Quantitative trait locus mapping reveals complex genetic architecture of quantitative virulence in the wheat pathogenZymoseptoria tritici

Abstract

SUMMARYWe conducted a comprehensive analysis of virulence in the fungal wheat pathogen Zymoseptoria tritici using quantitative trait locus (QTL) mapping. High-throughput phenotyping based on automated image analysis allowed the measurement of pathogen virulence on a scale and with a precision that was not previously possible. Across two mapping populations encompassing more than 520 progeny, 540 710 pycnidia were counted and their sizes and grey values were measured. A significant correlation was found between pycnidia size and both spore size and number. Precise measurements of percentage leaf area covered by lesions provided a quantitative measure of host damage. Combining these large and accurate phenotypic datasets with a dense panel of restriction site-associated DNA sequencing (RADseq) genetic markers enabled us to genetically dissect pathogen virulence into components related to host damage and those related to pathogen reproduction. We showed that different components of virulence can be under separate genetic control. Large-and small-effect QTLs were identified for all traits, with some QTLs specific to mapping populations, cultivars and traits and other QTLs shared among traits within the same mapping population. We associated the presence of four accessory chromosomes with small, but significant, increases in several virulence traits, providing the first evidence for a meaningful function associated with accessory chromosomes in this organism. A large-effect QTL involved in host specialization was identified on chromosome 7, leading to the identification of candidate genes having a large effect on virulence.

A small secreted protein in Zymoseptoria tritici is responsible for avirulence on wheat cultivars carrying the Stb6 resistance gene

“…Previous studies suggested that avirulence of Z. tritici strains on wheat cultivars carrying the Stb6 resistance gene is controlled by a single locus involved in a GFG interaction (Kema et al, 2000;Brading et al, 2002). We observed that the Swiss 1E4 strain used in previous QTL mapping experiments (Lendenmann et al, 2014;Stewart et al, 2016) was avirulent on the wheat cultivar 'Chinese Spring', which is known to carry Stb6 (Chartrain et al, 2005) (Fig. 1a).…”

“…Virulence of Z. tritici has a strong quantitative component (Zhan et al, 2007;Stewart et al, 2016). However, quantitative trait locus (QTL) mapping studies identified single large effect size QTLs (Mirzadi Gohari, 2015;Stewart et al, 2016) strongly indicating that Z. tritici virulence can also be governed by GFG interactions. Furthermore, this suggests that Z. tritici harbors avirulence effector genes.…”

A fungal avirulence factor encoded in a highly plastic genomic region triggers partial resistance to septoria tritici blotch

“…Mapping onto the new genome sequence provided twice as many SNP markers and enabled the identification of additional crossovers that allowed us to reduce the number of candidate genes in the previously identified virulence QTL on chromosome 7 (Stewart et al ., 2018). The new map yielded a narrower QTL interval (logarithm of the odds, LOD = 41.5, P  < 10 −15 ) located within the original QTL interval.…”

“…In addition to Stb6 , 19 other race‐specific Stb resistance genes with large effects have been mapped, but their corresponding avirulence factors remain unknown (Brown et al ., 2015). We hypothesised that one of these Stb genes might be responsible for the differences in resistance of cultivar Runal to two Swiss strains (3D1 and 3D7, Stewart et al ., 2018). The more virulent strain 3D7 produced necrotic lesions faster than strain 3D1.…”

“…1a,b). A single, large‐effect quantitative trait locus (QTL) encoding differences in lesion size and pycnidia density between 3D1 and 3D7 was mapped to a region on chromosome 7 (Stewart et al ., 2018). However, the genes responsible for the differences in virulence were not identified.…”