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NLR Gene Evolution in Plants
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NLR Gene Evolution in Plants

A special issue of Genes (ISSN 2073-4425). This special issue belongs to the section "Plant Genetics and Genomics".

Deadline for manuscript submissions: closed (24 January 2020) | Viewed by 23410

Special Issue Editors

Dr. Valérìe Geffroy

E-Mail Website
Guest Editor
Institute of Plant Sciences Paris Saclay (IPS2), INRAE, 91192 Gif sur Yvette CEDEX, France
Interests: disease resistance genes; NLR; legume; common bean; genomics
Dr. Patricia Faivre-Rampant

E-Mail
Co-Guest Editor
EPGV, INRA, Université Paris-Saclay, Evry, France

Special Issue Information

Dear Colleagues,

Disease resistance (R) genes are of major importance in crop breeding since they prevent potentially dramatic yield losses caused by plant pathogens and pests. The major class of R genes encodes nucleotide-binding and leucine-rich repeat immune receptors (NLRs) and corresponds to one of the largest and most diversified gene families in plant genomes. NLR act inside plant cells by recognizing directly or indirectly enemy molecules in order to activate defense response and stop the pathogen development. In turn, pathogens actively attempt to evade and interfere with plant response pathways, leading to a coevolutionary armrace between plants and pathogens. Consequently, plants need to maintain diversity at NLR genes to cope with an ever changing array of pathogens. NLR genes are often localized in complex clusters, a structural organization that may favour the dynamic evolution and diversification of NLRs to cope with fast-evolving pathogens.

This Special Issue focuses on the evolution of NLR genes in plants, and welcomes original research articles as well as review articles that summarize recent progress and discuss future needs/opportunities in a wide range of areas including, but not limited to, molecular breeding, comparative genomics, functional genomics, genetic/genomic diversity, genome-editing, NLR-engineering, and molecular evolution of NLR in plants.

Prof. Valérìe Geffroy
Dr. Patricia Faivre-Rampant
Guest Editor

Manuscript Submission Information

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Keywords

  • R genes
  • plants
  • disease resistance
  • plant-pathogen interaction
  • gene evolution

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Published Papers (5 papers)

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Research

28 pages, 2548 KiB  
Article
Comparative Genomics and Functional Studies of Wheat BED-NLR Loci
by Clemence Marchal, 10+ Wheat Genome Project, Georg Haberer, Manuel Spannagl and Cristobal Uauy
Genes 2020, 11(12), 1406; https://doi.org/10.3390/genes11121406 - 26 Nov 2020
Cited by 7 | Viewed by 3845
Abstract
Nucleotide-binding leucine-rich-repeat (LRR) receptors (NLRs) with non-canonical integrated domains (NLR-IDs) are widespread in plant genomes. Zinc-finger BED (named after the Drosophila proteins Boundary Element-Associated Factor and DNA Replication-related Element binding Factor, named BED hereafter) are among the most frequently found IDs. Five BED-NLRs [...] Read more.
Nucleotide-binding leucine-rich-repeat (LRR) receptors (NLRs) with non-canonical integrated domains (NLR-IDs) are widespread in plant genomes. Zinc-finger BED (named after the Drosophila proteins Boundary Element-Associated Factor and DNA Replication-related Element binding Factor, named BED hereafter) are among the most frequently found IDs. Five BED-NLRs conferring resistance against bacterial and fungal pathogens have been characterized. However, it is unknown whether BED-NLRs function in a manner similar to other NLR-IDs. Here, we used chromosome-level assemblies of wheat to explore the Yr7 and Yr5a genomic regions and show that, unlike known NLR-ID loci, there is no evidence for a NLR-partner in their vicinity. Using neighbor-network analyses, we observed that BED domains from BED-NLRs share more similarities with BED domains from single-BED proteins and from BED-containing proteins harboring domains that are conserved in transposases. We identified a nuclear localization signal (NLS) in Yr7, Yr5, and the other characterized BED-NLRs. We thus propose that this is a feature of BED-NLRs that confer resistance to plant pathogens. We show that the NLS was functional in truncated versions of the Yr7 protein when expressed in N. benthamiana. We did not observe cell-death upon the overexpression of Yr7 full-length, truncated, and ‘MHD’ variants in N. benthamiana. This suggests that either this system is not suitable to study BED-NLR signaling or that BED-NLRs require additional components to trigger cell death. These results define novel future directions to further understand the role of BED domains in BED-NLR mediated resistance. Full article
(This article belongs to the Special Issue NLR Gene Evolution in Plants)
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14 pages, 7538 KiB  
Article
Deciphering the Impact of a Bacterial Infection on Meiotic Recombination in Arabidopsis with Fluorescence Tagged Lines
by Ariane Gratias and Valérie Geffroy
Genes 2020, 11(7), 832; https://doi.org/10.3390/genes11070832 - 21 Jul 2020
Cited by 1 | Viewed by 3010
Abstract
Plants are under strong evolutionary pressure to maintain surveillance against pathogens. One major disease resistance mechanism is based on NB-LRR (NLR) proteins that specifically recognize pathogen effectors. The cluster organization of the NLR gene family could favor sequence exchange between NLR genes via [...] Read more.
Plants are under strong evolutionary pressure to maintain surveillance against pathogens. One major disease resistance mechanism is based on NB-LRR (NLR) proteins that specifically recognize pathogen effectors. The cluster organization of the NLR gene family could favor sequence exchange between NLR genes via recombination, favoring their evolutionary dynamics. Increasing data, based on progeny analysis, suggest the existence of a link between the perception of biotic stress and the production of genetic diversity in the offspring. This could be driven by an increased rate of meiotic recombination in infected plants, but this has never been strictly demonstrated. In order to test if pathogen infection can increase DNA recombination in pollen meiotic cells, we infected Arabidopsis Fluorescent Tagged Lines (FTL) with the virulent bacteria Pseudomonas syringae. We measured the meiotic recombination rate in two regions of chromosome 5, containing or not an NLR gene cluster. In all tested intervals, no significant difference in genetic recombination frequency between infected and control plants was observed. Although it has been reported that pathogen exposure can sometimes increase the frequency of recombinant progeny in plants, our findings suggest that meiotic recombination rate in Arabidopsis may be resilient to at least some pathogen attack. Alternative mechanisms are discussed. Full article
(This article belongs to the Special Issue NLR Gene Evolution in Plants)
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5 pages, 215 KiB  
Communication
NLGenomeSweeper: A Tool for Genome-Wide NBS-LRR Resistance Gene Identification
by Nicholas Toda, Camille Rustenholz, Agnès Baud, Marie-Christine Le Paslier, Joelle Amselem, Didier Merdinoglu and Patricia Faivre-Rampant
Genes 2020, 11(3), 333; https://doi.org/10.3390/genes11030333 - 20 Mar 2020
Cited by 23 | Viewed by 5215
Abstract
Although there are a number of bioinformatic tools to identify plant nucleotide-binding leucine-rich repeat (NLR) disease resistance genes based on conserved protein sequences, only a few of these tools have attempted to identify disease resistance genes that have not been annotated in the [...] Read more.
Although there are a number of bioinformatic tools to identify plant nucleotide-binding leucine-rich repeat (NLR) disease resistance genes based on conserved protein sequences, only a few of these tools have attempted to identify disease resistance genes that have not been annotated in the genome. The overall goal of the NLGenomeSweeper pipeline is to annotate NLR disease resistance genes, including RPW8, in the genome assembly with high specificity and a focus on complete functional genes. This is based on the identification of the complete NB-ARC domain, the most conserved domain of NLR genes, using the BLAST suite. In this way, the tool has a high specificity for complete genes and relatively intact pseudogenes. The tool returns all candidate NLR gene locations as well as InterProScan ORF and domain annotations for manual curation of the gene structure. Full article
(This article belongs to the Special Issue NLR Gene Evolution in Plants)
25 pages, 18339 KiB  
Article
LRRpredictor—A New LRR Motif Detection Method for Irregular Motifs of Plant NLR Proteins Using an Ensemble of Classifiers
by Eliza C. Martin, Octavina C. A. Sukarta, Laurentiu Spiridon, Laurentiu G. Grigore, Vlad Constantinescu, Robi Tacutu, Aska Goverse and Andrei-Jose Petrescu
Genes 2020, 11(3), 286; https://doi.org/10.3390/genes11030286 - 8 Mar 2020
Cited by 26 | Viewed by 5660
Abstract
Leucine-rich-repeats (LRRs) belong to an archaic procaryal protein architecture that is widely involved in protein–protein interactions. In eukaryotes, LRR domains developed into key recognition modules in many innate immune receptor classes. Due to the high sequence variability imposed by recognition specificity, precise repeat [...] Read more.
Leucine-rich-repeats (LRRs) belong to an archaic procaryal protein architecture that is widely involved in protein–protein interactions. In eukaryotes, LRR domains developed into key recognition modules in many innate immune receptor classes. Due to the high sequence variability imposed by recognition specificity, precise repeat delineation is often difficult especially in plant NOD-like Receptors (NLRs) notorious for showing far larger irregularities. To address this problem, we introduce here LRRpredictor, a method based on an ensemble of estimators designed to better identify LRR motifs in general but particularly adapted for handling more irregular LRR environments, thus allowing to compensate for the scarcity of structural data on NLR proteins. The extrapolation capacity tested on a set of annotated LRR domains from six immune receptor classes shows the ability of LRRpredictor to recover all previously defined specific motif consensuses and to extend the LRR motif coverage over annotated LRR domains. This analysis confirms the increased variability of LRR motifs in plant and vertebrate NLRs when compared to extracellular receptors, consistent with previous studies. Hence, LRRpredictor is able to provide novel insights into the diversification of LRR domains and a robust support for structure-informed analyses of LRRs in immune receptor functioning. Full article
(This article belongs to the Special Issue NLR Gene Evolution in Plants)
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26 pages, 2601 KiB  
Article
Population Genetics of the Highly Polymorphic RPP8 Gene Family
by Alice MacQueen, Dacheng Tian, Wenhan Chang, Eric Holub, Martin Kreitman and Joy Bergelson
Genes 2019, 10(9), 691; https://doi.org/10.3390/genes10090691 - 8 Sep 2019
Cited by 10 | Viewed by 4126
Abstract
Plant nucleotide-binding domain and leucine-rich repeat containing (NLR) genes provide some of the most extreme examples of polymorphism in eukaryotic genomes, rivalling even the vertebrate major histocompatibility complex. Surprisingly, this is also true in Arabidopsis thaliana, a predominantly selfing species with low [...] Read more.
Plant nucleotide-binding domain and leucine-rich repeat containing (NLR) genes provide some of the most extreme examples of polymorphism in eukaryotic genomes, rivalling even the vertebrate major histocompatibility complex. Surprisingly, this is also true in Arabidopsis thaliana, a predominantly selfing species with low heterozygosity. Here, we investigate how gene duplication and intergenic exchange contribute to this extraordinary variation. RPP8 is a three-locus system that is configured chromosomally as either a direct-repeat tandem duplication or as a single copy locus, plus a locus 2 Mb distant. We sequenced 48 RPP8 alleles from 37 accessions of A. thaliana and 12 RPP8 alleles from Arabidopsis lyrata to investigate the patterns of interlocus shared variation. The tandem duplicates display fixed differences and share less variation with each other than either shares with the distant paralog. A high level of shared polymorphism among alleles at one of the tandem duplicates, the single-copy locus and the distal locus, must involve both classical crossing over and intergenic gene conversion. Despite these polymorphism-enhancing mechanisms, the observed nucleotide diversity could not be replicated under neutral forward-in-time simulations. Only by adding balancing selection to the simulations do they approach the level of polymorphism observed at RPP8. In this NLR gene triad, genetic architecture, gene function and selection all combine to generate diversity. Full article
(This article belongs to the Special Issue NLR Gene Evolution in Plants)
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