Identification of a QTL region for tomato brown rugose fruit virus resistance in Solanum pimpinellifolium

Abstract

Tomato (Solanum lycopersicum L.), one of the most widely grown vegetables in the world, has been seriously impacted in the past decade by the emerging tomato brown rugose fruit virus (ToBRFV). ToBRFV is a seed-borne tobamovirus, with ability to overcome the commonly used Tm-2² resistance gene in tomato. The objective of this study was to conduct quantitative trait locus (QTL) mapping and identify single-nucleotide polymorphism (SNP) markers associated with ToBRFV resistance in tomato. Two F₂ populations were used for QTL mapping: One derived from a cross between S. pimpinellifolium USVL333 (PI 390718) × USVL332 (PI 390717) and another from 'Moneymaker' × USVL332 (PI 390717), with population sizes of 195 and 79 plants, respectively. The resistance trait was derived from the S. pimpinellifolium accession USVL332 (PI 390717). A major QTL for ToBRFV resistance was identified on chromosome 11 (SL4.0ch11), with the peak located at approximately 46.84 Mbp. This QTL spans a 22-kb interval between 46,825,788 bp and 46,847,421 bp, as determined through both genome-wide association study (GWAS) and QTL linkage mapping. Three SNP markers, SL4.0ch11_46825788, SL4.0ch11_46847421, and SL4.0ch11_46850215, demonstrated the most significant association with high LOD values (LOD = 13 in the Blink model) in GWAS analysis. In this genomic region, two disease resistance gene analogs, Solyc11g062150 (TIR-NBS-LRR resistance protein, Toll-Interleukin receptor) and Solyc11g062180 (disease resistance protein, leucine-rich repeat), were identified, which may serve as candidates for ToBRFV resistance. The QTL identified in this study could be valuable for plant breeders in facilitating tomato breeding with ToBRFV resistance.

Fig. 1

Representative phenotypes of genetic populations generated from their respective parents, F₁ and F₂ for resistance to tomato brown rugose fruit virus. A Phenotypic expression of the resistance line (S. pimpinellifolium ‘USVL332’) and the susceptible parent (S. lycopersicum ‘Moneymaker’) and their F₁ plants upon inoculation with ToBRFV US isolate (CA18-01); B Representative phenotypes of a F₂ MU population generated between ‘Moneymaker’ and ‘USVL332’ with mosaic, mottling, and leaf deformation (S) and normal healthy-looking leaves (R). C Representative phenotypes of a F₂ UU population generated between ‘USVL333’ and ‘USVL332’ with mosaic and mottling (S) and normal asymptomatic leaves (R)

Fig. 2

Distributions of resistance (R), intermediate susceptible (MS), and susceptible (S) individuals against tomato brown rugose fruit virus infection in the two individual F₂ populations (F₂.UU and F₂.MU) and a combination of both F₂ populations (F₂)

Fig. 3

Population genetic diversity analysis of two F2 populations consisting of 274 individuals. A Unrooted phylogenetic tree constructed using the neighbor-joining (NJ) method, showing three sub-populations; B 3D graphical plot of principal component analysis (PCA), illustrating the three sub-populations; and C PCA eigenvalue plot generated using GAPIT 3, showing that the top three principal components (PCA = 3) explain majority of the variation among the 274 F2 individuals

Fig. 4

Genome wide association study (GWAS) for ToBRFV resistance in Solanum pimpinellifolium was conducted. Four models: MLM, MLMM, FarmCPU, and Blink in GAPIT 3 were used to generate a QQ-plot (A) and Manhattan plots (B). A BLINK Manhattan plot (C) revealed SNP markers significantly associated with the ToBRFV resistance on chromosome 11

Fig. 5

The genetic map at the QTL region with the viewable SNPs on chromosome 11 created by single-trait multiple interval mapping (SMIM) for ToBRFV resistance, where x-axis presents genetic map with SNP markers, and y-axis presents LOD value