Angular Leaf Spot of Cucurbits is Associated With Genetically Diverse<i>Pseudomonas syringae</i>Strains

Newberry, E. A.; Jardini, Teresa M.; Rubio, I.; Roberts, Pamela D.; Babu, Binoy; Koike, S. T.; Bouzar, H.; Goss, Erica M.; Jones, J. B.; Bull, Carolee T.; Paret, Mathews L.

doi:10.1094/pdis-11-15-1332-re

Cited by 29 publications

(10 citation statements)

References 29 publications

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“…Furthermore, in these tests some of the most aggressive strains on pea were those closely related to strains from pea but that had been isolated from other diseased plants including lilac, common bean, hairy vetch and cantaloupe (Martin-Sanz et al 2013). Several independent studies on P. syringae causing blights to cucurbits have revealed that there is a wide genetic diversity of strains from epidemics to cantaloupe, squash and watermelon and that the strains are virulent to numerous cucurbit species as well as to other herbaceous plants (Morris et al 2000;Sedighian et al 2014;Newberry et al 2016). These examples raise questions about the extent of cross contaminations and spill over.…”

Section: Introductionmentioning

confidence: 99%

The overlapping continuum of host range among strains in the Pseudomonas syringae complex

et al. 2019

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Pseudomonas syringae is the most frequently emerging group of plant pathogenic bacteria. Because this bacterium is ubiquitous as an epiphyte and on various substrates in non-agricultural settings, there are many questions about how to assess the risk for plant disease posed by strains in the environment. Although P. syringae is considered to have discrete host ranges in defined pathovars, there have been few reports of comprehensive comparisons of host range potential. Here we present results of host range tests for 134 strains, representing eight phylogroups, from epidemics and environmental reservoirs on 15 to 22 plant species per test conducted in four separate tests to determine the patterns and extent of host range. We sought to identify trends that are indicative of distinct pathotypes and to assess if strains in the P. syringae complex are indeed restricted in their host range. We show that for each test, strains display a diversity of host ranges from very restricted to very broad regardless of the gamut of phylogroups used in the test. Overall, strains form an overlapping continuum of host range potential with equal representation of narrow, moderate and broad host ranges. Groups of distinct pathotypes, including strains with currently the same pathovar name, could not be identified. The absence of groupings was validated with statistical tests for pattern recognition. The extent of host range was positively correlated with the capacity of strains to swarm on semi-solid agar medium and with the abundance of genes in biosynthetic clusters and was inversely correlated with the abundance of genes for proteins with transmembrane domains in their genomes. Our results are consistent with the current paradigm that disease symptoms are the result of multiple molecular interactions between P. syringae and its plant host that are modulated by abiotic and biotic conditions. This leads us to propose that pathovar denominations do not correspond to the underlying biology of P. syringae. A new concept of pathogenicity that accounts for the continuum of pathogenic potential in P. syringae would open new perspectives to understand the evolution of pathogenicity in this bacterium and new insights to anticipate disease and to manage plant health.

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Section: Introductionmentioning

confidence: 99%

The overlapping continuum of host range among strains in the Pseudomonas syringae complex

et al. 2019

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“…These strains were isolated from watermelon and squash grown in six different Florida counties during these epidemics and comprised haplotypes one and two (Newberry et al, 2018). Three strains included for sequencing comprised haplotype three and were isolated from cantaloupe and squash grown in Florida, Georgia, and California between 2000 and 2006 (Newberry et al, 2016). Finally, three additional strains that were isolated from symptomatic squash grown in Italy, Serbia, and China between 2005 and 2013 were also sequenced because they were found to be identical at four partial housekeeping gene sequences to one of the previously mentioned haplotypes (Hwang et al, 2005).…”

Section: Methodsmentioning

confidence: 99%

“…syringae type/pathotype strain, LMG 1247 PT (=ICMP 3023 T ), within phylogroup 2b. Additionally, we identified two other clonal lineages collected from either the same, or previous bacterial leaf spot epidemics in the United States that shared a recent a common ancestor with the aforementioned epidemic clone; however, were located in a separate phylogroup within the same species, namely phylogroup 2a (Newberry et al, 2016, 2018). Although, we were able to precisely classify these pathogens within the phylogenetic structure of P. syringae sensu lato using MLSA, we were unable to delineate them from other strains collected from a diverse group of plant species or attribute them to any pathovar previously associated with cucurbit hosts, other than P. syringae pv.…”

Section: Introductionmentioning

confidence: 99%

Inference of Convergent Gene Acquisition Among Pseudomonas syringae Strains Isolated From Watermelon, Cantaloupe, and Squash

et al. 2019

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Pseudomonas syringae sensu stricto (phylogroup 2; referred to as P. syringae ) consists of an environmentally ubiquitous bacterial population associated with diseases of numerous plant species. Recent studies using multilocus sequence analysis have indicated the clonal expansion of several P. syringae lineages, located in phylogroups 2a and 2b, in association with outbreaks of bacterial spot disease of watermelon, cantaloupe, and squash in the United States. To investigate the evolutionary processes that led to the emergence of these epidemic lineages, we sequenced the genomes of six P. syringae strains that were isolated from cucurbits grown in the United States, Europe, and China over a period of more than a decade, as well as eight strains that were isolated from watermelon and squash grown in six different Florida counties during the 2013 and 2014 seasons. These data were subjected to comparative analyses along with 42 previously sequenced genomes of P. syringae stains collected from diverse plant species and environments available from GenBank. Maximum likelihood reconstruction of the P. syringae core genome revealed the presence of a hybrid phylogenetic group, comprised of cucurbit strains collected in Florida, Italy, Serbia, and France, which emerged through genome-wide homologous recombination between phylogroups 2a and 2b. Functional analysis of the recombinant core genome showed that pathways involved in the ATP-dependent transport and metabolism of amino acids, bacterial motility, and secretion systems were enriched for recombination. A survey of described virulence factors indicated the convergent acquisition of several accessory type 3 secreted effectors (T3SEs) among phylogenetically distinct lineages through integrative and conjugative element and plasmid loci. Finally, pathogenicity assays on watermelon and squash showed qualitative differences in virulence between strains of the same clonal lineage, which correlated with T3SEs acquired through various mechanisms of horizontal gene transfer (HGT). This study provides novel insights into the interplay of homologous recombination and HGT toward pathogen emergence and highlights the dynamic nature of P. syringae sensu lato genomes.

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“…2b). It is interesting to note that Newberry et al (2016) demonstrated that some strains associated with angular leaf spot in cucurbits are phylogenetically distinct from pathovar lachrymans. Strain classification is also an issue in other pathovars.…”

Section: Discussionmentioning

confidence: 99%

“…bacterial angular leaf spot, is distributed worldwide and appears on other cucurbit species as well. Novel haplotypes of P. syringae were observed to be common on multiple cucurbit hosts, thus illustrating this species' large ecological diversity (Newberry et al 2016). Moreover, pathovar lachrymans is particularly detrimental because it can facilitate infection by Pseudoperonospora cubensis, which is the most destructive cucumber pathogen that causes downy mildew (Olczak-Woltman et al 2008).…”

Section: Introductionmentioning

confidence: 96%

Genome analysis of Pseudomonas syringae pv. lachrymans strain 814/98 indicates diversity within the pathovar

et al. 2017

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Although many Pseudomonas syringae strains have already been determined, only a few genomes of strains belonging to pathovar lachrymans have been sequenced so far. In this study we report the genome sequence of P. syringae pv. lachrymans strain 814/98, which is highly virulent to cucumber. The genome size was estimated to be 6.58 Mb, with 57.97% GC content. In total, 6024 genes encoding proteins and 92 genes encoding RNAs were identified in this genome. Comparisons with the available sequenced genomes of pathovar lachrymans as well as with other P. syringae pathovars were conducted, revealing the presence of three unique plasmids and 24 type III effector proteins (TTEs) in strain 814/98. The phylogenetic analyses of MLST loci and TTEs clearly showed the existence of two distinct clusters of strains within pathovar lachrymans, which were grouped into either phylogroup 1 or 3, supporting non-monophyly within this pathovar.

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Angular Leaf Spot of Cucurbits is Associated With Genetically DiversePseudomonas syringaeStrains

Cited by 29 publications

References 29 publications

The overlapping continuum of host range among strains in the Pseudomonas syringae complex

The overlapping continuum of host range among strains in the Pseudomonas syringae complex

Inference of Convergent Gene Acquisition Among Pseudomonas syringae Strains Isolated From Watermelon, Cantaloupe, and Squash

Genome analysis of Pseudomonas syringae pv. lachrymans strain 814/98 indicates diversity within the pathovar

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