Abstract

Plant cell wall degrading enzymes (PCWDEs) of plant pathogens are receiving increasing interest for their potential to trigger plant defense reactions. In an antagonistic co-evolutionary arms race between host and pathogen, PCWDEs could be under strong selection. Here, we tested the hypothesis that PCWDEs in the fungal wheat pathogen Mycosphaerella graminicola have been positively selected by analyzing ratios of non-synonymous and synonymous nucleotide changes in the genes encoding these enzymes. Analyses of five PCWDEs demonstrated that one (β-xylosidase) has been under strong positive selection and experienced an accelerated rate of evolution. In contrast, PCWDEs in the closest relatives of M. graminicola collected from wild grasses did not show evidence for selection or deviation from a molecular clock. Since the genealogical divergence of M. graminicola from these latter species coincided with the onset of agriculture, we hypothesize that the recent domestication of the host plant and/or agricultural practices triggered positive selection in β-xylosidase and that this enzyme played a key role in the emergence of a host-specialized pathogen.

Highlights

  • The antagonistic co-evolution caused by host-pathogen interactions is among the most important forces shaping organismal diversity

  • 189 field-collected strains of M. graminicola originating from Iran, Israel, Oregon, Switzerland and Germany were sequenced for five genes encoding Plant cell wall degrading enzymes (PCWDEs)

  • Analyses of genes encoding PCWDEs in M. graminicola and closely related species provided novel insights into the evolutionary processes associated with pathogen domestication

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Summary

Introduction

The antagonistic co-evolution caused by host-pathogen interactions is among the most important forces shaping organismal diversity. Natural selection has generated a complex array of defense mechanisms to prevent or limit infection by pathogens. The basal immune system of plants detects molecules that are broadly conserved across a wide range of pathogen taxa. These molecules have been named pathogen-associated molecular patterns (PAMPs). Detection of microorganisms induces PAMPtriggered immunity (PTI), which may be the plant’s first line of defense. Identified PAMPs that elicit PTI in plants include fungal chitin and bacterial flagellins [2,3]. A second line of more specific resistance is induced in ‘‘gene-for-gene’’ interactions referred to as effector-triggered immunity (ETI). ETI involves proteins encoded by the plant resistance (R) genes that detect pathogen effector proteins

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