Ma Orthologous Genes in Prunus spp. Shed Light on a Noteworthy NBS-LRR Cluster Conferring Differential Resistance to Root-Knot Nematodes

Root-knot nematodes (RKNs) are considerable polyphagous pests that severely challenge plants worldwide and especially perennials. The specific genetic resistance of plants mainly relies on the NBS-LRR genes that are pivotal factors for pathogens control. In Prunus spp., the Ma plum and RMja almond g...

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Main Authors: Cyril Van Ghelder, Daniel Esmenjaud, Caroline Callot, Emeric Dubois, Marianne Mazier, Henri Duval
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-09-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fpls.2018.01269/full
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spelling doaj-fb79a98d168d486b897acda2a473e0ff2020-11-24T20:56:03ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2018-09-01910.3389/fpls.2018.01269393556Ma Orthologous Genes in Prunus spp. Shed Light on a Noteworthy NBS-LRR Cluster Conferring Differential Resistance to Root-Knot NematodesCyril Van Ghelder0Daniel Esmenjaud1Caroline Callot2Emeric Dubois3Marianne Mazier4Henri Duval5Institut Sophia Agrobiotech, INRA, CNRS, Université Côte d’Azur, Sophia Antipolis, FranceInstitut Sophia Agrobiotech, INRA, CNRS, Université Côte d’Azur, Sophia Antipolis, FranceCentre National de Ressources Génomiques Végétales, INRA, CNRS, Université de Toulouse, Castanet-Tolosan, FranceMGX-Montpellier GenomiX, CNRS, Montpellier, FranceUnité de Génétique et Amélioration des Fruits et Légumes (GAFL), INRA, Montfavet, FranceUnité de Génétique et Amélioration des Fruits et Légumes (GAFL), INRA, Montfavet, FranceRoot-knot nematodes (RKNs) are considerable polyphagous pests that severely challenge plants worldwide and especially perennials. The specific genetic resistance of plants mainly relies on the NBS-LRR genes that are pivotal factors for pathogens control. In Prunus spp., the Ma plum and RMja almond genes possess different spectra for resistance to RKNs. While previous works based on the Ma gene allowed to clone it and to decipher its peculiar TIR-NBS-LRR (TNL) structure, we only knew that the RMja gene mapped on the same chromosome as Ma. We carried out a high-resolution mapping using an almond segregating F2 progeny of 1448 seedlings from resistant (R) and susceptible (S) parental accessions, to locate precisely RMja on the peach genome, the reference sequence for Prunus species. We showed that the RMja gene maps in the Ma resistance cluster and that the Ma ortholog is the best candidate for RMja. This co-localization is a crucial step that opens the way to unravel the molecular determinants involved in the resistance to RKNs. Then we sequenced both almond parental NGS genomes and aligned them onto the RKN susceptible reference peach genome. We produced a BAC library of the R parental accession and, from two overlapping BAC clones, we obtained a 336-kb sequence encompassing the RMja candidate region. Thus, we could benefit from three Ma orthologous regions to investigate their sequence polymorphism, respectively, within plum (complete R spectrum), almond (incomplete R spectrum) and peach (null R spectrum). We showed that the Ma TNL cluster has evolved orthologs with a unique conserved structure comprised of five repeated post-LRR (PL) domains, which contain most polymorphism. In addition to support the Ma and RMja orthologous relationship, our results suggest that the polymorphism contained in the PL sequences might underlie differential resistance interactions with RKNs and an original immune mechanism in woody perennials. Besides, our study illustrates how PL exon duplications and losses shape TNL structure and give rise to atypical PL domain repeats of yet unknown role.https://www.frontiersin.org/article/10.3389/fpls.2018.01269/fullalmondMeloidogynenucleotide-binding site - leucine-rich repeat (NBS-LRR)Prunusresistance generoot-knot nematodes (RKNs)
collection DOAJ
language English
format Article
sources DOAJ
author Cyril Van Ghelder
Daniel Esmenjaud
Caroline Callot
Emeric Dubois
Marianne Mazier
Henri Duval
spellingShingle Cyril Van Ghelder
Daniel Esmenjaud
Caroline Callot
Emeric Dubois
Marianne Mazier
Henri Duval
Ma Orthologous Genes in Prunus spp. Shed Light on a Noteworthy NBS-LRR Cluster Conferring Differential Resistance to Root-Knot Nematodes
Frontiers in Plant Science
almond
Meloidogyne
nucleotide-binding site - leucine-rich repeat (NBS-LRR)
Prunus
resistance gene
root-knot nematodes (RKNs)
author_facet Cyril Van Ghelder
Daniel Esmenjaud
Caroline Callot
Emeric Dubois
Marianne Mazier
Henri Duval
author_sort Cyril Van Ghelder
title Ma Orthologous Genes in Prunus spp. Shed Light on a Noteworthy NBS-LRR Cluster Conferring Differential Resistance to Root-Knot Nematodes
title_short Ma Orthologous Genes in Prunus spp. Shed Light on a Noteworthy NBS-LRR Cluster Conferring Differential Resistance to Root-Knot Nematodes
title_full Ma Orthologous Genes in Prunus spp. Shed Light on a Noteworthy NBS-LRR Cluster Conferring Differential Resistance to Root-Knot Nematodes
title_fullStr Ma Orthologous Genes in Prunus spp. Shed Light on a Noteworthy NBS-LRR Cluster Conferring Differential Resistance to Root-Knot Nematodes
title_full_unstemmed Ma Orthologous Genes in Prunus spp. Shed Light on a Noteworthy NBS-LRR Cluster Conferring Differential Resistance to Root-Knot Nematodes
title_sort ma orthologous genes in prunus spp. shed light on a noteworthy nbs-lrr cluster conferring differential resistance to root-knot nematodes
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2018-09-01
description Root-knot nematodes (RKNs) are considerable polyphagous pests that severely challenge plants worldwide and especially perennials. The specific genetic resistance of plants mainly relies on the NBS-LRR genes that are pivotal factors for pathogens control. In Prunus spp., the Ma plum and RMja almond genes possess different spectra for resistance to RKNs. While previous works based on the Ma gene allowed to clone it and to decipher its peculiar TIR-NBS-LRR (TNL) structure, we only knew that the RMja gene mapped on the same chromosome as Ma. We carried out a high-resolution mapping using an almond segregating F2 progeny of 1448 seedlings from resistant (R) and susceptible (S) parental accessions, to locate precisely RMja on the peach genome, the reference sequence for Prunus species. We showed that the RMja gene maps in the Ma resistance cluster and that the Ma ortholog is the best candidate for RMja. This co-localization is a crucial step that opens the way to unravel the molecular determinants involved in the resistance to RKNs. Then we sequenced both almond parental NGS genomes and aligned them onto the RKN susceptible reference peach genome. We produced a BAC library of the R parental accession and, from two overlapping BAC clones, we obtained a 336-kb sequence encompassing the RMja candidate region. Thus, we could benefit from three Ma orthologous regions to investigate their sequence polymorphism, respectively, within plum (complete R spectrum), almond (incomplete R spectrum) and peach (null R spectrum). We showed that the Ma TNL cluster has evolved orthologs with a unique conserved structure comprised of five repeated post-LRR (PL) domains, which contain most polymorphism. In addition to support the Ma and RMja orthologous relationship, our results suggest that the polymorphism contained in the PL sequences might underlie differential resistance interactions with RKNs and an original immune mechanism in woody perennials. Besides, our study illustrates how PL exon duplications and losses shape TNL structure and give rise to atypical PL domain repeats of yet unknown role.
topic almond
Meloidogyne
nucleotide-binding site - leucine-rich repeat (NBS-LRR)
Prunus
resistance gene
root-knot nematodes (RKNs)
url https://www.frontiersin.org/article/10.3389/fpls.2018.01269/full
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