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Comparative analysis of the predicted secretomes of Rosaceae scab pathogens Venturia inaequalis and V. pirina reveals expanded effector families and putative determinants of host range

Identifieur interne : 000043 ( France/Analysis ); précédent : 000042; suivant : 000044

Comparative analysis of the predicted secretomes of Rosaceae scab pathogens Venturia inaequalis and V. pirina reveals expanded effector families and putative determinants of host range

Auteurs : Cecilia H. Deng [Nouvelle-Zélande] ; Kim M. Plummer ; Darcy A. B. Jones [Australie] ; Carl H. Mesarich [Nouvelle-Zélande] ; Jason Shiller [France] ; Adam P. Taranto [Australie] ; Andrew J. Robinson [Australie] ; Patrick Kastner ; Nathan E. Hall [Australie] ; Matthew D. Templeton [Nouvelle-Zélande] ; Joanna K. Bowen [Nouvelle-Zélande]

Source :

RBID : PMC:5412055

Abstract

Background

Fungal plant pathogens belonging to the genus Venturia cause damaging scab diseases of members of the Rosaceae. In terms of economic impact, the most important of these are V. inaequalis, which infects apple, and V. pirina, which is a pathogen of European pear. Given that Venturia fungi colonise the sub-cuticular space without penetrating plant cells, it is assumed that effectors that contribute to virulence and determination of host range will be secreted into this plant-pathogen interface. Thus the predicted secretomes of a range of isolates of Venturia with distinct host-ranges were interrogated to reveal putative proteins involved in virulence and pathogenicity.

Results

Genomes of Venturia pirina (one European pear scab isolate) and Venturia inaequalis (three apple scab, and one loquat scab, isolates) were sequenced and the predicted secretomes of each isolate identified. RNA-Seq was conducted on the apple-specific V. inaequalis isolate Vi1 (in vitro and infected apple leaves) to highlight virulence and pathogenicity components of the secretome. Genes encoding over 600 small secreted proteins (candidate effectors) were identified, most of which are novel to Venturia, with expansion of putative effector families a feature of the genus. Numerous genes with similarity to Leptosphaeria maculans AvrLm6 and the Verticillium spp. Ave1 were identified. Candidates for avirulence effectors with cognate resistance genes involved in race-cultivar specificity were identified, as were putative proteins involved in host-species determination. Candidate effectors were found, on average, to be in regions of relatively low gene-density and in closer proximity to repeats (e.g. transposable elements), compared with core eukaryotic genes.

Conclusions

Comparative secretomics has revealed candidate effectors from Venturia fungal plant pathogens that attack pome fruit. Effectors that are putative determinants of host range were identified; both those that may be involved in race-cultivar and host-species specificity. Since many of the effector candidates are in close proximity to repetitive sequences this may point to a possible mechanism for the effector gene family expansion observed and a route to diversification via transposition and repeat-induced point mutation.

Electronic supplementary material

The online version of this article (doi:10.1186/s12864-017-3699-1) contains supplementary material, which is available to authorized users.


Url:
DOI: 10.1186/s12864-017-3699-1
PubMed: 28464870
PubMed Central: 5412055


Affiliations:


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PMC:5412055

Le document en format XML

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<title xml:lang="en" level="a" type="main">Comparative analysis of the predicted secretomes of Rosaceae scab pathogens
<italic>Venturia inaequalis</italic>
and
<italic>V. pirina</italic>
reveals expanded effector families and putative determinants of host range</title>
<author>
<name sortKey="Deng, Cecilia H" sort="Deng, Cecilia H" uniqKey="Deng C" first="Cecilia H." last="Deng">Cecilia H. Deng</name>
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<nlm:aff id="Aff6">
<institution-wrap>
<institution-id institution-id-type="GRID">grid.452643.2</institution-id>
<institution></institution>
<institution>Life Sciences Computation Centre, Victorian Life Sciences Computation Initiative (VLSCI),</institution>
</institution-wrap>
Victoria, Australia</nlm:aff>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>Victoria</wicri:regionArea>
</affiliation>
</author>
<author>
<name sortKey="Kastner, Patrick" sort="Kastner, Patrick" uniqKey="Kastner P" first="Patrick" last="Kastner">Patrick Kastner</name>
<affiliation>
<nlm:aff id="Aff2">
<institution-wrap>
<institution-id institution-id-type="ISNI">0000 0001 2342 0938</institution-id>
<institution-id institution-id-type="GRID">grid.1018.8</institution-id>
<institution>Animal, Plant & Soil Sciences Department,</institution>
<institution>AgriBio Centre for AgriBioscience, La Trobe University,</institution>
</institution-wrap>
Melbourne, Victoria Australia</nlm:aff>
<wicri:noCountry code="subfield">Victoria Australia</wicri:noCountry>
</affiliation>
</author>
<author>
<name sortKey="Hall, Nathan E" sort="Hall, Nathan E" uniqKey="Hall N" first="Nathan E." last="Hall">Nathan E. Hall</name>
<affiliation>
<nlm:aff id="Aff2">
<institution-wrap>
<institution-id institution-id-type="ISNI">0000 0001 2342 0938</institution-id>
<institution-id institution-id-type="GRID">grid.1018.8</institution-id>
<institution>Animal, Plant & Soil Sciences Department,</institution>
<institution>AgriBio Centre for AgriBioscience, La Trobe University,</institution>
</institution-wrap>
Melbourne, Victoria Australia</nlm:aff>
<wicri:noCountry code="subfield">Victoria Australia</wicri:noCountry>
</affiliation>
<affiliation wicri:level="1">
<nlm:aff id="Aff6">
<institution-wrap>
<institution-id institution-id-type="GRID">grid.452643.2</institution-id>
<institution></institution>
<institution>Life Sciences Computation Centre, Victorian Life Sciences Computation Initiative (VLSCI),</institution>
</institution-wrap>
Victoria, Australia</nlm:aff>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>Victoria</wicri:regionArea>
</affiliation>
</author>
<author>
<name sortKey="Templeton, Matthew D" sort="Templeton, Matthew D" uniqKey="Templeton M" first="Matthew D." last="Templeton">Matthew D. Templeton</name>
<affiliation wicri:level="1">
<nlm:aff id="Aff1">
<institution-wrap>
<institution-id institution-id-type="GRID">grid.27859.31</institution-id>
<institution></institution>
<institution>The New Zealand Institute for Plant & Food Research Limited (PFR),</institution>
</institution-wrap>
Auckland, New Zealand</nlm:aff>
<country xml:lang="fr">Nouvelle-Zélande</country>
<wicri:regionArea>Auckland</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1">
<nlm:aff id="Aff4">
<institution-wrap>
<institution-id institution-id-type="ISNI">0000 0004 0372 3343</institution-id>
<institution-id institution-id-type="GRID">grid.9654.e</institution-id>
<institution>The School of Biological Sciences,</institution>
<institution>University of Auckland,</institution>
</institution-wrap>
Auckland, New Zealand</nlm:aff>
<country xml:lang="fr">Nouvelle-Zélande</country>
<wicri:regionArea>Auckland</wicri:regionArea>
</affiliation>
</author>
<author>
<name sortKey="Bowen, Joanna K" sort="Bowen, Joanna K" uniqKey="Bowen J" first="Joanna K." last="Bowen">Joanna K. Bowen</name>
<affiliation wicri:level="1">
<nlm:aff id="Aff1">
<institution-wrap>
<institution-id institution-id-type="GRID">grid.27859.31</institution-id>
<institution></institution>
<institution>The New Zealand Institute for Plant & Food Research Limited (PFR),</institution>
</institution-wrap>
Auckland, New Zealand</nlm:aff>
<country xml:lang="fr">Nouvelle-Zélande</country>
<wicri:regionArea>Auckland</wicri:regionArea>
</affiliation>
</author>
</analytic>
<series>
<title level="j">BMC Genomics</title>
<idno type="eISSN">1471-2164</idno>
<imprint>
<date when="2017">2017</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc>
<textClass></textClass>
</profileDesc>
</teiHeader>
<front>
<div type="abstract" xml:lang="en">
<sec>
<title>Background</title>
<p>Fungal plant pathogens belonging to the genus
<italic>Venturia</italic>
cause damaging scab diseases of members of the Rosaceae. In terms of economic impact, the most important of these are
<italic>V. inaequalis</italic>
, which infects apple, and
<italic>V. pirina</italic>
, which is a pathogen of European pear. Given that
<italic>Venturia</italic>
fungi colonise the sub-cuticular space without penetrating plant cells, it is assumed that effectors that contribute to virulence and determination of host range will be secreted into this plant-pathogen interface. Thus the predicted secretomes of a range of isolates of
<italic>Venturia</italic>
with distinct host-ranges were interrogated to reveal putative proteins involved in virulence and pathogenicity.</p>
</sec>
<sec>
<title>Results</title>
<p>Genomes of
<italic>Venturia pirina</italic>
(one European pear scab isolate) and
<italic>Venturia inaequalis</italic>
(three apple scab, and one loquat scab, isolates) were sequenced and the predicted secretomes of each isolate identified. RNA-Seq was conducted on the apple-specific
<italic>V. inaequalis</italic>
isolate Vi1 (in vitro and infected apple leaves) to highlight virulence and pathogenicity components of the secretome. Genes encoding over 600 small secreted proteins (candidate effectors) were identified, most of which are novel to
<italic>Venturia</italic>
, with expansion of putative effector families a feature of the genus. Numerous genes with similarity to
<italic>Leptosphaeria maculans AvrLm6</italic>
and the
<italic>Verticillium</italic>
spp.
<italic>Ave1</italic>
were identified. Candidates for avirulence effectors with cognate resistance genes involved in race-cultivar specificity were identified, as were putative proteins involved in host-species determination. Candidate effectors were found, on average, to be in regions of relatively low gene-density and in closer proximity to repeats (e.g. transposable elements), compared with core eukaryotic genes.</p>
</sec>
<sec>
<title>Conclusions</title>
<p>Comparative secretomics has revealed candidate effectors from
<italic>Venturia</italic>
fungal plant pathogens that attack pome fruit. Effectors that are putative determinants of host range were identified; both those that may be involved in race-cultivar and host-species specificity. Since many of the effector candidates are in close proximity to repetitive sequences this may point to a possible mechanism for the effector gene family expansion observed and a route to diversification via transposition and repeat-induced point mutation.</p>
</sec>
<sec>
<title>Electronic supplementary material</title>
<p>The online version of this article (doi:10.1186/s12864-017-3699-1) contains supplementary material, which is available to authorized users.</p>
</sec>
</div>
</front>
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