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.

Highlights

  • Crops are threatened by rapidly evolving pathogen populations, resulting in economically important yield losses and requiring continuous breeding for new resistant cultivars (Oerke, 2006)

  • We identify differentially expressed genes between isolates and between formae speciales, and show they are enriched in candidate effectors

  • For the most HE genes we found that 34.7% encoded for proteins related to the secretome, while another 34.7% encoded for proteins related to ribosomal or mitochondrial functions

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Summary

Introduction

Crops are threatened by rapidly evolving pathogen populations, resulting in economically important yield losses and requiring continuous breeding for new resistant cultivars (Oerke, 2006). Plant pathogenic fungi are considered the most important cause of disease and pathogens such as powdery mildew and leaf rust can cause up to 20 and 50% of yield losses in wheat, respectively (Conner et al, 2003; Huerta-Espino et al, 2011; Dean et al, 2012). These two pathogens are obligate biotrophs that require living host cells to complete their life cycle. Over 1,000 putative effectors have been identified in the genome of rust fungi from the genus Melampsora (Basidiomycetes) (Hacquard et al, 2012; Saunders et al, 2012) and over 500 in cereal powdery mildews (Pedersen et al, 2012; Praz et al, 2017)

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