An Introduced Crop Plant Is Driving Diversification of the Virulent Bacterial Pathogen <named-content content-type="genus-species">Erwinia tracheiphila</named-content>

ABSTRACT Erwinia tracheiphila is the causal agent of bacterial wilt of cucurbits, an economically important phytopathogen affecting few cultivated Cucurbitaceae host plant species in temperate eastern North America. However, essentially nothing is known about E. tracheiphila population structure or...

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Autores principales:	Lori R. Shapiro, Joseph N. Paulson, Brian J. Arnold, Erin D. Scully, Olga Zhaxybayeva, Naomi E. Pierce, Jorge Rocha, Vanja Klepac-Ceraj, Kristina Holton, Roberto Kolter
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	Erwinia agriculture cucurbit disease ecology host jump monoculture Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/7bbfe1264d364e44848a42b072661f58
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spelling	oai:doaj.org-article:7bbfe1264d364e44848a42b072661f582021-11-15T15:58:20ZAn Introduced Crop Plant Is Driving Diversification of the Virulent Bacterial Pathogen <named-content content-type="genus-species">Erwinia tracheiphila</named-content>10.1128/mBio.01307-182150-7511https://doaj.org/article/7bbfe1264d364e44848a42b072661f582018-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01307-18https://doaj.org/toc/2150-7511ABSTRACT Erwinia tracheiphila is the causal agent of bacterial wilt of cucurbits, an economically important phytopathogen affecting few cultivated Cucurbitaceae host plant species in temperate eastern North America. However, essentially nothing is known about E. tracheiphila population structure or genetic diversity. To address this shortcoming, a representative collection of 88 E. tracheiphila isolates was gathered from throughout its geographic range, and their genomes were sequenced. Phylogenomic analysis revealed three genetic clusters with distinct hrpT3SS virulence gene repertoires, host plant association patterns, and geographic distributions. Low genetic heterogeneity within each cluster suggests a recent population bottleneck followed by population expansion. We showed that in the field and greenhouse, cucumber (Cucumis sativus), which was introduced to North America by early Spanish conquistadors, is the most susceptible host plant species and the only species susceptible to isolates from all three lineages. The establishment of large agricultural populations of highly susceptible C. sativus in temperate eastern North America may have facilitated the original emergence of E. tracheiphila into cucurbit agroecosystems, and this introduced plant species may now be acting as a highly susceptible reservoir host. Our findings have broad implications for agricultural sustainability by drawing attention to how worldwide crop plant movement, agricultural intensification, and locally unique environments may affect the emergence, evolution, and epidemic persistence of virulent microbial pathogens. IMPORTANCE Erwinia tracheiphila is a virulent phytopathogen that infects two genera of cucurbit crop plants, Cucurbita spp. (pumpkin and squash) and Cucumis spp. (muskmelon and cucumber). One of the unusual ecological traits of this pathogen is that it is limited to temperate eastern North America. Here, we complete the first large-scale sequencing of an E. tracheiphila isolate collection. From phylogenomic, comparative genomic, and empirical analyses, we find that introduced Cucumis spp. crop plants are driving the diversification of E. tracheiphila into multiple lineages. Together, the results from this study show that locally unique biotic (plant population) and abiotic (climate) conditions can drive the evolutionary trajectories of locally endemic pathogens in unexpected ways.Lori R. ShapiroJoseph N. PaulsonBrian J. ArnoldErin D. ScullyOlga ZhaxybayevaNaomi E. PierceJorge RochaVanja Klepac-CerajKristina HoltonRoberto KolterAmerican Society for MicrobiologyarticleErwiniaagriculturecucurbitdisease ecologyhost jumpmonocultureMicrobiologyQR1-502ENmBio, Vol 9, Iss 5 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	Erwinia agriculture cucurbit disease ecology host jump monoculture Microbiology QR1-502
spellingShingle	Erwinia agriculture cucurbit disease ecology host jump monoculture Microbiology QR1-502 Lori R. Shapiro Joseph N. Paulson Brian J. Arnold Erin D. Scully Olga Zhaxybayeva Naomi E. Pierce Jorge Rocha Vanja Klepac-Ceraj Kristina Holton Roberto Kolter An Introduced Crop Plant Is Driving Diversification of the Virulent Bacterial Pathogen <named-content content-type="genus-species">Erwinia tracheiphila</named-content>
description	ABSTRACT Erwinia tracheiphila is the causal agent of bacterial wilt of cucurbits, an economically important phytopathogen affecting few cultivated Cucurbitaceae host plant species in temperate eastern North America. However, essentially nothing is known about E. tracheiphila population structure or genetic diversity. To address this shortcoming, a representative collection of 88 E. tracheiphila isolates was gathered from throughout its geographic range, and their genomes were sequenced. Phylogenomic analysis revealed three genetic clusters with distinct hrpT3SS virulence gene repertoires, host plant association patterns, and geographic distributions. Low genetic heterogeneity within each cluster suggests a recent population bottleneck followed by population expansion. We showed that in the field and greenhouse, cucumber (Cucumis sativus), which was introduced to North America by early Spanish conquistadors, is the most susceptible host plant species and the only species susceptible to isolates from all three lineages. The establishment of large agricultural populations of highly susceptible C. sativus in temperate eastern North America may have facilitated the original emergence of E. tracheiphila into cucurbit agroecosystems, and this introduced plant species may now be acting as a highly susceptible reservoir host. Our findings have broad implications for agricultural sustainability by drawing attention to how worldwide crop plant movement, agricultural intensification, and locally unique environments may affect the emergence, evolution, and epidemic persistence of virulent microbial pathogens. IMPORTANCE Erwinia tracheiphila is a virulent phytopathogen that infects two genera of cucurbit crop plants, Cucurbita spp. (pumpkin and squash) and Cucumis spp. (muskmelon and cucumber). One of the unusual ecological traits of this pathogen is that it is limited to temperate eastern North America. Here, we complete the first large-scale sequencing of an E. tracheiphila isolate collection. From phylogenomic, comparative genomic, and empirical analyses, we find that introduced Cucumis spp. crop plants are driving the diversification of E. tracheiphila into multiple lineages. Together, the results from this study show that locally unique biotic (plant population) and abiotic (climate) conditions can drive the evolutionary trajectories of locally endemic pathogens in unexpected ways.
format	article
author	Lori R. Shapiro Joseph N. Paulson Brian J. Arnold Erin D. Scully Olga Zhaxybayeva Naomi E. Pierce Jorge Rocha Vanja Klepac-Ceraj Kristina Holton Roberto Kolter
author_facet	Lori R. Shapiro Joseph N. Paulson Brian J. Arnold Erin D. Scully Olga Zhaxybayeva Naomi E. Pierce Jorge Rocha Vanja Klepac-Ceraj Kristina Holton Roberto Kolter
author_sort	Lori R. Shapiro
title	An Introduced Crop Plant Is Driving Diversification of the Virulent Bacterial Pathogen <named-content content-type="genus-species">Erwinia tracheiphila</named-content>
title_short	An Introduced Crop Plant Is Driving Diversification of the Virulent Bacterial Pathogen <named-content content-type="genus-species">Erwinia tracheiphila</named-content>
title_full	An Introduced Crop Plant Is Driving Diversification of the Virulent Bacterial Pathogen <named-content content-type="genus-species">Erwinia tracheiphila</named-content>
title_fullStr	An Introduced Crop Plant Is Driving Diversification of the Virulent Bacterial Pathogen <named-content content-type="genus-species">Erwinia tracheiphila</named-content>
title_full_unstemmed	An Introduced Crop Plant Is Driving Diversification of the Virulent Bacterial Pathogen <named-content content-type="genus-species">Erwinia tracheiphila</named-content>
title_sort	introduced crop plant is driving diversification of the virulent bacterial pathogen <named-content content-type="genus-species">erwinia tracheiphila</named-content>
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/7bbfe1264d364e44848a42b072661f58
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An Introduced Crop Plant Is Driving Diversification of the Virulent Bacterial Pathogen <named-content content-type="genus-species">Erwinia tracheiphila</named-content>

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