Serveur d'exploration Melampsora (ISTEX)

Attention, ce site est en cours de développement !
Attention, site généré par des moyens informatiques à partir de corpus bruts.
Les informations ne sont donc pas validées.

TNL genes in peach: insights into the post-LRR domain

Identifieur interne : 000697 ( Ncbi/Merge ); précédent : 000696; suivant : 000698

TNL genes in peach: insights into the post-LRR domain

Auteurs : Cyril Van Ghelder [France] ; Daniel Esmenjaud [France]

Source :

RBID : PMC:4851768

Abstract

Background

Plants develop sustainable defence responses to pathogen attacks through resistance (R) genes contributing to effector-triggered immunity (ETI). TIR-NB-LRR genes (TNL genes) constitute a major family of ETI R genes in dicots. The putative functions or roles of the TIR, NB and LRR domains of the proteins they encode (TNLs) are well documented, but TNLs also have a poorly characterised C-terminal region, the function of which is unknown in most cases. We characterised this prevalent stress-response protein family in a perennial plant, using the genome of peach (Prunus persica), the model Prunus species. The first TNL gene from this genus to be cloned, the Ma gene, confers complete-spectrum resistance to root-knot nematodes (RKNs) and encodes a protein with a huge C-terminal region with five duplicated post-LRR (PL) domains. This gene was the cornerstone of this study.

Results

We investigated the role of this C-terminal region, by first describing the frequency, distribution and structural characteristics of i) TNL genes and ii) their PL domains in the peach genome, using the v1.0 Sanger sequence together with the v2.0 sequence, which has better genome annotation due to the incorporation of transcriptomic data. We detected 195 predicted TNL genes from the eight peach chromosomes: 85 % of these genes mapped to chromosomes 1, 2, 7 and 8. We reconstructed the putative structure of the predicted exons of all the TNL genes identified, and it was possible to retrieve the PL domains among two thirds of the TNL genes. We used our predicted TNL gene sequences to develop an annotation file for use with the Gbrowse tool in the v2.0 genome. The use of these annotation data made it possible to detect transcribed PL sequences in two Prunus species. We then used consensus sequences defined on the basis of 124 PL domains to design specific motifs, and we found that the use of these motifs significantly increased the numbers of PL domains and correlative TNL genes detected in diverse dicot genomes. Based on PL signatures, we showed that TNL genes with multiple PL domains were rare in peach and the other plants screened. The five-PL domain pattern is probably unique to Ma and its orthologues within Prunus and closely related genera from the Rosaceae and was probably inherited from the common ancestor of these plants in the subfamily Spiraeoideae.

Conclusions

The first physical TNL gene map for Prunus species can be used for the further investigation of R genes in this genus. The PL signature motifs are a complementary tool for the detection of TNL R genes in dicots. The low degree of similarity between PL domains and the neighbouring LRR exons and the specificity of PL signature motifs suggest that PL and LRR domains have different origins, with PL domains being specific to TNL genes, and possibly essential to the functioning of these genes in some cases. Investigations of the role of the oversized Ma PL region, in ligand binding or intramolecular interactions for example, may help to enrich our understanding of NB-LRR-mediated plant immunity to RKNs.

Electronic supplementary material

The online version of this article (doi:10.1186/s12864-016-2635-0) contains supplementary material, which is available to authorized users.


Url:
DOI: 10.1186/s12864-016-2635-0
PubMed: 27129402
PubMed Central: 4851768

Links toward previous steps (curation, corpus...)


Links to Exploration step

PMC:4851768

Le document en format XML

<record>
<TEI>
<teiHeader>
<fileDesc>
<titleStmt>
<title xml:lang="en">TNL genes in peach: insights into the post-LRR domain</title>
<author>
<name sortKey="Van Ghelder, Cyril" sort="Van Ghelder, Cyril" uniqKey="Van Ghelder C" first="Cyril" last="Van Ghelder">Cyril Van Ghelder</name>
<affiliation wicri:level="3">
<nlm:aff id="Aff1">INRA, UMR 1355 Institut Sophia Agrobiotech, 06900 Sophia Antipolis, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>INRA, UMR 1355 Institut Sophia Agrobiotech, 06900 Sophia Antipolis</wicri:regionArea>
<placeName>
<region type="region" nuts="2">Provence-Alpes-Côte d'Azur</region>
<settlement type="city">Sophia Antipolis</settlement>
</placeName>
</affiliation>
<affiliation wicri:level="3">
<nlm:aff id="Aff2">University Nice Sophia Antipolis, UMR 7254 Institut Sophia Agrobiotech, 06900 Sophia Antipolis, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>University Nice Sophia Antipolis, UMR 7254 Institut Sophia Agrobiotech, 06900 Sophia Antipolis</wicri:regionArea>
<placeName>
<region type="region" nuts="2">Provence-Alpes-Côte d'Azur</region>
<settlement type="city">Sophia Antipolis</settlement>
</placeName>
</affiliation>
<affiliation wicri:level="3">
<nlm:aff id="Aff3">CNRS, UMR 7254 Institut Sophia Agrobiotech, 06900 Sophia Antipolis, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>CNRS, UMR 7254 Institut Sophia Agrobiotech, 06900 Sophia Antipolis</wicri:regionArea>
<placeName>
<region type="region" nuts="2">Provence-Alpes-Côte d'Azur</region>
<settlement type="city">Sophia Antipolis</settlement>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Esmenjaud, Daniel" sort="Esmenjaud, Daniel" uniqKey="Esmenjaud D" first="Daniel" last="Esmenjaud">Daniel Esmenjaud</name>
<affiliation wicri:level="3">
<nlm:aff id="Aff1">INRA, UMR 1355 Institut Sophia Agrobiotech, 06900 Sophia Antipolis, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>INRA, UMR 1355 Institut Sophia Agrobiotech, 06900 Sophia Antipolis</wicri:regionArea>
<placeName>
<region type="region" nuts="2">Provence-Alpes-Côte d'Azur</region>
<settlement type="city">Sophia Antipolis</settlement>
</placeName>
</affiliation>
<affiliation wicri:level="3">
<nlm:aff id="Aff2">University Nice Sophia Antipolis, UMR 7254 Institut Sophia Agrobiotech, 06900 Sophia Antipolis, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>University Nice Sophia Antipolis, UMR 7254 Institut Sophia Agrobiotech, 06900 Sophia Antipolis</wicri:regionArea>
<placeName>
<region type="region" nuts="2">Provence-Alpes-Côte d'Azur</region>
<settlement type="city">Sophia Antipolis</settlement>
</placeName>
</affiliation>
<affiliation wicri:level="3">
<nlm:aff id="Aff3">CNRS, UMR 7254 Institut Sophia Agrobiotech, 06900 Sophia Antipolis, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>CNRS, UMR 7254 Institut Sophia Agrobiotech, 06900 Sophia Antipolis</wicri:regionArea>
<placeName>
<region type="region" nuts="2">Provence-Alpes-Côte d'Azur</region>
<settlement type="city">Sophia Antipolis</settlement>
</placeName>
</affiliation>
</author>
</titleStmt>
<publicationStmt>
<idno type="wicri:source">PMC</idno>
<idno type="pmid">27129402</idno>
<idno type="pmc">4851768</idno>
<idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4851768</idno>
<idno type="RBID">PMC:4851768</idno>
<idno type="doi">10.1186/s12864-016-2635-0</idno>
<date when="2016">2016</date>
<idno type="wicri:Area/Pmc/Corpus">000144</idno>
<idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000144</idno>
<idno type="wicri:Area/Pmc/Curation">000144</idno>
<idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000144</idno>
<idno type="wicri:Area/Pmc/Checkpoint">000563</idno>
<idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">000563</idno>
<idno type="wicri:Area/Ncbi/Merge">000697</idno>
</publicationStmt>
<sourceDesc>
<biblStruct>
<analytic>
<title xml:lang="en" level="a" type="main">TNL genes in peach: insights into the post-LRR domain</title>
<author>
<name sortKey="Van Ghelder, Cyril" sort="Van Ghelder, Cyril" uniqKey="Van Ghelder C" first="Cyril" last="Van Ghelder">Cyril Van Ghelder</name>
<affiliation wicri:level="3">
<nlm:aff id="Aff1">INRA, UMR 1355 Institut Sophia Agrobiotech, 06900 Sophia Antipolis, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>INRA, UMR 1355 Institut Sophia Agrobiotech, 06900 Sophia Antipolis</wicri:regionArea>
<placeName>
<region type="region" nuts="2">Provence-Alpes-Côte d'Azur</region>
<settlement type="city">Sophia Antipolis</settlement>
</placeName>
</affiliation>
<affiliation wicri:level="3">
<nlm:aff id="Aff2">University Nice Sophia Antipolis, UMR 7254 Institut Sophia Agrobiotech, 06900 Sophia Antipolis, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>University Nice Sophia Antipolis, UMR 7254 Institut Sophia Agrobiotech, 06900 Sophia Antipolis</wicri:regionArea>
<placeName>
<region type="region" nuts="2">Provence-Alpes-Côte d'Azur</region>
<settlement type="city">Sophia Antipolis</settlement>
</placeName>
</affiliation>
<affiliation wicri:level="3">
<nlm:aff id="Aff3">CNRS, UMR 7254 Institut Sophia Agrobiotech, 06900 Sophia Antipolis, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>CNRS, UMR 7254 Institut Sophia Agrobiotech, 06900 Sophia Antipolis</wicri:regionArea>
<placeName>
<region type="region" nuts="2">Provence-Alpes-Côte d'Azur</region>
<settlement type="city">Sophia Antipolis</settlement>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Esmenjaud, Daniel" sort="Esmenjaud, Daniel" uniqKey="Esmenjaud D" first="Daniel" last="Esmenjaud">Daniel Esmenjaud</name>
<affiliation wicri:level="3">
<nlm:aff id="Aff1">INRA, UMR 1355 Institut Sophia Agrobiotech, 06900 Sophia Antipolis, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>INRA, UMR 1355 Institut Sophia Agrobiotech, 06900 Sophia Antipolis</wicri:regionArea>
<placeName>
<region type="region" nuts="2">Provence-Alpes-Côte d'Azur</region>
<settlement type="city">Sophia Antipolis</settlement>
</placeName>
</affiliation>
<affiliation wicri:level="3">
<nlm:aff id="Aff2">University Nice Sophia Antipolis, UMR 7254 Institut Sophia Agrobiotech, 06900 Sophia Antipolis, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>University Nice Sophia Antipolis, UMR 7254 Institut Sophia Agrobiotech, 06900 Sophia Antipolis</wicri:regionArea>
<placeName>
<region type="region" nuts="2">Provence-Alpes-Côte d'Azur</region>
<settlement type="city">Sophia Antipolis</settlement>
</placeName>
</affiliation>
<affiliation wicri:level="3">
<nlm:aff id="Aff3">CNRS, UMR 7254 Institut Sophia Agrobiotech, 06900 Sophia Antipolis, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>CNRS, UMR 7254 Institut Sophia Agrobiotech, 06900 Sophia Antipolis</wicri:regionArea>
<placeName>
<region type="region" nuts="2">Provence-Alpes-Côte d'Azur</region>
<settlement type="city">Sophia Antipolis</settlement>
</placeName>
</affiliation>
</author>
</analytic>
<series>
<title level="j">BMC Genomics</title>
<idno type="eISSN">1471-2164</idno>
<imprint>
<date when="2016">2016</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc>
<textClass></textClass>
</profileDesc>
</teiHeader>
<front>
<div type="abstract" xml:lang="en">
<sec>
<title>Background</title>
<p>Plants develop sustainable defence responses to pathogen attacks through resistance (
<italic>R</italic>
) genes contributing to effector-triggered immunity (ETI). TIR-NB-LRR genes (TNL genes) constitute a major family of ETI
<italic>R</italic>
genes in dicots. The putative functions or roles of the TIR, NB and LRR domains of the proteins they encode (TNLs) are well documented, but TNLs also have a poorly characterised C-terminal region, the function of which is unknown in most cases. We characterised this prevalent stress-response protein family in a perennial plant, using the genome of peach (
<italic>Prunus persica</italic>
), the model
<italic>Prunus</italic>
species. The first TNL gene from this genus to be cloned, the
<italic>Ma</italic>
gene, confers complete-spectrum resistance to root-knot nematodes (RKNs) and encodes a protein with a huge C-terminal region with five duplicated post-LRR (PL) domains. This gene was the cornerstone of this study.</p>
</sec>
<sec>
<title>Results</title>
<p>We investigated the role of this C-terminal region, by first describing the frequency, distribution and structural characteristics of i) TNL genes and ii) their PL domains in the peach genome, using the v1.0 Sanger sequence together with the v2.0 sequence, which has better genome annotation due to the incorporation of transcriptomic data. We detected 195 predicted TNL genes from the eight peach chromosomes: 85 % of these genes mapped to chromosomes 1, 2, 7 and 8. We reconstructed the putative structure of the predicted exons of all the TNL genes identified, and it was possible to retrieve the PL domains among two thirds of the TNL genes. We used our predicted TNL gene sequences to develop an annotation file for use with the Gbrowse tool in the v2.0 genome. The use of these annotation data made it possible to detect transcribed PL sequences in two
<italic>Prunus</italic>
species. We then used consensus sequences defined on the basis of 124 PL domains to design specific motifs, and we found that the use of these motifs significantly increased the numbers of PL domains and correlative TNL genes detected in diverse dicot genomes. Based on PL signatures, we showed that TNL genes with multiple PL domains were rare in peach and the other plants screened. The five-PL domain pattern is probably unique to
<italic>Ma</italic>
and its orthologues within
<italic>Prunus</italic>
and closely related genera from the Rosaceae and was probably inherited from the common ancestor of these plants in the subfamily Spiraeoideae.</p>
</sec>
<sec>
<title>Conclusions</title>
<p>The first physical TNL gene map for
<italic>Prunus</italic>
species can be used for the further investigation of
<italic>R</italic>
genes in this genus. The PL signature motifs are a complementary tool for the detection of TNL
<italic>R</italic>
genes in dicots. The low degree of similarity between PL domains and the neighbouring LRR exons and the specificity of PL signature motifs suggest that PL and LRR domains have different origins, with PL domains being specific to TNL genes, and possibly essential to the functioning of these genes in some cases. Investigations of the role of the oversized
<italic>Ma</italic>
PL region, in ligand binding or intramolecular interactions for example, may help to enrich our understanding of NB-LRR-mediated plant immunity to RKNs.</p>
</sec>
<sec>
<title>Electronic supplementary material</title>
<p>The online version of this article (doi:10.1186/s12864-016-2635-0) contains supplementary material, which is available to authorized users.</p>
</sec>
</div>
</front>
<back>
<div1 type="bibliography">
<listBibl>
<biblStruct>
<analytic>
<author>
<name sortKey="Jones, Jdg" uniqKey="Jones J">JDG Jones</name>
</author>
<author>
<name sortKey="Dangl, Jl" uniqKey="Dangl J">JL Dangl</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Dangl, Jl" uniqKey="Dangl J">JL Dangl</name>
</author>
<author>
<name sortKey="Jones, Jdg" uniqKey="Jones J">JDG Jones</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Meyers, Bc" uniqKey="Meyers B">BC Meyers</name>
</author>
<author>
<name sortKey="Kozik, A" uniqKey="Kozik A">A Kozik</name>
</author>
<author>
<name sortKey="Griego, A" uniqKey="Griego A">A Griego</name>
</author>
<author>
<name sortKey="Kuang, Hh" uniqKey="Kuang H">HH Kuang</name>
</author>
<author>
<name sortKey="Michelmore, Rw" uniqKey="Michelmore R">RW Michelmore</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Zhou, T" uniqKey="Zhou T">T Zhou</name>
</author>
<author>
<name sortKey="Wang, Y" uniqKey="Wang Y">Y Wang</name>
</author>
<author>
<name sortKey="Chen, Jq" uniqKey="Chen J">JQ Chen</name>
</author>
<author>
<name sortKey="Araki, H" uniqKey="Araki H">H Araki</name>
</author>
<author>
<name sortKey="Jing, Z" uniqKey="Jing Z">Z Jing</name>
</author>
<author>
<name sortKey="Jiang, K" uniqKey="Jiang K">K Jiang</name>
</author>
<author>
<name sortKey="Shen, J" uniqKey="Shen J">J Shen</name>
</author>
<author>
<name sortKey="Tian, D" uniqKey="Tian D">D Tian</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Kohler, A" uniqKey="Kohler A">A Kohler</name>
</author>
<author>
<name sortKey="Rinaldi, C" uniqKey="Rinaldi C">C Rinaldi</name>
</author>
<author>
<name sortKey="Duplessis, S" uniqKey="Duplessis S">S Duplessis</name>
</author>
<author>
<name sortKey="Baucher, M" uniqKey="Baucher M">M Baucher</name>
</author>
<author>
<name sortKey="Geelen, D" uniqKey="Geelen D">D Geelen</name>
</author>
<author>
<name sortKey="Duchaussoy, F" uniqKey="Duchaussoy F">F Duchaussoy</name>
</author>
<author>
<name sortKey="Meyers, Bc" uniqKey="Meyers B">BC Meyers</name>
</author>
<author>
<name sortKey="Boerjan, W" uniqKey="Boerjan W">W Boerjan</name>
</author>
<author>
<name sortKey="Martin, F" uniqKey="Martin F">F Martin</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Yang, Sh" uniqKey="Yang S">SH Yang</name>
</author>
<author>
<name sortKey="Zhang, Xh" uniqKey="Zhang X">XH Zhang</name>
</author>
<author>
<name sortKey="Yue, Jx" uniqKey="Yue J">JX Yue</name>
</author>
<author>
<name sortKey="Tian, Dc" uniqKey="Tian D">DC Tian</name>
</author>
<author>
<name sortKey="Chen, Jq" uniqKey="Chen J">JQ Chen</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Yue, Jx" uniqKey="Yue J">JX Yue</name>
</author>
<author>
<name sortKey="Meyers, Bc" uniqKey="Meyers B">BC Meyers</name>
</author>
<author>
<name sortKey="Chen, Jq" uniqKey="Chen J">JQ Chen</name>
</author>
<author>
<name sortKey="Tian, Dc" uniqKey="Tian D">DC Tian</name>
</author>
<author>
<name sortKey="Yang, Sh" uniqKey="Yang S">SH Yang</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Tarr, De" uniqKey="Tarr D">DE Tarr</name>
</author>
<author>
<name sortKey="Alexander, Hm" uniqKey="Alexander H">HM Alexander</name>
</author>
</analytic>
</biblStruct>
<biblStruct></biblStruct>
<biblStruct></biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Hulbert, Sh" uniqKey="Hulbert S">SH Hulbert</name>
</author>
<author>
<name sortKey="Webb, Ca" uniqKey="Webb C">CA Webb</name>
</author>
<author>
<name sortKey="Smith, Sm" uniqKey="Smith S">SM Smith</name>
</author>
<author>
<name sortKey="Sun, Q" uniqKey="Sun Q">Q Sun</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Noel, L" uniqKey="Noel L">L Noel</name>
</author>
<author>
<name sortKey="Moores, Tl" uniqKey="Moores T">TL Moores</name>
</author>
<author>
<name sortKey="Van Der Biezen, Ea" uniqKey="Van Der Biezen E">EA van der Biezen</name>
</author>
<author>
<name sortKey="Parniske, M" uniqKey="Parniske M">M Parniske</name>
</author>
<author>
<name sortKey="Daniels, Mj" uniqKey="Daniels M">MJ Daniels</name>
</author>
<author>
<name sortKey="Parker, Je" uniqKey="Parker J">JE Parker</name>
</author>
<author>
<name sortKey="Jones, Jdg" uniqKey="Jones J">JDG Jones</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Paal, J" uniqKey="Paal J">J Paal</name>
</author>
<author>
<name sortKey="Henselewski, H" uniqKey="Henselewski H">H Henselewski</name>
</author>
<author>
<name sortKey="Muth, J" uniqKey="Muth J">J Muth</name>
</author>
<author>
<name sortKey="Meksem, K" uniqKey="Meksem K">K Meksem</name>
</author>
<author>
<name sortKey="Menendez, Cm" uniqKey="Menendez C">CM Menendez</name>
</author>
<author>
<name sortKey="Salamini, F" uniqKey="Salamini F">F Salamini</name>
</author>
<author>
<name sortKey="Ballvora, A" uniqKey="Ballvora A">A Ballvora</name>
</author>
<author>
<name sortKey="Gebhardt, C" uniqKey="Gebhardt C">C Gebhardt</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Claverie, M" uniqKey="Claverie M">M Claverie</name>
</author>
<author>
<name sortKey="Dirlewanger, E" uniqKey="Dirlewanger E">E Dirlewanger</name>
</author>
<author>
<name sortKey="Bosselut, N" uniqKey="Bosselut N">N Bosselut</name>
</author>
<author>
<name sortKey="Van Ghelder, C" uniqKey="Van Ghelder C">C Van Ghelder</name>
</author>
<author>
<name sortKey="Voisin, R" uniqKey="Voisin R">R Voisin</name>
</author>
<author>
<name sortKey="Kleinhentz, M" uniqKey="Kleinhentz M">M Kleinhentz</name>
</author>
<author>
<name sortKey="Lafargue, B" uniqKey="Lafargue B">B Lafargue</name>
</author>
<author>
<name sortKey="Abad, P" uniqKey="Abad P">P Abad</name>
</author>
<author>
<name sortKey="Rosso, Mn" uniqKey="Rosso M">MN Rosso</name>
</author>
<author>
<name sortKey="Chalhoub, B" uniqKey="Chalhoub B">B Chalhoub</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Lawrence, Gj" uniqKey="Lawrence G">GJ Lawrence</name>
</author>
<author>
<name sortKey="Finnegan, Ej" uniqKey="Finnegan E">EJ Finnegan</name>
</author>
<author>
<name sortKey="Ayliffe, Ma" uniqKey="Ayliffe M">MA Ayliffe</name>
</author>
<author>
<name sortKey="Ellis, Jg" uniqKey="Ellis J">JG Ellis</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Dinesh Kumar, Sp" uniqKey="Dinesh Kumar S">SP Dinesh-Kumar</name>
</author>
<author>
<name sortKey="Tham, Wh" uniqKey="Tham W">WH Tham</name>
</author>
<author>
<name sortKey="Baker, Bj" uniqKey="Baker B">BJ Baker</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Hinsch, M" uniqKey="Hinsch M">M Hinsch</name>
</author>
<author>
<name sortKey="Staskawicz, B" uniqKey="Staskawicz B">B Staskawicz</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Ellis, Jg" uniqKey="Ellis J">JG Ellis</name>
</author>
<author>
<name sortKey="Lawrence, Gj" uniqKey="Lawrence G">GJ Lawrence</name>
</author>
<author>
<name sortKey="Luck, Je" uniqKey="Luck J">JE Luck</name>
</author>
<author>
<name sortKey="Dodds, Pn" uniqKey="Dodds P">PN Dodds</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Mestre, P" uniqKey="Mestre P">P Mestre</name>
</author>
<author>
<name sortKey="Baulcombe, Dc" uniqKey="Baulcombe D">DC Baulcombe</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Takken, Flw" uniqKey="Takken F">FLW Takken</name>
</author>
<author>
<name sortKey="Goverse, A" uniqKey="Goverse A">A Goverse</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Mchale, L" uniqKey="Mchale L">L McHale</name>
</author>
<author>
<name sortKey="Tan, Xp" uniqKey="Tan X">XP Tan</name>
</author>
<author>
<name sortKey="Koehl, P" uniqKey="Koehl P">P Koehl</name>
</author>
<author>
<name sortKey="Michelmore, Rw" uniqKey="Michelmore R">RW Michelmore</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Belkhadir, Y" uniqKey="Belkhadir Y">Y Belkhadir</name>
</author>
<author>
<name sortKey="Subramaniam, R" uniqKey="Subramaniam R">R Subramaniam</name>
</author>
<author>
<name sortKey="Dangl, Jl" uniqKey="Dangl J">JL Dangl</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Dodds, Pn" uniqKey="Dodds P">PN Dodds</name>
</author>
<author>
<name sortKey="Lawrence, Gj" uniqKey="Lawrence G">GJ Lawrence</name>
</author>
<author>
<name sortKey="Ellis, Jg" uniqKey="Ellis J">JG Ellis</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Ellis, Jg" uniqKey="Ellis J">JG Ellis</name>
</author>
<author>
<name sortKey="Dodds, Pn" uniqKey="Dodds P">PN Dodds</name>
</author>
<author>
<name sortKey="Lawrence, Gj" uniqKey="Lawrence G">GJ Lawrence</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Bryan, Gt" uniqKey="Bryan G">GT Bryan</name>
</author>
<author>
<name sortKey="Wu, Ks" uniqKey="Wu K">KS Wu</name>
</author>
<author>
<name sortKey="Farrall, L" uniqKey="Farrall L">L Farrall</name>
</author>
<author>
<name sortKey="Jia, Yl" uniqKey="Jia Y">YL Jia</name>
</author>
<author>
<name sortKey="Hershey, Hp" uniqKey="Hershey H">HP Hershey</name>
</author>
<author>
<name sortKey="Mcadams, Sa" uniqKey="Mcadams S">SA McAdams</name>
</author>
<author>
<name sortKey="Faulk, Kn" uniqKey="Faulk K">KN Faulk</name>
</author>
<author>
<name sortKey="Donaldson, Gk" uniqKey="Donaldson G">GK Donaldson</name>
</author>
<author>
<name sortKey="Tarchini, R" uniqKey="Tarchini R">R Tarchini</name>
</author>
<author>
<name sortKey="Valent, B" uniqKey="Valent B">B Valent</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Van Der Hoorn, Ral" uniqKey="Van Der Hoorn R">RAL van der Hoorn</name>
</author>
<author>
<name sortKey="Kamoun, S" uniqKey="Kamoun S">S Kamoun</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Collier, Sm" uniqKey="Collier S">SM Collier</name>
</author>
<author>
<name sortKey="Moffett, P" uniqKey="Moffett P">P Moffett</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Dodds, Pn" uniqKey="Dodds P">PN Dodds</name>
</author>
<author>
<name sortKey="Rathjen, Jp" uniqKey="Rathjen J">JP Rathjen</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Cesari, S" uniqKey="Cesari S">S Cesari</name>
</author>
<author>
<name sortKey="Bernoux, M" uniqKey="Bernoux M">M Bernoux</name>
</author>
<author>
<name sortKey="Moncuquet, P" uniqKey="Moncuquet P">P Moncuquet</name>
</author>
<author>
<name sortKey="Kroj, T" uniqKey="Kroj T">T Kroj</name>
</author>
<author>
<name sortKey="Dodds, Pn" uniqKey="Dodds P">PN Dodds</name>
</author>
</analytic>
</biblStruct>
<biblStruct></biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Wirthmueller, L" uniqKey="Wirthmueller L">L Wirthmueller</name>
</author>
<author>
<name sortKey="Zhang, Y" uniqKey="Zhang Y">Y Zhang</name>
</author>
<author>
<name sortKey="Jones, Jdg" uniqKey="Jones J">JDG Jones</name>
</author>
<author>
<name sortKey="Parker, Je" uniqKey="Parker J">JE Parker</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Deslandes, L" uniqKey="Deslandes L">L Deslandes</name>
</author>
<author>
<name sortKey="Olivier, J" uniqKey="Olivier J">J Olivier</name>
</author>
<author>
<name sortKey="Theulieres, F" uniqKey="Theulieres F">F Theulieres</name>
</author>
<author>
<name sortKey="Hirsch, J" uniqKey="Hirsch J">J Hirsch</name>
</author>
<author>
<name sortKey="Feng, Dx" uniqKey="Feng D">DX Feng</name>
</author>
<author>
<name sortKey="Bittner Eddy, P" uniqKey="Bittner Eddy P">P Bittner-Eddy</name>
</author>
<author>
<name sortKey="Beynon, J" uniqKey="Beynon J">J Beynon</name>
</author>
<author>
<name sortKey="Marco, Y" uniqKey="Marco Y">Y Marco</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Noutoshi, Y" uniqKey="Noutoshi Y">Y Noutoshi</name>
</author>
<author>
<name sortKey="Ito, T" uniqKey="Ito T">T Ito</name>
</author>
<author>
<name sortKey="Seki, M" uniqKey="Seki M">M Seki</name>
</author>
<author>
<name sortKey="Nakashita, H" uniqKey="Nakashita H">H Nakashita</name>
</author>
<author>
<name sortKey="Yoshida, S" uniqKey="Yoshida S">S Yoshida</name>
</author>
<author>
<name sortKey="Marco, Y" uniqKey="Marco Y">Y Marco</name>
</author>
<author>
<name sortKey="Shirasu, K" uniqKey="Shirasu K">K Shirasu</name>
</author>
<author>
<name sortKey="Shinozaki, K" uniqKey="Shinozaki K">K Shinozaki</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Verde, I" uniqKey="Verde I">I Verde</name>
</author>
<author>
<name sortKey="Abbott, Ag" uniqKey="Abbott A">AG Abbott</name>
</author>
<author>
<name sortKey="Scalabrin, S" uniqKey="Scalabrin S">S Scalabrin</name>
</author>
<author>
<name sortKey="Jung, S" uniqKey="Jung S">S Jung</name>
</author>
<author>
<name sortKey="Shu, S" uniqKey="Shu S">S Shu</name>
</author>
<author>
<name sortKey="Marroni, F" uniqKey="Marroni F">F Marroni</name>
</author>
<author>
<name sortKey="Zhebentyayeva, T" uniqKey="Zhebentyayeva T">T Zhebentyayeva</name>
</author>
<author>
<name sortKey="Dettori, Mt" uniqKey="Dettori M">MT Dettori</name>
</author>
<author>
<name sortKey="Grimwood, J" uniqKey="Grimwood J">J Grimwood</name>
</author>
<author>
<name sortKey="Cattonaro, F" uniqKey="Cattonaro F">F Cattonaro</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Solovyev, V" uniqKey="Solovyev V">V Solovyev</name>
</author>
<author>
<name sortKey="Kosarev, P" uniqKey="Kosarev P">P Kosarev</name>
</author>
<author>
<name sortKey="Seledsov, I" uniqKey="Seledsov I">I Seledsov</name>
</author>
<author>
<name sortKey="Vorobyev, D" uniqKey="Vorobyev D">D Vorobyev</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Zdobnov, Em" uniqKey="Zdobnov E">EM Zdobnov</name>
</author>
<author>
<name sortKey="Apweiler, R" uniqKey="Apweiler R">R Apweiler</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Schornack, S" uniqKey="Schornack S">S Schornack</name>
</author>
<author>
<name sortKey="Ballvora, A" uniqKey="Ballvora A">A Ballvora</name>
</author>
<author>
<name sortKey="Gurlebeck, D" uniqKey="Gurlebeck D">D Gurlebeck</name>
</author>
<author>
<name sortKey="Peart, J" uniqKey="Peart J">J Peart</name>
</author>
<author>
<name sortKey="Ganal, M" uniqKey="Ganal M">M Ganal</name>
</author>
<author>
<name sortKey="Baker, B" uniqKey="Baker B">B Baker</name>
</author>
<author>
<name sortKey="Bonas, U" uniqKey="Bonas U">U Bonas</name>
</author>
<author>
<name sortKey="Lahaye, T" uniqKey="Lahaye T">T Lahaye</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Gassmann, W" uniqKey="Gassmann W">W Gassmann</name>
</author>
<author>
<name sortKey="Hinsch, Me" uniqKey="Hinsch M">ME Hinsch</name>
</author>
<author>
<name sortKey="Staskawicz, Bj" uniqKey="Staskawicz B">BJ Staskawicz</name>
</author>
</analytic>
</biblStruct>
<biblStruct></biblStruct>
<biblStruct></biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Velasco, R" uniqKey="Velasco R">R Velasco</name>
</author>
<author>
<name sortKey="Zharkikh, A" uniqKey="Zharkikh A">A Zharkikh</name>
</author>
<author>
<name sortKey="Troggio, M" uniqKey="Troggio M">M Troggio</name>
</author>
<author>
<name sortKey="Cartwright, Da" uniqKey="Cartwright D">DA Cartwright</name>
</author>
<author>
<name sortKey="Cestaro, A" uniqKey="Cestaro A">A Cestaro</name>
</author>
<author>
<name sortKey="Pruss, D" uniqKey="Pruss D">D Pruss</name>
</author>
<author>
<name sortKey="Pindo, M" uniqKey="Pindo M">M Pindo</name>
</author>
<author>
<name sortKey="Fitzgerald, Lm" uniqKey="Fitzgerald L">LM FitzGerald</name>
</author>
<author>
<name sortKey="Vezzulli, S" uniqKey="Vezzulli S">S Vezzulli</name>
</author>
<author>
<name sortKey="Reid, J" uniqKey="Reid J">J Reid</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Marone, D" uniqKey="Marone D">D Marone</name>
</author>
<author>
<name sortKey="Russo, Ma" uniqKey="Russo M">MA Russo</name>
</author>
<author>
<name sortKey="Laido, G" uniqKey="Laido G">G Laido</name>
</author>
<author>
<name sortKey="De Leonardis, Am" uniqKey="De Leonardis A">AM De Leonardis</name>
</author>
<author>
<name sortKey="Mastrangelo, Am" uniqKey="Mastrangelo A">AM Mastrangelo</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Deslandes, L" uniqKey="Deslandes L">L Deslandes</name>
</author>
<author>
<name sortKey="Olivier, J" uniqKey="Olivier J">J Olivier</name>
</author>
<author>
<name sortKey="Peeters, N" uniqKey="Peeters N">N Peeters</name>
</author>
<author>
<name sortKey="Feng, Dx" uniqKey="Feng D">DX Feng</name>
</author>
<author>
<name sortKey="Khounlotham, M" uniqKey="Khounlotham M">M Khounlotham</name>
</author>
<author>
<name sortKey="Boucher, C" uniqKey="Boucher C">C Boucher</name>
</author>
<author>
<name sortKey="Somssich, I" uniqKey="Somssich I">I Somssich</name>
</author>
<author>
<name sortKey="Genin, S" uniqKey="Genin S">S Genin</name>
</author>
<author>
<name sortKey="Marco, Y" uniqKey="Marco Y">Y Marco</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Potter, D" uniqKey="Potter D">D Potter</name>
</author>
<author>
<name sortKey="Eriksson, T" uniqKey="Eriksson T">T Eriksson</name>
</author>
<author>
<name sortKey="Evans, Rc" uniqKey="Evans R">RC Evans</name>
</author>
<author>
<name sortKey="Oh, S" uniqKey="Oh S">S Oh</name>
</author>
<author>
<name sortKey="Smedmark, Jee" uniqKey="Smedmark J">JEE Smedmark</name>
</author>
<author>
<name sortKey="Morgan, Dr" uniqKey="Morgan D">DR Morgan</name>
</author>
<author>
<name sortKey="Kerr, M" uniqKey="Kerr M">M Kerr</name>
</author>
<author>
<name sortKey="Robertson, Kr" uniqKey="Robertson K">KR Robertson</name>
</author>
<author>
<name sortKey="Arsenault, M" uniqKey="Arsenault M">M Arsenault</name>
</author>
<author>
<name sortKey="Dickinson, Ta" uniqKey="Dickinson T">TA Dickinson</name>
</author>
</analytic>
</biblStruct>
<biblStruct></biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Dixon, Ms" uniqKey="Dixon M">MS Dixon</name>
</author>
<author>
<name sortKey="Jones, Da" uniqKey="Jones D">DA Jones</name>
</author>
<author>
<name sortKey="Keddie, Js" uniqKey="Keddie J">JS Keddie</name>
</author>
<author>
<name sortKey="Thomas, Cm" uniqKey="Thomas C">CM Thomas</name>
</author>
<author>
<name sortKey="Harrison, K" uniqKey="Harrison K">K Harrison</name>
</author>
<author>
<name sortKey="Jones, Jdg" uniqKey="Jones J">JDG Jones</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Song, Wy" uniqKey="Song W">WY Song</name>
</author>
<author>
<name sortKey="Wang, Gl" uniqKey="Wang G">GL Wang</name>
</author>
<author>
<name sortKey="Chen, Ll" uniqKey="Chen L">LL Chen</name>
</author>
<author>
<name sortKey="Kim, Hs" uniqKey="Kim H">HS Kim</name>
</author>
<author>
<name sortKey="Pi, Ly" uniqKey="Pi L">LY Pi</name>
</author>
<author>
<name sortKey="Holsten, T" uniqKey="Holsten T">T Holsten</name>
</author>
<author>
<name sortKey="Gardner, J" uniqKey="Gardner J">J Gardner</name>
</author>
<author>
<name sortKey="Wang, B" uniqKey="Wang B">B Wang</name>
</author>
<author>
<name sortKey="Zhai, Wx" uniqKey="Zhai W">WX Zhai</name>
</author>
<author>
<name sortKey="Zhu, Lh" uniqKey="Zhu L">LH Zhu</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Milligan, Sb" uniqKey="Milligan S">SB Milligan</name>
</author>
<author>
<name sortKey="Bodeau, J" uniqKey="Bodeau J">J Bodeau</name>
</author>
<author>
<name sortKey="Yaghoobi, J" uniqKey="Yaghoobi J">J Yaghoobi</name>
</author>
<author>
<name sortKey="Kaloshian, I" uniqKey="Kaloshian I">I Kaloshian</name>
</author>
<author>
<name sortKey="Zabel, P" uniqKey="Zabel P">P Zabel</name>
</author>
<author>
<name sortKey="Williamson, Vm" uniqKey="Williamson V">VM Williamson</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Cesari, S" uniqKey="Cesari S">S Cesari</name>
</author>
<author>
<name sortKey="Thilliez, G" uniqKey="Thilliez G">G Thilliez</name>
</author>
<author>
<name sortKey="Ribot, C" uniqKey="Ribot C">C Ribot</name>
</author>
<author>
<name sortKey="Chalvon, V" uniqKey="Chalvon V">V Chalvon</name>
</author>
<author>
<name sortKey="Michel, C" uniqKey="Michel C">C Michel</name>
</author>
<author>
<name sortKey="Jauneau, A" uniqKey="Jauneau A">A Jauneau</name>
</author>
<author>
<name sortKey="Rivas, S" uniqKey="Rivas S">S Rivas</name>
</author>
<author>
<name sortKey="Alaux, L" uniqKey="Alaux L">L Alaux</name>
</author>
<author>
<name sortKey="Kanzaki, H" uniqKey="Kanzaki H">H Kanzaki</name>
</author>
<author>
<name sortKey="Okuyama, Y" uniqKey="Okuyama Y">Y Okuyama</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Sudol, M" uniqKey="Sudol M">M Sudol</name>
</author>
<author>
<name sortKey="Chen, Hi" uniqKey="Chen H">HI Chen</name>
</author>
<author>
<name sortKey="Bougeret, C" uniqKey="Bougeret C">C Bougeret</name>
</author>
<author>
<name sortKey="Einbond, A" uniqKey="Einbond A">A Einbond</name>
</author>
<author>
<name sortKey="Bork, P" uniqKey="Bork P">P Bork</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Luck, Je" uniqKey="Luck J">JE Luck</name>
</author>
<author>
<name sortKey="Lawrence, Gj" uniqKey="Lawrence G">GJ Lawrence</name>
</author>
<author>
<name sortKey="Dodds, Pn" uniqKey="Dodds P">PN Dodds</name>
</author>
<author>
<name sortKey="Shepherd, Kw" uniqKey="Shepherd K">KW Shepherd</name>
</author>
<author>
<name sortKey="Ellis, Jg" uniqKey="Ellis J">JG Ellis</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Le Roux, C" uniqKey="Le Roux C">C Le Roux</name>
</author>
<author>
<name sortKey="Huet, G" uniqKey="Huet G">G Huet</name>
</author>
<author>
<name sortKey="Jauneau, A" uniqKey="Jauneau A">A Jauneau</name>
</author>
<author>
<name sortKey="Camborde, L" uniqKey="Camborde L">L Camborde</name>
</author>
<author>
<name sortKey="Tremousaygue, D" uniqKey="Tremousaygue D">D Tremousaygue</name>
</author>
<author>
<name sortKey="Kraut, A" uniqKey="Kraut A">A Kraut</name>
</author>
<author>
<name sortKey="Zhou, B" uniqKey="Zhou B">B Zhou</name>
</author>
<author>
<name sortKey="Levaillant, M" uniqKey="Levaillant M">M Levaillant</name>
</author>
<author>
<name sortKey="Adachi, H" uniqKey="Adachi H">H Adachi</name>
</author>
<author>
<name sortKey="Yoshioka, H" uniqKey="Yoshioka H">H Yoshioka</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Sarris, Pf" uniqKey="Sarris P">PF Sarris</name>
</author>
<author>
<name sortKey="Duxbury, Z" uniqKey="Duxbury Z">Z Duxbury</name>
</author>
<author>
<name sortKey="Huh, Su" uniqKey="Huh S">SU Huh</name>
</author>
<author>
<name sortKey="Ma, Y" uniqKey="Ma Y">Y Ma</name>
</author>
<author>
<name sortKey="Segonzac, C" uniqKey="Segonzac C">C Segonzac</name>
</author>
<author>
<name sortKey="Sklenar, J" uniqKey="Sklenar J">J Sklenar</name>
</author>
<author>
<name sortKey="Derbyshire, P" uniqKey="Derbyshire P">P Derbyshire</name>
</author>
<author>
<name sortKey="Cevik, V" uniqKey="Cevik V">V Cevik</name>
</author>
<author>
<name sortKey="Rallapalli, G" uniqKey="Rallapalli G">G Rallapalli</name>
</author>
<author>
<name sortKey="Saucet, Sb" uniqKey="Saucet S">SB Saucet</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Esmenjaud, D" uniqKey="Esmenjaud D">D Esmenjaud</name>
</author>
<author>
<name sortKey="Voisin, R" uniqKey="Voisin R">R Voisin</name>
</author>
<author>
<name sortKey="Van Ghelder, C" uniqKey="Van Ghelder C">C Van Ghelder</name>
</author>
<author>
<name sortKey="Bosselut, N" uniqKey="Bosselut N">N Bosselut</name>
</author>
<author>
<name sortKey="Lafargue, B" uniqKey="Lafargue B">B Lafargue</name>
</author>
<author>
<name sortKey="Di Vito, M" uniqKey="Di Vito M">M Di Vito</name>
</author>
<author>
<name sortKey="Dirlewanger, E" uniqKey="Dirlewanger E">E Dirlewanger</name>
</author>
<author>
<name sortKey="Poessel, Jl" uniqKey="Poessel J">JL Poessel</name>
</author>
<author>
<name sortKey="Kleinhentz, M" uniqKey="Kleinhentz M">M Kleinhentz</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Van Ghelder, C" uniqKey="Van Ghelder C">C Van Ghelder</name>
</author>
<author>
<name sortKey="Lafargue, B" uniqKey="Lafargue B">B Lafargue</name>
</author>
<author>
<name sortKey="Dirlewanger, E" uniqKey="Dirlewanger E">E Dirlewanger</name>
</author>
<author>
<name sortKey="Ouassa, A" uniqKey="Ouassa A">A Ouassa</name>
</author>
<author>
<name sortKey="Voisin, R" uniqKey="Voisin R">R Voisin</name>
</author>
<author>
<name sortKey="Polidori, J" uniqKey="Polidori J">J Polidori</name>
</author>
<author>
<name sortKey="Kleinhentz, M" uniqKey="Kleinhentz M">M Kleinhentz</name>
</author>
<author>
<name sortKey="Esmenjaud, D" uniqKey="Esmenjaud D">D Esmenjaud</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Bendahmane, A" uniqKey="Bendahmane A">A Bendahmane</name>
</author>
<author>
<name sortKey="Farnham, G" uniqKey="Farnham G">G Farnham</name>
</author>
<author>
<name sortKey="Moffett, P" uniqKey="Moffett P">P Moffett</name>
</author>
<author>
<name sortKey="Baulcombe, Dc" uniqKey="Baulcombe D">DC Baulcombe</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Whitham, S" uniqKey="Whitham S">S Whitham</name>
</author>
<author>
<name sortKey="Dineshkumar, Sp" uniqKey="Dineshkumar S">SP Dineshkumar</name>
</author>
<author>
<name sortKey="Choi, D" uniqKey="Choi D">D Choi</name>
</author>
<author>
<name sortKey="Hehl, R" uniqKey="Hehl R">R Hehl</name>
</author>
<author>
<name sortKey="Corr, C" uniqKey="Corr C">C Corr</name>
</author>
<author>
<name sortKey="Baker, B" uniqKey="Baker B">B Baker</name>
</author>
</analytic>
</biblStruct>
<biblStruct></biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Ameline Torregrosa, C" uniqKey="Ameline Torregrosa C">C Ameline-Torregrosa</name>
</author>
<author>
<name sortKey="Wang, B B" uniqKey="Wang B">B-B Wang</name>
</author>
<author>
<name sortKey="O Leness, Ms" uniqKey="O Leness M">MS O’Bleness</name>
</author>
<author>
<name sortKey="Deshpande, S" uniqKey="Deshpande S">S Deshpande</name>
</author>
<author>
<name sortKey="Zhu, H" uniqKey="Zhu H">H Zhu</name>
</author>
<author>
<name sortKey="Roe, B" uniqKey="Roe B">B Roe</name>
</author>
<author>
<name sortKey="Young, Nd" uniqKey="Young N">ND Young</name>
</author>
<author>
<name sortKey="Cannon, Sb" uniqKey="Cannon S">SB Cannon</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Shang, J" uniqKey="Shang J">J Shang</name>
</author>
<author>
<name sortKey="Tao, Y" uniqKey="Tao Y">Y Tao</name>
</author>
<author>
<name sortKey="Chen, X" uniqKey="Chen X">X Chen</name>
</author>
<author>
<name sortKey="Zou, Y" uniqKey="Zou Y">Y Zou</name>
</author>
<author>
<name sortKey="Lei, C" uniqKey="Lei C">C Lei</name>
</author>
<author>
<name sortKey="Wang, J" uniqKey="Wang J">J Wang</name>
</author>
<author>
<name sortKey="Li, X" uniqKey="Li X">X Li</name>
</author>
<author>
<name sortKey="Zhao, X" uniqKey="Zhao X">X Zhao</name>
</author>
<author>
<name sortKey="Zhang, M" uniqKey="Zhang M">M Zhang</name>
</author>
<author>
<name sortKey="Lu, Z" uniqKey="Lu Z">Z Lu</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Cheng, X" uniqKey="Cheng X">X Cheng</name>
</author>
<author>
<name sortKey="Hang, H" uniqKey="Hang H">H Hang</name>
</author>
<author>
<name sortKey="Zhao, Y" uniqKey="Zhao Y">Y Zhao</name>
</author>
<author>
<name sortKey="Qian, Y" uniqKey="Qian Y">Y Qian</name>
</author>
<author>
<name sortKey="Zhu, S" uniqKey="Zhu S">S Zhu</name>
</author>
<author>
<name sortKey="Cheng, B" uniqKey="Cheng B">B Cheng</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Cheng, Y" uniqKey="Cheng Y">Y Cheng</name>
</author>
<author>
<name sortKey="Li, X" uniqKey="Li X">X Li</name>
</author>
<author>
<name sortKey="Jiang, H" uniqKey="Jiang H">H Jiang</name>
</author>
<author>
<name sortKey="Ma, W" uniqKey="Ma W">W Ma</name>
</author>
<author>
<name sortKey="Miao, W" uniqKey="Miao W">W Miao</name>
</author>
<author>
<name sortKey="Yamada, T" uniqKey="Yamada T">T Yamada</name>
</author>
<author>
<name sortKey="Zhang, M" uniqKey="Zhang M">M Zhang</name>
</author>
</analytic>
</biblStruct>
</listBibl>
</div1>
</back>
</TEI>
<pmc article-type="research-article">
<pmc-dir>properties open_access</pmc-dir>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">BMC Genomics</journal-id>
<journal-id journal-id-type="iso-abbrev">BMC Genomics</journal-id>
<journal-title-group>
<journal-title>BMC Genomics</journal-title>
</journal-title-group>
<issn pub-type="epub">1471-2164</issn>
<publisher>
<publisher-name>BioMed Central</publisher-name>
<publisher-loc>London</publisher-loc>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">27129402</article-id>
<article-id pub-id-type="pmc">4851768</article-id>
<article-id pub-id-type="publisher-id">2635</article-id>
<article-id pub-id-type="doi">10.1186/s12864-016-2635-0</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Research Article</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>TNL genes in peach: insights into the post-LRR domain</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Van Ghelder</surname>
<given-names>Cyril</given-names>
</name>
<address>
<email>Cyril.Van-Ghelder@paca.inra.fr</email>
</address>
<xref ref-type="aff" rid="Aff1"></xref>
<xref ref-type="aff" rid="Aff2"></xref>
<xref ref-type="aff" rid="Aff3"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Esmenjaud</surname>
<given-names>Daniel</given-names>
</name>
<xref ref-type="aff" rid="Aff1"></xref>
<xref ref-type="aff" rid="Aff2"></xref>
<xref ref-type="aff" rid="Aff3"></xref>
</contrib>
<aff id="Aff1">
<label></label>
INRA, UMR 1355 Institut Sophia Agrobiotech, 06900 Sophia Antipolis, France</aff>
<aff id="Aff2">
<label></label>
University Nice Sophia Antipolis, UMR 7254 Institut Sophia Agrobiotech, 06900 Sophia Antipolis, France</aff>
<aff id="Aff3">
<label></label>
CNRS, UMR 7254 Institut Sophia Agrobiotech, 06900 Sophia Antipolis, France</aff>
</contrib-group>
<pub-date pub-type="epub">
<day>30</day>
<month>4</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="pmc-release">
<day>30</day>
<month>4</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="collection">
<year>2016</year>
</pub-date>
<volume>17</volume>
<elocation-id>317</elocation-id>
<history>
<date date-type="received">
<day>29</day>
<month>10</month>
<year>2015</year>
</date>
<date date-type="accepted">
<day>22</day>
<month>4</month>
<year>2016</year>
</date>
</history>
<permissions>
<copyright-statement>© Van Ghelder and Esmenjaud. 2016</copyright-statement>
<license license-type="OpenAccess">
<license-p>
<bold>Open Access</bold>
This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (
<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>
), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (
<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/publicdomain/zero/1.0/">http://creativecommons.org/publicdomain/zero/1.0/</ext-link>
) applies to the data made available in this article, unless otherwise stated.</license-p>
</license>
</permissions>
<abstract id="Abs1">
<sec>
<title>Background</title>
<p>Plants develop sustainable defence responses to pathogen attacks through resistance (
<italic>R</italic>
) genes contributing to effector-triggered immunity (ETI). TIR-NB-LRR genes (TNL genes) constitute a major family of ETI
<italic>R</italic>
genes in dicots. The putative functions or roles of the TIR, NB and LRR domains of the proteins they encode (TNLs) are well documented, but TNLs also have a poorly characterised C-terminal region, the function of which is unknown in most cases. We characterised this prevalent stress-response protein family in a perennial plant, using the genome of peach (
<italic>Prunus persica</italic>
), the model
<italic>Prunus</italic>
species. The first TNL gene from this genus to be cloned, the
<italic>Ma</italic>
gene, confers complete-spectrum resistance to root-knot nematodes (RKNs) and encodes a protein with a huge C-terminal region with five duplicated post-LRR (PL) domains. This gene was the cornerstone of this study.</p>
</sec>
<sec>
<title>Results</title>
<p>We investigated the role of this C-terminal region, by first describing the frequency, distribution and structural characteristics of i) TNL genes and ii) their PL domains in the peach genome, using the v1.0 Sanger sequence together with the v2.0 sequence, which has better genome annotation due to the incorporation of transcriptomic data. We detected 195 predicted TNL genes from the eight peach chromosomes: 85 % of these genes mapped to chromosomes 1, 2, 7 and 8. We reconstructed the putative structure of the predicted exons of all the TNL genes identified, and it was possible to retrieve the PL domains among two thirds of the TNL genes. We used our predicted TNL gene sequences to develop an annotation file for use with the Gbrowse tool in the v2.0 genome. The use of these annotation data made it possible to detect transcribed PL sequences in two
<italic>Prunus</italic>
species. We then used consensus sequences defined on the basis of 124 PL domains to design specific motifs, and we found that the use of these motifs significantly increased the numbers of PL domains and correlative TNL genes detected in diverse dicot genomes. Based on PL signatures, we showed that TNL genes with multiple PL domains were rare in peach and the other plants screened. The five-PL domain pattern is probably unique to
<italic>Ma</italic>
and its orthologues within
<italic>Prunus</italic>
and closely related genera from the Rosaceae and was probably inherited from the common ancestor of these plants in the subfamily Spiraeoideae.</p>
</sec>
<sec>
<title>Conclusions</title>
<p>The first physical TNL gene map for
<italic>Prunus</italic>
species can be used for the further investigation of
<italic>R</italic>
genes in this genus. The PL signature motifs are a complementary tool for the detection of TNL
<italic>R</italic>
genes in dicots. The low degree of similarity between PL domains and the neighbouring LRR exons and the specificity of PL signature motifs suggest that PL and LRR domains have different origins, with PL domains being specific to TNL genes, and possibly essential to the functioning of these genes in some cases. Investigations of the role of the oversized
<italic>Ma</italic>
PL region, in ligand binding or intramolecular interactions for example, may help to enrich our understanding of NB-LRR-mediated plant immunity to RKNs.</p>
</sec>
<sec>
<title>Electronic supplementary material</title>
<p>The online version of this article (doi:10.1186/s12864-016-2635-0) contains supplementary material, which is available to authorized users.</p>
</sec>
</abstract>
<kwd-group xml:lang="en">
<title>Keywords</title>
<kwd>TIR-NB-LRR</kwd>
<kwd>Peach</kwd>
<kwd>Genome</kwd>
<kwd>
<italic>Prunus</italic>
</kwd>
<kwd>Resistance</kwd>
<kwd>Post-LRR domain</kwd>
<kwd>NB-LRR superfamily</kwd>
</kwd-group>
<custom-meta-group>
<custom-meta>
<meta-name>issue-copyright-statement</meta-name>
<meta-value>© The Author(s) 2016</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
</front>
</pmc>
<affiliations>
<list>
<country>
<li>France</li>
</country>
<region>
<li>Provence-Alpes-Côte d'Azur</li>
</region>
<settlement>
<li>Sophia Antipolis</li>
</settlement>
</list>
<tree>
<country name="France">
<region name="Provence-Alpes-Côte d'Azur">
<name sortKey="Van Ghelder, Cyril" sort="Van Ghelder, Cyril" uniqKey="Van Ghelder C" first="Cyril" last="Van Ghelder">Cyril Van Ghelder</name>
</region>
<name sortKey="Esmenjaud, Daniel" sort="Esmenjaud, Daniel" uniqKey="Esmenjaud D" first="Daniel" last="Esmenjaud">Daniel Esmenjaud</name>
<name sortKey="Esmenjaud, Daniel" sort="Esmenjaud, Daniel" uniqKey="Esmenjaud D" first="Daniel" last="Esmenjaud">Daniel Esmenjaud</name>
<name sortKey="Esmenjaud, Daniel" sort="Esmenjaud, Daniel" uniqKey="Esmenjaud D" first="Daniel" last="Esmenjaud">Daniel Esmenjaud</name>
<name sortKey="Van Ghelder, Cyril" sort="Van Ghelder, Cyril" uniqKey="Van Ghelder C" first="Cyril" last="Van Ghelder">Cyril Van Ghelder</name>
<name sortKey="Van Ghelder, Cyril" sort="Van Ghelder, Cyril" uniqKey="Van Ghelder C" first="Cyril" last="Van Ghelder">Cyril Van Ghelder</name>
</country>
</tree>
</affiliations>
</record>

Pour manipuler ce document sous Unix (Dilib)

EXPLOR_STEP=$WICRI_ROOT/Bois/explor/MelampsoraV2/Data/Ncbi/Merge
HfdSelect -h $EXPLOR_STEP/biblio.hfd -nk 000697 | SxmlIndent | more

Ou

HfdSelect -h $EXPLOR_AREA/Data/Ncbi/Merge/biblio.hfd -nk 000697 | SxmlIndent | more

Pour mettre un lien sur cette page dans le réseau Wicri

{{Explor lien
   |wiki=    Bois
   |area=    MelampsoraV2
   |flux=    Ncbi
   |étape=   Merge
   |type=    RBID
   |clé=     PMC:4851768
   |texte=   TNL genes in peach: insights into the post-LRR domain
}}

Pour générer des pages wiki

HfdIndexSelect -h $EXPLOR_AREA/Data/Ncbi/Merge/RBID.i   -Sk "pubmed:27129402" \
       | HfdSelect -Kh $EXPLOR_AREA/Data/Ncbi/Merge/biblio.hfd   \
       | NlmPubMed2Wicri -a MelampsoraV2 

Wicri

This area was generated with Dilib version V0.6.38.
Data generation: Tue Nov 24 19:18:52 2020. Site generation: Tue Nov 24 19:22:33 2020