Mapping of SnTox3–Snn3 as a major determinant of field susceptibility to Septoria nodorum leaf blotch in the SHA3/CBRD × Naxos population

Abstract

The effect of the SnTox3-Snn3 interaction was documented for the first time under natural infection at the adult plant stage in the field. Co-segregating SNP markers were identified. Parastagonospora nodorum is a necrotrophic pathogen of wheat, causing Septoria nodorum blotch (SNB) affecting both the leaf and glume. P. nodorum is the major leaf blotch pathogen on spring wheat in Norway. Resistance to the disease is quantitative, but several host-specific interactions between necrotrophic effectors (NEs) and host sensitivity (Snn) genes have been identified, playing a major role at the seedling stage. However, the effect of these interactions in the field under natural infection has not been investigated. In the present study, we saturated the genetic map of the recombinant inbred (RI) population SHA3/CBRD × Naxos using the Illumina 90 K SNP chip. The population had previously been evaluated for segregation of SNB susceptibility in field trials. Here, we infiltrated the population with the purified NEs SnToxA, SnTox1 and SnTox3, and mapped the Snn3 locus on 5BS based on sensitivity segregation and SNP marker data. We also conducted inoculation and culture filtrate (CF) infiltration experiments on the population with four selected P. nodorum isolates from Norway and North America. Remapping of quantitative trait loci (QTL) for field resistance showed that the SnTox3-Snn3 interaction could explain 24% of the phenotypic variation in the field, and more than 51% of the variation in seedling inoculations. To our knowledge, this is the first time the effect of this interaction has been documented at the adult plant stage under natural infection in the field.

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

“…Resistance to SNG and SNL showed a continuous phenotypic distribution reflecting their quantitative nature. Moreover, five QTL associated with resistance to SNB were identified, indicating polygenic inheritance, which is in agreement with several previous studies on adult plant resistance in wheat (Schnurbusch et al 2003;Aguilar et al 2005;Uphaus et al 2007;Shankar et al 2008;Francki et al 2011;Lu and Lillemo 2014;Ruud et al 2017;Francki et al 2018). None of the DH lines were fully resistant on glumes and leaves, but more frequently they were less diseased than the resistant parent Liwilla (transgressive segregation observed), and alleles from the susceptible parent Begra also contributed to the resistance level.…”

“…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).…”

“…However, for other identified resistance QTL such co-location was not observed, as reviewed by Francki (2013). Interesting data on the role of Snn-SnTox interactions for SNB adult plant resistance were provided by studies of Friesen et al (2009) and Ruud et al (2017). Significant SnToxA-Tsn1 and SnTox2-Snn2 interaction was detected and accounted for as much as 18% and 15% of the variation in disease severity on the flag leaf, respectively, after inoculation with a single isolate ).…”

“…Significant SnToxA-Tsn1 and SnTox2-Snn2 interaction was detected and accounted for as much as 18% and 15% of the variation in disease severity on the flag leaf, respectively, after inoculation with a single isolate ). QTL analysis of adult plant SNB resistance under natural pathogen infection revealed a significant effect of the SnTox3-Snn3 interaction that could explain up to 24% of the phenotypic variation (Ruud et al 2017).…”

Genetic analysis of wheat sensitivity to the ToxB fungal effector from Pyrenophora tritici-repentis, the causal agent of tan spot

“…Collectively, these results indicate that minor necrotrophic fungal pathogen effector sensitivity QTL may also be relevant to field resistance to this class of wheat necrotrophic fungal pathogens, as has been shown for the major P. nodorum effector sensitivity loci Tsn1, Snn1 and Snn3-B1 in wheat (e.g. Friesen et al 2009;Phan et al 2016;Ruud et al 2017).…”