemiology of this plant pathogen.IMPORTANCEXylella fastidiosa is an important vector-borne plant pathogen. We used a set of 72 genomes that constitutes the largest assembled data set for this bacterial species so far to investigate genetic relationships and the impact of recombination on phylogenetic clades and to compare genome content at the subspecies level, and we used a molecular dating approach to infer the evolutionary rate of X. fastidiosa The results demonstrate that recombination is important in shaping the genomes of X. fastidiosa and that each of the main subspecies is under different selective pressures. We hope insights from this study will improve our understanding of X. fastidiosa evolution and biology.

Project description:Xylella fastidiosa infects several economically important crops in the Americas, and it also recently emerged in Europe. Here, using a set of Xylella genomes reflective of the genus-wide diversity, we performed a pan-genome analysis based on both core and accessory genes for two purposes: (i) to test associations between genetic divergence and plant host species and (ii) to identify positively selected genes that are potentially involved in arms-race dynamics. For the former, tests yielded significant evidence for the specialization of X. fastidiosa to plant host species. This observation contributes to a growing literature suggesting that the phylogenetic history of X. fastidiosa lineages affects the host range. For the latter, our analyses uncovered evidence of positive selection across codons for 5.3% (67 of 1,257) of the core genes and 5.4% (201 of 3,691) of the accessory genes. These genes are candidates to encode interacting factors with plant and insect hosts. Most of these genes had unknown functions, but we did identify some tractable candidates, including nagZ_2, which encodes a beta-glucosidase that is important for Neisseria gonorrhoeae biofilm formation; cya, which modulates gene expression in pathogenic bacteria, and barA, a membrane associated histidine kinase that has roles in cell division, metabolism, and pili formation. IMPORTANCE Xylella fastidiosa causes devasting diseases to several critical crops. Because X. fastidiosa colonizes and infects many plant species, it is important to understand whether the genome of X. fastidiosa has genetic determinants that underlie specialization to specific host plants. We analyzed genome sequences of X. fastidiosa to investigate evolutionary relationships and to test for evidence of positive selection on specific genes. We found a significant signal between genome diversity and host plants, consistent with bacterial specialization to specific plant hosts. By screening for positive selection, we identified both core and accessory genes that may affect pathogenicity, including genes involved in biofilm formation.

Dataset Information

Comparative Genomics of Xylella fastidiosa Explores Candidate Host-Specificity Determinants and Expands the Known Repertoire of Mobile Genetic Elements and Immunity Systems.

Publications

Comparative Genomics of <i>Xylella fastidiosa</i> Explores Candidate Host-Specificity Determinants and Expands the Known Repertoire of Mobile Genetic Elements and Immunity Systems.

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