Non-parent of Origin Expression of Numerous Effector Genes Indicates a Role of Gene Regulation in Host Adaption of the Hybrid Triticale Powdery Mildew Pathogen

Abstract

Powdery mildew is an important disease of cereals. It is caused by one species, Blumeria graminis, which is divided into formae speciales each of which is highly specialized to one host. Recently, a new form capable of growing on triticale (B.g. triticale) has emerged through hybridization between wheat and rye mildews (B.g. tritici and B.g. secalis, respectively). In this work, we used RNA sequencing to study the molecular basis of host adaptation in B.g. triticale. We analyzed gene expression in three B.g. tritici isolates, two B.g. secalis isolates and two B.g. triticale isolates and identified a core set of putative effector genes that are highly expressed in all formae speciales. We also found that the genes differentially expressed between isolates of the same form as well as between different formae speciales were enriched in putative effectors. Their coding genes belong to several families including some which contain known members of mildew avirulence (Avr) and suppressor (Svr) genes. Based on these findings we propose that effectors play an important role in host adaptation that is mechanistically based on Avr-Resistance gene-Svr interactions. We also found that gene expression in the B.g. triticale hybrid is mostly conserved with the parent-of-origin, but some genes inherited from B.g. tritici showed a B.g. secalis-like expression. Finally, we identified 11 unambiguous cases of putative effector genes with hybrid-specific, non-parent of origin gene expression, and we propose that they are possible determinants of host specialization in triticale mildew. These data suggest that altered expression of multiple effector genes, in particular Avr and Svr related factors, might play a role in mildew host adaptation based on hybridization.

A chromosome‐scale genome assembly reveals a highly dynamic effector repertoire of wheat powdery mildew

“…To test if family members within clusters are co‐regulated, we analyzed expression patterns within and between candidate effector families. Here, we used published transcriptome data from isolate 96224 growing on the susceptible wheat cv Chinese Spring (Praz et al ., ) at 48 h post infection (when the haustorium is formed and the host–pathogen interaction is established). We observed a wide range of expression levels within individual families (Figs S3, S11).…”

“…We therefore analyzed differential gene expression between three B.g. tritici isolates (96224, 94202, JIW2) on cv Chinese Spring, published in Praz et al (2018) at the time of haustorium formation (2 d after infection). Among the 339 differentially expressed genes between two isolates (|log FC| > 1.5 and P-value < 0.01), 87 are effector genes (25.7%, enrichment).…”

Rapid evolution in plant–microbe interactions – a molecular genomics perspective

“…This form of adaptation will lead to isolates with diverse transcriptional profiles, which could also have different fitness optima on the same host. Indeed, individual isolates of the same forma specialis of B. graminis show considerable differences in expression levels of effector genes during infection (Praz et al, 2018). Similarly, in Z. tritici, 20-30% of the genes are differentially regulated between individual isolates during infection of the same host, and are likely to account for the quantitative variation in virulence within this species (Palma-Guerrero et al, 2017).…”

Cross-Kingdom RNAi of Pathogen Effectors Leads to Quantitative Adult Plant Resistance in Wheat

“…tritici infected seedlings at three dpi, a time point corresponding to the haustorial stage. Previous studies have shown that gene expression levels of SvrPm3 a1/f 1 are the highest during haustorium formation (Bourras et al, 2015(Bourras et al, , 2019Praz et al, 2018). Similarly, several members of the SvrPm3 a1/f 1 effector gene family, including Bgt_Bcg-6 and Bgt_Bcg-7, are induced at that same stage ( Supplementary Figure 4) (Praz et al, 2018;Bourras et al, 2019), suggesting that this time point is particularly appropriate for the quantification of mRNA levels of all three effectors, and to assess HIGS efficiency.…”

“…), HIGS is an important tool for functional genomics (Nowara et al, 2010;Pliego et al, 2013). In this system, successful infection is typically characterized by the formation of a highly specialized feeding structure called the haustorium, shortly after an appressorium-mediated penetration of the plant cell wall (Praz et al, 2018). The haustorium is a poorly understood membrane invagination that develops inside the host epidermal cell, and serves as a basis for the emergence of a network of strictly epiphytic hyphae which can form secondary appressoria (Kwaaitaal et al, 2017).…”