Genetic mapping identifies QTL and candidate genes including Mendel's A gene controlling high levels of partial resistance to Fusarium avenaceum in Pea.

Fav-Ps2.1 is the first major QTL reported for Fusarium avenaceum resistance in pea and co-localizes with Mendel's A gene and putative resistance genes. A novel moderate-effect QTL Fav-Ps5.1 and one epistatic locus, independent of the A gene, were also reported. Flavonoid compounds associated with resistance to this pathogen were identified. Fusarium avenaceum, a necrotrophic soil-borne pathogen, is a member of the root rot pathogen complex posing a major threat to pea yield and quality worldwide. Strong resistance to Fusarium root rot (FRR) in pea is associated with seed coat and flower pigmentation, controlled by Mendel's A locus regulating anthocyanin biosynthesis. It is not clear whether the A locus is acting alongside resistance genes to confer high levels of resistance or whether alternative genetic pathways exist in pea cultivars. In this study, a pea recombinant inbred line population of 160 lines called PR-20 (AA×aa), polyphenolic profiles, and the pea reference genome were leveraged to understand the genetic control of Fusarium avenaceum resistance. Two novel quantitative trait loci (QTLs) including a major QTL Fav-Ps2.1 (41-42.2 cM) on chromosome 6 with 95% phenotypic variance explained (PVE), a moderate-effect QTL Fav-Ps5.1 (126-134 cM) on chromosome 3 with 9% PVE, and a putative epistatic interaction with 15% PVE, associated with resistance to F. avenaceum were identified. Both the epistatic region and Fav-Ps5.1 are anthocyanin pigment-independent. Fav-Ps5.1 is co-localized with many defense-response and flavonoid-related genes including NDR1/HIN1-like protein, WDR, MYB111, WRKY, Chitinase, PAL1, F-box/LRR-repeat protein, E3 ubiquitin-protein ligase PUB22, ABC transporters, and probable ethylene response sensor 1. Fav-Ps2.1 is co-localized with 35 disease resistance-related genes and overlaps with the A locus, which may explain the high PVE. A 'pea tobacco mosaic virus (TMV) resistance N-like protein' gene, encoding TIR-LRR domains, marks the peak of Fav-Ps2.1 at ~ 0.12 cM upstream of the A locus. Regression analysis with whole seed polyphenolic compounds in randomly selected 14 PR-20 lines including the parents showed that some colorless flavonoids (anthocyanin precursors), encoded by genes other than A, explained more variation in disease resistance (R2 = 87-99%; P ≤ 0.001), compared to the A gene-encoding anthocyanin compounds (R2 = 38-86%; P ≤ 0.018). Our results demonstrate that high FRR resistance is not determined only by the A locus but emerges from multiple coordinated resistance loci. These findings provide new insights into the genetic basis of F. avenaceum resistance for breeding FRR resistance in white-flowered pea varieties.