Genome‐wide association study identifies quantitative trait loci associated with resistance to Verticillium dahliae race 3 in tomato

TL;DR

This study identifies genetic loci linked to resistance against a new strain of Verticillium wilt in tomatoes, offering tools to breed more resilient varieties.

Contribution

The discovery of two novel resistance loci on chromosome 5 and the demonstration of GWAS-assisted genomic prediction's improved accuracy for tomato breeding.

Findings

Four candidate genes associated with VW resistance were identified, including two novel loci on chromosome 5.

GWAS-assisted genomic prediction improved predictive ability for VW resistance by up to 16.4% compared to standard models.

The candidate genes are involved in plant defense and cell wall modification.

Abstract

Verticillium wilt (VW) disease, caused by Verticillium dahliae Kleb., is a major threat to tomato (Solanum lycopersicum L.) production. Identifying loci associated with VW resistance can accelerate breeding efforts and support sustainable disease management. Although the Ve1 and Ve2 genes confer resistance to V. dahliae races 1 and 2, the emergence of race 3 in the United States poses a new challenge. To investigate the genetic basis of quantitative resistance to the race 3 strain KJ14a, we evaluated 250 diverse tomato accessions. Disease severity and incidence were assessed weekly over 5 weeks, using chlorosis/necrosis percentage (CN_perc) and the number of symptomatic leaves (LC) as phenotypes. OmeSeq quantitative reduced‐representation sequencing yielded 42,941 high‐quality single nucleotide polymorphism and insertion‐deletion markers. Genome‐wide association study (GWAS) and local linkage disequilibrium analyses identified four candidate genes associated with VW resistance on chromosomes 3, 5, and 7, including two loci mapping to previously reported quantitative trait loci and two novel resistance loci on chromosome 5. The candidate genes are involved in plant defense and the modification of cell walls. To validate and assess the breeding potential of marker‐trait associations, we applied GWAS‐assisted best linear unbiased prediction (GWABLUP). Using an additive + dominance model and GWABLUP with top 100 associated markers, predictive ability for LC improved by 16.4% and 4.8%, and for CN_perc by 11.7% and 7.9%, compared to standard genomic best linear unbiased prediction using 100 and 18,000 genome‐wide markers, respectively. These results offer valuable insights into the genetic architecture of VW resistance to race 3 and demonstrate the potential of combining GWAS and genomic prediction to accelerate tomato breeding for durable disease resistance.

Verticillium wilt (VW), caused by Verticillium dahliae Kleb., poses a significant threat to global tomato production.The extensive cultivation of tomato varieties containing the Ve1 gene has led to an increase in the prevalence of race 2 and race 3 strains in tomato fields.Linkage disequilibrium (LD)‐based genome‐wide association study (GWAS) approach can identify genetic loci significantly associated with resistance to VW.Identify candidate genes linked to VW resistance and with predicted functions.A GWAS‐informed genomic prediction model can improve predictive ability and expedite the breeding process.

Verticillium wilt (VW), caused by Verticillium dahliae Kleb., poses a significant threat to global tomato production.

The extensive cultivation of tomato varieties containing the Ve1 gene has led to an increase in the prevalence of race 2 and race 3 strains in tomato fields.

Linkage disequilibrium (LD)‐based genome‐wide association study (GWAS) approach can identify genetic loci significantly associated with resistance to VW.

Identify candidate genes linked to VW resistance and with predicted functions.

A GWAS‐informed genomic prediction model can improve predictive ability and expedite the breeding process.

Verticillium wilt (VW) is a severe soilborne disease that poses a significant threat to tomato production. The phase‐out of fumigants like methyl bromide, along with the emergence of race 3 of Verticillium dahliae Kleb., underscores the need for sustainable resistance strategies. In this study, we employed genome‐wide association study (GWAS) analysis to identify four candidate genes associated with VW resistance in tomato, including two novel loci on chromosome 5. To evaluate their breeding potential, we applied a genomic prediction assisted by GWAS (GWABLUP). This approach improved predictive ability for VW resistance by up to 16.4% compared to standard genomic prediction models. Our findings provide new insights into the genetic basis of VW resistance, suggesting that the identified markers could be valuable tools for breeding more resilient tomato varieties.

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