Dataset Information

Verticillium longisporum infection induces organ-specific glucosinolate degradation in Arabidopsis thaliana.

ABSTRACT: The species Verticillium represents a group of highly destructive fungal pathogens, responsible for vascular wilt in a number of crops. The host response to infection by Verticillium longisporum at the level of secondary plant metabolites has not been well explored. Natural variation in the glucosinolate (GLS) composition of four Arabidopsis thaliana accessions was characterized: the accessions Bur-0 and Hi-0 accumulated alkenyl GLS, while 3-hydroxypropyl GLS predominated in Kn-0 and Ler-0. With respect to GLS degradation products, Hi-0 and Kn-0 generated mainly isothiocyanates, whereas Bur-0 released epithionitriles and Ler-0 nitriles. An analysis of the effect on the composition of both GLS and its breakdown products in the leaf and root following the plants' exposure to V. longisporum revealed a number of organ- and accession-specific alterations. In the less disease susceptible accessions Bur-0 and Ler-0, colonization depressed the accumulation of GLS in the rosette leaves but accentuated it in the roots. In contrast, in the root, the level of GLS breakdown products in three of the four accessions fell, suggestive of their conjugation or binding to a fungal target molecule(s). The plant-pathogen interaction influenced both the organ- and accession-specific formation of GLS degradation products.

SUBMITTER: Witzel K

PROVIDER: S-EPMC4498036 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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Verticillium longisporum infection induces organ-specific glucosinolate degradation in Arabidopsis thaliana.

Witzel Katja K Hanschen Franziska S FS Klopsch Rebecca R Ruppel Silke S Schreiner Monika M Grosch Rita R

Frontiers in plant science 20150710

The species Verticillium represents a group of highly destructive fungal pathogens, responsible for vascular wilt in a number of crops. The host response to infection by Verticillium longisporum at the level of secondary plant metabolites has not been well explored. Natural variation in the glucosinolate (GLS) composition of four Arabidopsis thaliana accessions was characterized: the accessions Bur-0 and Hi-0 accumulated alkenyl GLS, while 3-hydroxypropyl GLS predominated in Kn-0 and Ler-0. With ...[more]

PMID: 26217360

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Project description:BACKGROUND: Verticillium longisporum is a soil-borne vascular pathogen infecting cruciferous hosts such as oilseed rape. Quantitative disease resistance (QDR) is the major control means, but its molecular basis is poorly understood so far. Quantitative trait locus (QTL) mapping was performed using a new (Bur×Ler) recombinant inbred line (RIL) population of Arabidopsis thaliana. Phytohormone measurements and analyses in defined mutants and near-isogenic lines (NILs) were used to identify genes and signalling pathways that underlie different resistance QTL. RESULTS: QTL for resistance to V. longisporum-induced stunting, systemic colonization by the fungus and for V. longisporum-induced chlorosis were identified. Stunting resistance QTL were contributed by both parents. The strongest stunting resistance QTL was shown to be identical with Erecta. A functional Erecta pathway, which was present in Bur, conferred partial resistance to V. longisporum-induced stunting. Bur showed severe stunting susceptibility in winter. Three stunting resistance QTL of Ler origin, two co-localising with wall-associated kinase-like (Wakl)-genes, were detected in winter. Furthermore, Bur showed a much stronger induction of salicylic acid (SA) by V. longisporum than Ler. Systemic colonization was controlled independently of stunting. The vec1 QTL on chromosome 2 had the strongest effect on systemic colonization. The same chromosomal region controlled the level of abscisic acid (ABA) and jasmonic acid (JA) in response to V. longisporum: The level of ABA was higher in colonization-susceptible Ler than in colonization-resistant Bur after V. longisporum infection. JA was down-regulated in Bur after infection, but not in Ler. These differences were also demonstrated in NILs, varying only in the region containing vec1. All phytohormone responses were shown to be independent of Erecta. CONCLUSIONS: Signalling systems with a hitherto unknown role in the QDR of A. thaliana against V. longisporum were identified: Erecta mediated resistance against V. longisporum-induced stunting. Independent of Erecta, stunting was caused in a light-dependent manner with possible participation of SA and Wakl genes. ABA and JA showed a genotype-specific response that corresponded with systemic colonization by the fungus. Understanding the biological basis of phenotypic variation in A. thaliana with respect to V. longisporum resistance will provide new approaches for implementing durable resistance in cruciferous crops.

Project description:Hybridization is an important evolutionary mechanism that can enable organisms to adapt to environmental challenges. It has previously been shown that the fungal allodiploid species Verticillium longisporum, the causal agent of verticillium stem striping in rapeseed, originated from at least three independent hybridization events between two haploid Verticillium species. To reveal the impact of genome duplication as a consequence of hybridization, we studied the genome and transcriptome dynamics upon two independent V. longisporum hybridization events, represented by the hybrid lineages "A1/D1" and "A1/D3." We show that V. longisporum genomes are characterized by extensive chromosomal rearrangements, including between parental chromosomal sets. V. longisporum hybrids display signs of evolutionary dynamics that are typically associated with the aftermath of allodiploidization, such as haploidization and more relaxed gene evolution. The expression patterns of the two subgenomes within the two hybrid lineages are more similar than those of the shared A1 parent between the two lineages, showing that the expression patterns of the parental genomes homogenized within a lineage. However, as genes that display differential parental expression in planta do not typically display the same pattern in vitro, we conclude that subgenome-specific responses occur in both lineages. Overall, our study uncovers genomic and transcriptomic plasticity during the evolution of the filamentous fungal hybrid V. longisporum and illustrates its adaptive potential. IMPORTANCE Verticillium is a genus of plant-associated fungi that includes a few plant pathogens that collectively affect a wide range of hosts. On several occasions, haploid Verticillium species hybridized into the stable allodiploid species Verticillium longisporum, which is, in contrast to haploid Verticillium species, a Brassicaceae specialist. Here, we studied the evolutionary genome and transcriptome dynamics of V. longisporum and the impact of the hybridization. V. longisporum genomes display a mosaic structure due to genomic rearrangements between the parental chromosome sets. Similar to other allopolyploid hybrids, V. longisporum displays an ongoing loss of heterozygosity and more relaxed gene evolution. Also, differential parental gene expression is observed, with enrichment for genes that encode secreted proteins. Intriguingly, the majority of these genes display subgenome-specific responses under differential growth conditions. In conclusion, hybridization has incited the genomic and transcriptomic plasticity that enables adaptation to environmental changes in a parental allele-specific fashion.

Dataset Information

Verticillium longisporum infection induces organ-specific glucosinolate degradation in Arabidopsis thaliana.

Publications

Verticillium longisporum infection induces organ-specific glucosinolate degradation in Arabidopsis thaliana.

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