Novel sources of resistance to Septoria nodorum blotch in the Vavilov wheat collection identified by genome-wide association studies

Abstract

Key messageThe fungus Parastagonospora nodorum causes Septoria nodorum blotch (SNB) of wheat. A genetically diverse wheat panel was used to dissect the complexity of SNB and identify novel sources of resistance.AbstractThe fungus Parastagonospora nodorum is the causal agent of Septoria nodorum blotch (SNB) of wheat. The pathosystem is mediated by multiple fungal necrotrophic effector–host sensitivity gene interactions that include SnToxA–Tsn1, SnTox1–Snn1, and SnTox3–Snn3. A P. nodorum strain lacking SnToxA, SnTox1, and SnTox3 (toxa13) retained wild-type-like ability to infect some modern wheat cultivars, suggesting evidence of other effector-mediated susceptibility gene interactions or the lack of host resistance genes. To identify genomic regions harbouring such loci, we examined a panel of 295 historic wheat accessions from the N. I. Vavilov Institute of Plant Genetic Resources in Russia, which is comprised of genetically diverse landraces and breeding lines registered from 1920 to 1990. The wheat panel was subjected to effector bioassays, infection with P. nodorum wild type (SN15) and toxa13. In general, SN15 was more virulent than toxa13. Insensitivity to all three effectors contributed significantly to resistance against SN15, but not toxa13. Genome-wide association studies using phenotypes from SN15 infection detected quantitative trait loci (QTL) on chromosomes 1BS (Snn1), 2DS, 5AS, 5BS (Snn3), 3AL, 4AL, 4BS, and 7AS. For toxa13 infection, a QTL was detected on 5AS (similar to SN15), plus two additional QTL on 2DL and 7DL. Analysis of resistance phenotypes indicated that plant breeders may have inadvertently selected for effector insensitivity from 1940 onwards. We identify accessions that can be used to develop bi-parental mapping populations to characterise resistance-associated alleles for subsequent introgression into modern bread wheat to minimise the impact of SNB.Electronic supplementary materialThe online version of this article (10.1007/s00122-018-3073-y) contains supplementary material, which is available to authorized users.

Role of Effector-Sensitivity Gene Interactions and Durability of Quantitative Resistance to Septoria Nodorum Blotch in Eastern U.S. Wheat

“…The Tsn1-SnToxA interaction can confer susceptibility in the field in regions where Tsn1 has not been selected against. However, contrary to what is sometimes stated [e.g., (Waters et al, 2011;Tan et al, 2015;Phan et al, 2018)], there is no reason to suppose that in general, wheat-P. nodorum interactions are completely or even mainly defined by Snn-NE relationships, or that NE are required for pathogenesis. Resistance is polygenic, involving genes with minor effects, and foliar and glume infections are controlled by genes that segregate independently (Fried and Meister, 1987;Bostwick et al, 1993;Francki, 2013;Francki et al, 2017).…”

“…Of 73 Australian P. nodorum isolates, 97% possessed SnToxA (Stukenbrock and McDonald, 2007;McDonald et al, 2013); however, that collection was from a single field and the Tsn1 status of the wheat cultivar was unknown (Oliver et al, 2009). As over half of sampled wheat cultivars grown in Western Australia were sensitive to SnToxA, it appeared that breeders there had not selected against Tsn1, possibly because neither sensitivity to SnToxA nor to SnTox3 was significantly associated with cultivar resistance level as measured via artificial inoculation with a mixture of current isolates (Oliver et al, 2009;Waters et al, 2011) By contrast, effector sensitivity tests on Vavilov wheat collection accessions showed that since 1940, breeders in Russia and Kazakhstan had selected directly or indirectly against Tsn1 and also against Snn1, although not against Snn3 (Phan et al, 2018).…”

Quantitative trait loci analysis of adult plant resistance to Parastagonospora nodorum blotch in winter wheat cv. Liwilla (Triticum aestivum L.)

“…Molecular mapping and quantitative trait loci (QTL) analyses using bi-parental populations and genome-wide association studies (GWAS) greatly augment the understanding of the inheritance and genetic control of SNB resistance. A number of QTL have been identified on chromosomes such as 1A, 1B, 2B, 2D, 3A, 4A, 4B, 4D, 5A, 5B, 5D, 6A, 6D, 7A, 7B and 7D for the seedling resistance (Czembor et al 2003;Arseniuk et al 2004;Liu et al 2004b;Reszka et al 2007;Shankar et al 2008;Faris and Friesen 2009;Friesen et al 2009Friesen et al , 2012Adhikari et al 2011;Abeysekara et al 2012;Ruud et al 2017;Phan et al 2018), on 1A, 1B, 2A, 2D, 3A, 3B, 4B, 5A, 5B, 7B and 7A for adult plant leaf resistance (Aguilar et al 2005;Shankar et al 2008;Friesen et al 2009;Francki et al 2011;Lu and Lillemo 2014;Jighly et al 2016;Ruud et al 2017;Francki et al 2018), and on 2A, 2B, 2D, 3A, 3B, 4A, 4B, 5A, 5B, 6B, 7A and 7D for glume resistance (Schnurbusch et al 2003;Aguilar et al 2005;Uphaus et al 2007;Shankar et al 2008;Shatalina et al 2014;Jighly et al 2016;Francki et al 2018).…”

Genome-wide association study of multiple yield components in a diversity panel of polyploid sugarcane (Saccharum spp.)

“…GWASpoly in R is a software tailored for polyploids, which could model different types of polyploid gene actions in GWAS, including additive, simplex dominant, and duplex dominant (Rosyara et al 2016). This software has been tested in a simulated tetraploid population, and successfully applied in potato, sunflower, orchardgrass and wheat for GWAS (Berdugo-Cely et al 2017; Bock et al 2018; Phan et al 2018; Rosyara et al 2016; Zhao et al 2017). However, this software has not been utilized for GWAS in sugarcane.…”