Patterns of inter- and intrasubspecific homologous recombination inform eco-evolutionary dynamics of <i>Xylella fastidiosa</i>

Potnis, Neha; Kandel, Prem P.; Merfa, Marcus V.; Retchless, Adam C.; Parker, Jennifer; Stenger, Drake C.; Almeida, Rodrigo P. P.; Bergsma-Vlami, M.; Westenberg, Marcel; Cobine, Paul A.; Fuente, Leonardo De La

doi:10.1038/s41396-019-0423-y

Cited by 50 publications

(74 citation statements)

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“…Less considered are the impacts of homologous recombination across species. Our results add to a growing body of literature suggesting that, while perhaps less common than intraspecific homologous recombination ( 22 , 23 ), interspecific gene exchange facilitated by homologous recombination at syntenic loci is an important mechanism of adaptation ( 24 ). All three cbsA HGT events within Xanthomonas occurred through homologous recombination in syntenic neighborhoods flanking cbsA presence/absence polymorphisms, and two of these resulted in the reversal of an ancestral loss event (Figure 2), suggesting that synteny conservation potentiates not only gene gain but the reversal of lineage-specific gene loss.…”

Section: Discussionsupporting

confidence: 67%

Repeated gain and loss of a single gene modulates the evolution of vascular pathogen lifestyles

Gluck‐Thaler

Cerutti

Pérez‐Quintero

et al. 2020

Preprint

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37Vascular pathogens travel long distances through host veins leading to life-threatening, systemic 38 infections. In contrast, non-vascular pathogens remain restricted to infection sites, triggering 39 localized symptom development. The contrasting features of vascular and non-vascular diseases 40 suggest distinct etiologies, but the basis for each remains unclear. Here, we show that the 41 hydrolase CbsA acts as a phenotypic switch between vascular and non-vascular plant 42 pathogenesis. cbsA was enriched in genomes of vascular phytopathogenic bacteria in the 43 Xanthomonadaceae family and absent in most non-vascular species. CbsA expression allowed 44 non-vascular Xanthomonas to cause vascular blight while cbsA mutagenesis resulted in reduction 45 of vascular or enhanced non-vascular symptom development. Phylogenetic hypothesis testing 46 further revealed that cbsA was lost in multiple non-vascular lineages and more recently gained by 47 some vascular subgroups, suggesting that vascular pathogenesis is ancestral. Our results overall 48 demonstrate how the gain and loss of single loci can facilitate the evolution of complex ecological 49 traits. 50 51 52 4 MAIN TEXT 53 54 55 56 Pathogenic microorganisms cause diseases of animals and plants. Some pathogenic species 57 colonize the host vasculature, which leads to systemic infection, while others remain localized to 58 non-vascular tissues. Complex structural and biochemical differences between vascular and non-59 vascular tissues suggest that pathogens have multiple distinct adaptations to either environment, 60 yet the genetic and evolutionary bases of such adaptations are largely unknown. 61 62 Adaptations often occur through wholesale gain and loss of specific genes, resulting in more rapid 63 evolution compared with incremental changes at the DNA sequence level alone (1). In bacteria, 64 gene gain occurs primarily through horizontal gene transfer while gene loss or pseudogenization 65 occurs through multiple mechanisms, including transposon-mediated insertions and sequence 66 deletions in open reading frames (2-4). Especially for loci encoding ecologically relevant traits, 67 gene gain and loss effectively act as phenotypic switches, enabling rapid shifts between what 68 otherwise seem like complex lifestyles (3). For example, transitions between plant pathogenic and 69 commensal Pseudomonas (5), transitions between mutualist and parasitic phenotypes in nitrogen-70 fixing bacteria (6, 7) and transitions between mutualistic and plant pathogenic Rhodococcus (8) 71 have all been shown to reproducibly occur through the gain and loss of genomic islands 72 containing multiple genes all contributing to the same phenotype. Such rapid evolutionary 73 dynamics have profound implications for our understanding of disease ecology and disease 74 management strategies. 75 76 93 94Here, we used Xanthomonas as a model to study the etiology of plant vascular pathogenesis 95 because this genus contains multiple independent pairs of strains from the same species that cause 96 e...

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Section: Discussionsupporting

confidence: 67%

Repeated gain and loss of a single gene modulates the evolution of vascular pathogen lifestyles

Gluck‐Thaler

Cerutti

Pérez‐Quintero

et al. 2020

Preprint

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“…Homologous recombination events were detected in Xf and were suspected to be associated with host-shift, as documented for the subspecies morus (Nunney et al, 2014). But intrasubspecific homologous recombination events could be more frequent than intersubspecific events (Potnis et al, 2019). Based on genome sequence analyses, it was proposed to merge the subspecies fastidiosa, morus, and sandyi in the subspecies fastidiosa [hereafter referred to Xff sensu lato (Xffsl) to avoid confusion with classical Xff], the subspecies multiplex and pauca remaining coherent groups and distantly related from Xff (Marcelletti and Scortichini, 2016;Denancé et al, 2019).…”

Section: Introductionmentioning

confidence: 92%

Novel Tetraplex Quantitative PCR Assays for Simultaneous Detection and Identification of Xylella fastidiosa Subspecies in Plant Tissues

et al. 2019

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Xylella fastidiosa (Xf) is an insect-borne bacterium confined to the xylem vessels of plants. This plant pathogen has a broad host range estimated to 560 plant species. Five subspecies of the pathogen with different but overlapping host ranges have been described, but only three subspecies are widely accepted, namely subspecies fastidiosa, multiplex, and pauca. Initially limited to the Americas, Xf has been detected in Europe since 2013. As management of X. fastidiosa outbreaks in Europe depends on the identification of the subspecies, accurate determination of the subspecies in infected plants as early as possible is of major interest. Thus, we developed various tetraplex and triplex quantitative PCR (qPCR) assays for X. fastidiosa detection and subspecies identification in planta in a single reaction. We designed primers and probes using SkIf, a bioinformatics tool based on k-mers, to detect specific signatures of the species and subspecies from a data set of 58 genome sequences representative of X. fastidiosa diversity. We tested the qPCR assays on 39 target and 30 non-target strains, as well as on 13 different plant species spiked with strains of the different subspecies of X. fastidiosa, and on samples from various environmental and inoculated host plants. Sensitivity of simplex assays was equal or slightly better than the reference protocol on purified DNA. Tetraplex qPCR assays had the same sensitivity than the reference protocol and allowed X. fastidiosa detection in all spiked matrices up to 10 3 cells.ml −1. Moreover, mix infections of two to three subspecies could be detected in the same sample with tetraplex assays. In environmental plant samples, the tetraplex qPCR assays allowed subspecies identification when the current method based on multilocus sequence typing failed. The qPCR assays described here are robust and modular tools that are efficient for differentiating X. fastidiosa subspecies directly in plant samples.

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“…Intra-subspecific and inter-subspecific recombination commonly occur in subsp. pauca (Nunney et al 2012;Coletta-Filho et al 2017;Potnis et al 2019). Nonetheless, the frequency of recombination events varies among clades.…”

Section: Historical Perspectivementioning

confidence: 99%

Citrus Variegated Chlorosis: an Overview of 30 Years of Research and Disease Management

Coletta-Filho

Castillo

Laranjeira

et al. 2020

Trop. plant pathol.

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The emergence of citrus variegated chlorosis (CVC) disease had dramatic consequences to the citrus industry in Brazil. First reported in São Paulo State in 1987, this disease affected approximately 100 million sweet orange trees in the region 20 years later. However, current estimates indicate that the number of diseased trees has been reduced 25-fold since 2009. In this review we summarize research on CVC since its emergence, focusing on work that has contributed to the observed success in managing this disease in the field. Knowledge that CVC is caused by a bacterium (Xylella fastidiosa-now classified as X. fastidiosa subsp. pauca) that is transmited by infected plant material (grafting and nursery plant) and insect vectors, the citrus nursery production system switched in 2003 to a certification program in which plants are grown in insect proof screen-houses and routinely monitored for X. fastidiosa infection. Research triggered by the genome sequencing of a CVC isolate in 2000, the first plant pathogenic bacterium to have its complete genome sequenced, integrated molecular tools and approaches into research aimed at understanding the biology of this pathogen. Ultimately, the challenges imposed by CVC led to significant improvements in the scientific and technical knowledge linked to sweet orange production, and to the development of a more sustainable and resilient citrus industry in Brazil.

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Patterns of inter- and intrasubspecific homologous recombination inform eco-evolutionary dynamics of Xylella fastidiosa

Cited by 50 publications

References 85 publications

Repeated gain and loss of a single gene modulates the evolution of vascular pathogen lifestyles

Repeated gain and loss of a single gene modulates the evolution of vascular pathogen lifestyles

Novel Tetraplex Quantitative PCR Assays for Simultaneous Detection and Identification of Xylella fastidiosa Subspecies in Plant Tissues

Citrus Variegated Chlorosis: an Overview of 30 Years of Research and Disease Management

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