Natural selection on coding and noncoding DNA sequences is associated with virulence genes in a plant pathogenic fungus.

Gabriel E Rech,Michael R Thon,Maria Anisimova,José M Sanz-Martín,Serenella A Sukno

doi:10.1093/gbe/evu192

Abstract

Natural selection leaves imprints on DNA, offering the opportunity to identify functionally important regions of the genome. Identifying the genomic regions affected by natural selection within pathogens can aid in the pursuit of effective strategies to control diseases. In this study, we analyzed genome-wide patterns of selection acting on different classes of sequences in a worldwide sample of eight strains of the model plant-pathogenic fungus Colletotrichum graminicola. We found evidence of selective sweeps, balancing selection, and positive selection affecting both protein-coding and noncoding DNA of pathogenicity-related sequences. Genes encoding putative effector proteins and secondary metabolite biosynthetic enzymes show evidence of positive selection acting on the coding sequence, consistent with an Arms Race model of evolution. The 5′ untranslated regions (UTRs) of genes coding for effector proteins and genes upregulated during infection show an excess of high-frequency polymorphisms likely the consequence of balancing selection and consistent with the Red Queen hypothesis of evolution acting on these putative regulatory sequences. Based on the findings of this work, we propose that even though adaptive substitutions on coding sequences are important for proteins that interact directly with the host, polymorphisms in the regulatory sequences may confer flexibility of gene expression in the virulence processes of this important plant pathogen.

Highlights

The rapid accumulation of genome sequences and the development of powerful statistical methods, to detect signatures of adaptation, provide us an unprecedented opportunity to increase our understanding of functionally important genomic regions
The 50 untranslated regions (UTRs) of genes coding for effector proteins and genes upregulated during infection show an excess of high-frequency polymorphisms likely the consequence of balancing selection and consistent with the Red Queen hypothesis of evolution acting on these putative regulatory sequences
We investigate patterns of selection operating on both protein-coding DNA sequences (CDSs) and noncoding intergenic and intronic sequences in a worldwide sample of eight strains of the filamentous fungus Colletotrichum graminicola (Cg)

Summary

Introduction

The rapid accumulation of genome sequences and the development of powerful statistical methods, to detect signatures of adaptation, provide us an unprecedented opportunity to increase our understanding of functionally important genomic regions. The high level of similarity between proteins (in number and function), from phenotypically very different organisms, and the fact that a large proportion of the nonprotein-coding DNA of eukaryotic genomes is functional (Kondrashov 2005; Taft et al 2007; Raffaele and Kamoun 2012), has led to many researchers to ask whether phenotypic diversity is mainly determined by changes in protein-coding sequences or in the noncoding regulatory sequences (King and Wilson 1975; Oleksiak et al 2002; Gasch et al 2004; Whitehead and Crawford 2006; Wray 2007) For this reason, much attention has recently been given to understanding the function of noncoding DNA sequences, as exemplified by the human ENCODE project (ENCODE Project Consortium 2012) as well as to study the molecular evolution of these sequences (Zhen and Andolfatto 2012).

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