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Diversifying selection in the wheat stem rust fungus acts predominantly on pathogen-associated gene families and reveals candidate effectors

Sperschneider, Jana; Ying, Hua; Dodds, Peter N; Gardiner, Donald M; Upadhyaya, Narayana M; Singh, Karam B; Manners, John M; Taylor, Jennifer M

Description

Plant pathogens cause severe losses to crop plants and threaten global food production. One striking example is the wheat stem rust fungus, Puccinia graminis f. sp. tritici, which can rapidly evolve new virulent pathotypes in response to resistant host lines. Like several other filamentous fungal and oomycete plant pathogens, its genome features expanded gene families that have been implicated in host-pathogen interactions, possibly encoding effector proteins that interact directly with target...[Show more]

dc.contributor.authorSperschneider, Jana
dc.contributor.authorYing, Hua
dc.contributor.authorDodds, Peter N
dc.contributor.authorGardiner, Donald M
dc.contributor.authorUpadhyaya, Narayana M
dc.contributor.authorSingh, Karam B
dc.contributor.authorManners, John M
dc.contributor.authorTaylor, Jennifer M
dc.date.accessioned2016-01-27T01:03:03Z
dc.date.available2016-01-27T01:03:03Z
dc.identifier.issn1664-462X
dc.identifier.urihttp://hdl.handle.net/1885/95667
dc.description.abstractPlant pathogens cause severe losses to crop plants and threaten global food production. One striking example is the wheat stem rust fungus, Puccinia graminis f. sp. tritici, which can rapidly evolve new virulent pathotypes in response to resistant host lines. Like several other filamentous fungal and oomycete plant pathogens, its genome features expanded gene families that have been implicated in host-pathogen interactions, possibly encoding effector proteins that interact directly with target host defense proteins. Previous efforts to understand virulence largely relied on the prediction of secreted, small and cysteine-rich proteins as candidate effectors and thus delivered an overwhelming number of candidates. Here, we implement an alternative analysis strategy that uses the signal of adaptive evolution as a line of evidence for effector function, combined with comparative information and expression data. We demonstrate that in planta up-regulated genes that are rapidly evolving are found almost exclusively in pathogen-associated gene families, affirming the impact of host-pathogen co-evolution on genome structure and the adaptive diversification of specialized gene families. In particular, we predict 42 effector candidates that are conserved only across pathogens, induced during infection and rapidly evolving. One of our top candidates has recently been shown to induce genotype-specific hypersensitive cell death in wheat. This shows that comparative genomics incorporating the evolutionary signal of adaptation is powerful for predicting effector candidates for laboratory verification. Our system can be applied to a wide range of pathogens and will give insight into host-pathogen dynamics, ultimately leading to progress in strategies for disease control.
dc.description.sponsorshipJana Sperschneider was supported by the CSIRO Transformational Biology Capability platform. Donald M. Gardiner was partially supported by the Australian Grains Research and Development Corporation. Narayana M. Upadhyaya and Peter N. Dodds thank the Two Blades Foundation for financial support.
dc.publisherFrontiers Research Foundation
dc.rights© 2014 Sperschneider, Ying, Dodds, Gardiner, Upadhyaya, Singh, Manners and Taylor. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
dc.sourceFrontiers in Plant Science
dc.subjectpuccinia graminis
dc.subjectadaptation
dc.subjectavirulence
dc.subjecteffector
dc.subjectfungal pathogens
dc.subjectrust
dc.subjectselection
dc.titleDiversifying selection in the wheat stem rust fungus acts predominantly on pathogen-associated gene families and reveals candidate effectors
dc.typeJournal article
local.description.notesImported from ARIES
local.identifier.citationvolume5
dc.date.issued2014-09-01
local.identifier.absfor060703
local.identifier.ariespublicationu9511635xPUB1426
local.publisher.urlhttp://www.frontiersin.org/
local.type.statusPublished Version
local.contributor.affiliationSperschneider, Jana, CSIRO, Australia
local.contributor.affiliationYing, Hua, College of Medicine, Biology and Environment, CMBE Research School of Biology, Division of Evolution, Ecology & Genetics, The Australian National University
local.contributor.affiliationDodds, Peter N, CSIRO , Australia
local.contributor.affiliationGardiner, Donald M , Commonwealth Scientific and Industrial Research Organization, Australia
local.contributor.affiliationUpadhyaya, Narayana M, CSIRO Plant Industry, Australia
local.contributor.affiliationSingh, Karam B , CSIRO, Australia
local.contributor.affiliationManners, John, CSIRO, Australia
local.contributor.affiliationTaylor, Jennifer, CSIRO, Australia
local.identifier.essn1664-462X
local.bibliographicCitation.issue372
local.bibliographicCitation.startpage372
local.bibliographicCitation.lastpage13
local.identifier.doi10.3389/fpls.2014.00372
local.identifier.absseo829999
dc.date.updated2016-06-14T09:19:58Z
local.identifier.scopusID2-s2.0-84907348558
CollectionsANU Research Publications

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