ABSTRACT
As obligatory parasites, plant viruses alter host cellular metabolism. There is a lack of information on the variability of virus-induced metabolic responses among genetically diverse plants in a natural context with daily changing conditions. To decipher the metabolic landscape of plant-virus interactions in a natural setting, twenty-six and ten accessions of Arabidopsis thaliana were inoculated with Turnip mosaic virus (TuMV), in two field experiments over 2 years. The accessions were measured for viral accumulation, above-ground biomass, targeted and untargeted metabolic profiles. The phenotypes of the accessions ranged from susceptibility to resistance. Susceptible and resistant accessions were shown to have different metabolic routes after inoculation. Susceptible genotypes accumulate primary and secondary metabolites upon infection, at the cost of hindered growth. Twenty-one metabolic signatures significantly accumulated in resistant accessions whereas they maintained their growth as mock-inoculated plants without biomass penalty. Metabolic content was demonstrated to discriminate and be highly predictive of the susceptibility of inoculated Arabidopsis. This study is the first to describe the metabolic landscape of plant-virus interactions in a natural setting and its predictive link to susceptibility. It provides new insights on plant-virus interactions. In this undomesticated species and in ecologically realistic conditions, growth and resistance are in a permanent conversation.
ABSTRACT
The genetic architecture of plant response to viruses has often been studied in model nonnatural pathosystems under controlled conditions. There is an urgent need to elucidate the genetic architecture of the response to viruses in a natural setting. A field experiment was performed in each of two years. In total, 317 Arabidopsis thaliana accessions were inoculated with its natural Turnip mosaic virus (TuMV). The accessions were phenotyped for viral accumulation, frequency of infected plants, stem length and symptoms. Genome-wide association mapping was performed. Arabidopsis thaliana exhibits extensive natural variation in its response to TuMV in the field. The underlying genetic architecture reveals a more quantitative picture than in controlled conditions. Ten genomic regions were consistently identified across the two years. RTM3 (Restricted TEV Movement 3) is a major candidate for the response to TuMV in the field. New candidate genes include Dead box helicase 1, a Tim Barrel domain protein and the eukaryotic translation initiation factor eIF3b. To our knowledge, this study is the first to report the genetic architecture of quantitative response of A. thaliana to a naturally occurring virus in a field environment, thereby highlighting relevant candidate genes involved in plant virus interactions in nature.
Subject(s)
Arabidopsis/genetics , Arabidopsis/virology , Genetic Loci , Genome, Plant , Genome-Wide Association Study , Host-Pathogen Interactions/genetics , Potyvirus/physiology , Ecotype , Genotype , Polymorphism, Single Nucleotide/geneticsABSTRACT
Sharka is a devastating viral disease caused by the Plum pox virus (PPV) in stone fruit trees and few sources of resistance are known in its natural hosts. Since any knowledge gained from Arabidopsis on plant virus susceptibility factors is likely to be transferable to crop species, Arabidopsis's natural variation was searched for host factors essential for PPV infection. To locate regions of the genome associated with susceptibility to PPV, linkage analysis was performed on six biparental populations as well as on multiparental lines. To refine quantitative trait locus (QTL) mapping, a genome-wide association analysis was carried out using 147 Arabidopsis accessions. Evidence was found for linkage on chromosomes 1, 3 and 5 with restriction of PPV long-distance movement. The most relevant signals occurred within a region at the bottom of chromosome 3, which comprises seven RTM3-like TRAF domain-containing genes. Since the resistance mechanism analyzed here is recessive and the rtm3 knockout mutant is susceptible to PPV infection, it suggests that other gene(s) present in the small identified region encompassing RTM3 are necessary for PPV long-distance movement. In consequence, we report here the occurrence of host factor(s) that are indispensable for virus long-distance movement.
Subject(s)
Arabidopsis/genetics , Chromosome Mapping/methods , Genetic Linkage , Genome, Plant , Plum Pox Virus/pathogenicity , Agrobacterium tumefaciens/genetics , Agrobacterium tumefaciens/metabolism , Alleles , Arabidopsis/immunology , Arabidopsis/metabolism , Arabidopsis/virology , Arabidopsis Proteins/genetics , Arabidopsis Proteins/metabolism , Chromosomes, Plant/genetics , Chromosomes, Plant/metabolism , Crosses, Genetic , Disease Resistance , Gene Knockout Techniques , Genes, Plant , Genetic Association Studies/methods , Microsatellite Repeats , Plant Diseases/genetics , Plant Diseases/immunology , Plant Diseases/virology , Plum Pox Virus/immunology , Plum Pox Virus/metabolism , Pollination , Polymorphism, Single Nucleotide , Quantitative Trait LociABSTRACT
BACKGROUND: The non conventional RTM (Restricted Tobacco etch virus Movement) resistance which restricts long distance movement of some plant viruses in Arabidopsis thaliana is still poorly understood. Though at least three RTM genes have been identified, their precise role(s) in the process as well as whether other genes are involved needs to be elucidated. METHODOLOGY/PRINCIPAL FINDINGS: In this study, the natural variation of the RTM genes was analysed at the amino acid level in relation with their functionality to restrict the long distance movement of Lettuce mosaic potyvirus (LMV). We identified non-functional RTM alleles in LMV-susceptible Arabidopsis accessions as well as some of the mutations leading to the non-functionality of the RTM proteins. Our data also indicate that more than 40% of the resistant accessions to LMV are controlled by the RTM genes. In addition, two new RTM loci were genetically identified. CONCLUSIONS/SIGNIFICANCE: Our results show that the RTM resistance seems to be a complex biological process which would involves at least five different proteins. The next challenges will be to understand how the different RTM protein domains are involved in the resistance mechanism and to characterise the new RTM genes for a better understanding of the blocking of the long distance transport of plant viruses.