Characterization of the Xylella fastidiosa PD1671 Gene Encoding Degenerate c-di-GMP GGDEF/EAL Domains, and Its Role in the Development of Pierce’s Disease

Cursino, Luciana; Athinuwat, Dusit; Patel, Kelly R.; Galvani, Cheryl D.; Zaini, Paulo A.; Li, Yaxin; Fuente, Leonardo De La; Hoch, H. C.; Burr, Thomas J.; Mowery, Patricia

doi:10.1371/journal.pone.0121851

Cited by 14 publications

(5 citation statements)

References 81 publications

(118 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…fastidiosa and multiplex; PD_1285 has a putative conserved RseA domain, a negative regulator of E activity, which suppresses transcription of heat shock response promoters. Four genes with high dN/dS values were associated with GO terms: pilY1 (PD_1611) was associated with a pilus tipassociated protein (34), PD_1506 with a hemolysin-type calcium binding protein involved in pathogenesis (GO:0009405), frpC with a peptidase; and PD_1671 with a GGDEF domain-containing response regulator (35).…”

Section: Vanhove Et Almentioning

confidence: 99%

Genomic Diversity and Recombination among Xylella fastidiosa Subspecies

Vanhove

Retchless

Sicard

et al. 2019

Appl Environ Microbiol

Self Cite

103

View full text Add to dashboard Cite

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 ϫ 10 Ϫ7 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 ϭ 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. IMPORTANCE Xylella 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.

show abstract

Section: Vanhove Et Almentioning

confidence: 99%

Genomic Diversity and Recombination among Xylella fastidiosa Subspecies

Vanhove

Retchless

Sicard

et al. 2019

Appl Environ Microbiol

Self Cite

103

View full text Add to dashboard Cite

show abstract

“…In plant pathogenic bacteria, c-di-GMP regulates numerous pathways that contribute to virulence and host colonization (25). While biofilm formation has been shown to be positively affected by increasing intracellular levels of c-di-GMP in vitro in several systems including E. amylovora (8,9), Pseudomonas fluorescens (26), Xanthomonas oryzae (27), and Xylella fastidiosa (28), a direct link between c-di-GMP mediated regulation and xylem colonization has not been established in these systems. An important finding in our study is that the absence of both intracellular c-di-GMP along with the elimination of the regulatory network involving c-di-GMP renders E. amylovora unable to colonize the xylem within apple shoots.…”

Section: Discussionmentioning

confidence: 99%

The cyclic di-GMP network is a global regulator of phase-transition and attachment-dependent host colonization in Erwinia amylovora

Selbmann

Sundin

2021

Preprint

View full text Add to dashboard Cite

Cyclic-di-GMP (c-di-GMP) is an essential bacterial second messenger that regulates the transition to biofilm formation in the phytopathogen Erwinia amylovora. The c-di-GMP system in E. amylovora is comprised of 12 diguanylate cyclase/Edc (dimerize cyclic-di-GMP) and phosphodiesterase/Pde (hydrolyze cyclic-di-GMP) proteins that are characterized by the presence of GGDEF and/or EAL motifs in their domain architecture. In order to study the global regulatory effect (without the inclusion of systemic regulatory impedance) of the c-di-GMP system in E. amylovora, we eliminated all 12 edc and pde genes in E. amylovora Ea1189Δ12. Comparisons between the representative transcriptomic profiles of Ea1189Δ12 and the combinatorial edc gene knockout mutant (Ea1189Δ5) revealed marked overall distinctions in expression levels for targets in a wide range of regulatory categories, including metabolic pathways involved in the utilization of methionine, isoleucine, histidine, etc. as well as critical signal transduction pathways including the Rcs phosphorelay and PhoPQ system. A complete loss of the cyclic-di-GMP signaling components resulted in the inability of Ea1189Δ12 cells to attach to and form biofilms in vitro and within the xylem vasculature in apple shoots. Using a flow-based in vitro biofilm system, we found that initial surface sensing was primarily dependent on the flagellar filament (FliC), following which the type IV pilus (HofC) was required to anchor cells to the surface to initialize biofilm development. A transcriptomic analysis of WT E. amylovora Ea1189 and Ea1189Δ12 cells in various stages of biofilm development revealed that cyclic-di-GMP based regulation had widespread effects on purine and pyrimidine biosynthesis pathways, amylovoran biosynthesis genes and the EnvZ/OmpR signal transduction system. Additionally, complementing individual eliminated genes back into Ea1189Δ12, and the collective evaluation of several virulence factors, enabled the correlative clustering of the functional effect rendered by each Edc and Pde enzyme in the system.SignificanceCyclic-di-GMP dependent regulation, in the context of biofilm formation, has been studied in several bacterial systems. However, the comprehensiveness of the studies exploring the role of individual genetic components related to cyclic-di-GMP is affected by the often large number of diguanylate cyclase and phosphodiesterase enzymes present within individual bacterial systems. To explore the evolutionary dependencies related to cyclic-di-GMP in E. amylovora, we used a collective elimination approach, whereby all of the enzymes involved in cyclic-di-GMP metabolism were eliminated from the system. This approach enabled us to highlight the critical importance of cyclic-di-GMP in plant xylem colonization due to its effect on surface attachment. Additionally, we highlight the global transcriptomic effect of cyclic-di-GMP dependent signaling at various stages of biofilm development. Our approach is aimed at exploring the regulatory role of individual cyclic-di-GMP related enzymes in a background that is free from any redundancy-based feedback.

show abstract

“…pauca, with at least two pilA copies being conserved in all isolates from both subspecies. The potential significance of pilA gain/loss events in twitching and motility [12,70] and its putative role in X. fastidiosa virulence remains to be evaluated; however, these results suggest that gene duplication might be evolutionarily important for certain virulence factors.…”

Section: Discussionmentioning

confidence: 99%

Impacts of local population history and ecology on the evolution of a globally dispersed pathogen

et al. 2020

View full text Add to dashboard Cite

Background: Pathogens with a global distribution face diverse biotic and abiotic conditions across populations. Moreover, the ecological and evolutionary history of each population is unique. Xylella fastidiosa is a xylem-dwelling bacterium infecting multiple plant hosts, often with detrimental effects. As a group, X. fastidiosa is divided into distinct subspecies with allopatric historical distributions and patterns of multiple introductions from numerous source populations. The capacity of X. fastidiosa to successfully colonize and cause disease in naïve plant hosts varies among subspecies, and potentially, among populations. Within Central America (i.e. Costa Rica) two X. fastidiosa subspecies coexist: the native subsp. fastidiosa and the introduced subsp. pauca. Using whole genome sequences, the patterns of gene gain/loss, genomic introgression, and genetic diversity were characterized within Costa Rica and contrasted to other X. fastidiosa populations. Results: Within Costa Rica, accessory and core genome analyses showed a highly malleable genome with numerous intra-and inter-subspecific gain/loss events. Likewise, variable levels of inter-subspecific introgression were found within and between both coexisting subspecies; nonetheless, the direction of donor/recipient subspecies to the recombinant segments varied. Some strains appeared to recombine more frequently than others; however, no group of genes or gene functions were overrepresented within recombinant segments. Finally, the patterns of genetic diversity of subsp. fastidiosa in Costa Rica were consistent with those of other native populations (i.e. subsp. pauca in Brazil). Conclusions: Overall, this study shows the importance of characterizing local evolutionary and ecological history in the context of worldwide pathogen distribution.

show abstract

Characterization of the Xylella fastidiosa PD1671 Gene Encoding Degenerate c-di-GMP GGDEF/EAL Domains, and Its Role in the Development of Pierce’s Disease

Cited by 14 publications

References 81 publications

Genomic Diversity and Recombination among Xylella fastidiosa Subspecies

Genomic Diversity and Recombination among Xylella fastidiosa Subspecies

The cyclic di-GMP network is a global regulator of phase-transition and attachment-dependent host colonization in Erwinia amylovora

Impacts of local population history and ecology on the evolution of a globally dispersed pathogen

Contact Info

Product

Resources

About