ABSTRACT
BACKGROUND: Root-knot nematodes transform vascular host cells into permanent feeding structures to withdraw nutrients from the host plant. Ecotypes of Arabidopsis thaliana can display large quantitative variation in susceptibility to the root-knot nematode Meloidogyne incognita, which is thought to be independent of dominant major resistance genes. However, in an earlier genome-wide association study of the interaction between Arabidopsis and M. incognita we identified a quantitative trait locus harboring homologs of dominant resistance genes but with minor effect on susceptibility to the M. incognita population tested. RESULTS: Here, we report on the characterization of two of these genes encoding the TIR-NB-LRR immune receptor DSC1 (DOMINANT SUPPRESSOR OF Camta 3 NUMBER 1) and the TIR-NB-LRR-WRKY-MAPx protein WRKY19 in nematode-infected Arabidopsis roots. Nematode infection studies and whole transcriptome analyses using the Arabidopsis mutants showed that DSC1 and WRKY19 co-regulate susceptibility of Arabidopsis to M. incognita. CONCLUSION: Given the head-to-head orientation of DSC1 and WRKY19 in the Arabidopsis genome our data suggests that both genes may function as a TIR-NB-LRR immune receptor pair. Unlike other TIR-NB-LRR pairs involved in dominant disease resistance in plants, DSC1 and WRKY19 most likely regulate basal levels of immunity to root-knot nematodes.
Subject(s)
Arabidopsis Proteins/genetics , Arabidopsis/genetics , Plant Diseases/immunology , Plant Immunity/genetics , Tylenchoidea/physiology , Animals , Arabidopsis/immunology , Arabidopsis/parasitology , Arabidopsis Proteins/metabolism , Gene Expression Profiling , Gene Expression Regulation, Plant , Plant Diseases/parasitology , Quantitative Trait LociABSTRACT
Root-knot nematodes transform vascular host cells into permanent feeding structures to selectively withdraw their nutrients from host plants during the course of several weeks. The susceptibility of host plants to root-knot nematode infections is thought to be a complex trait involving many genetic loci. However, genome-wide association (GWA) analysis has so far revealed only four quantitative trait loci (QTLs) linked to the reproductive success of the root-knot nematode Meloidogyne incognita in Arabidopsis thaliana, which suggests that the genetic architecture underlying host susceptibility could be much simpler than previously thought. Here, we report that, by using a relaxed stringency approach in a GWA analysis, we could identify 15 additional loci linked to quantitative variation in the reproductive success of M. incognita in Arabidopsis. To test the robustness of our analysis, we functionally characterized six genes located in a QTL with the lowest acceptable statistical support and smallest effect size. This led us to identify ETHYLENE RESPONSE FACTOR 6 (ERF6) as a novel susceptibility gene for M. incognita in Arabidopsis. ERF6 functions as a transcriptional activator and suppressor of genes in response to various abiotic stresses independent of ethylene signalling. However, whole-transcriptome analysis of nematode-infected roots of the Arabidopsis erf6-1 knockout mutant line showed that allelic variation at this locus may regulate the conversion of aminocyclopropane-1-carboxylate (ACC) into ethylene by altering the expression of 1-aminocyclopropane-1-carboxylate oxidase 3 (ACO3). Our data further suggest that tolerance to abiotic stress mediated by ERF6 forms a novel layer of control in the susceptibility of Arabidopsis to M. incognita.
Subject(s)
Adaptation, Physiological , Arabidopsis Proteins/metabolism , Arabidopsis/physiology , Arabidopsis/parasitology , Plant Diseases/parasitology , Stress, Physiological/physiology , Transcription Factors/metabolism , Tylenchoidea/physiology , Animals , Arabidopsis/genetics , Arabidopsis Proteins/genetics , Biosynthetic Pathways/genetics , Ethylenes/biosynthesis , Gene Expression Regulation, Plant , Genome, Plant , Polymorphism, Single Nucleotide/genetics , Quantitative Trait Loci/genetics , Stress, Physiological/genetics , Transcription Factors/geneticsABSTRACT
Susceptibility to the root-knot nematode Meloidogyne incognita in plants is thought to be a complex trait based on multiple genes involved in cell differentiation, growth and defence. Previous genetic analyses of susceptibility to M. incognita have mainly focused on segregating dominant resistance genes in crops. It is not known if plants harbour significant genetic variation in susceptibility to M. incognita independent of dominant resistance. To study the genetic architecture of susceptibility to M. incognita, we analysed nematode reproduction on a highly diverse set of 340 natural inbred lines of Arabidopsis thaliana with genome-wide association mapping. We observed a surprisingly large variation in nematode reproduction among these lines. Genome-wide association mapping revealed four quantitative trait loci (QTLs) located on chromosomes 1 and 5 of A. thaliana significantly associated with reproductive success of M. incognita, none of which harbours typical resistance gene homologues. Mutant analysis of three genes located in two QTLs showed that the transcription factor BRASSINAZOLE RESISTANT1 and an F-box family protein may function as (co-)regulators of susceptibility to M. incognita in Arabidopsis. Our data suggest that breeding for loss-of-susceptibility, based on allelic variants critically involved in nematode feeding, could be used to make crops more resilient to root-knot nematodes.
Subject(s)
Arabidopsis/genetics , Arabidopsis/parasitology , Chromosome Mapping , Genetic Predisposition to Disease , Genome-Wide Association Study , Plant Diseases/parasitology , Plant Roots/parasitology , Tylenchoidea/physiology , Animals , Chromosomes, Plant/genetics , Gene Expression Regulation, Plant , Mutation/genetics , Plant Diseases/genetics , Plant Roots/genetics , Polymorphism, Single Nucleotide/genetics , Quantitative Trait Loci/genetics , ReproductionABSTRACT
Non-specific lipid-transfer proteins (nsLTPs) are capable of binding lipid compounds in plant tissues and are coded by the nsLTP genes. Here, we present the analysis of expression of a family of potato (Solanum tuberosum) nsLTP genes that express throughout the developing plant in a highly tissue-specific manner. Three transcript-derived fragments were isolated using an amplified restriction fragment polymorphism-derived technique for RNA fingerprinting that show homology to plant nsLTP genes. These transcript-derived fragments displayed modulated expression profiles related to the development of new tissues, with a peak of transcription around the time of tuberization and just prior to sprout development, at dormancy breakage. In addition, a homologous family of expressed sequence tags was identified whose individual members could be classified according to their tissue specificity. Two subgroups of expressed sequence tags were found to express during tuber life cycle. To study the regulation of potato nsLTP genes, two putative potato nsLTP promoters were isolated and their expression was studied using promoter-marker-gene fusions. The results showed that one of the two promoters directed a highly specific pattern of expression detected in the phloem surrounding the nodes of young plants and in the same tissue of tuber related organs, whereas the second putative promoter showed little tissue or organ specificity. This difference in expression is likely due to a 331-bp insertion present in the tissue-specific promoter.
