DNA loss at the Ceratocystis fimbriata mating locus results in self-sterility.

P Markus Wilken,Michael J Wingfield,Brenda D Wingfield,Z Wilhelm De Beer,Emma T Steenkamp,Sung-Hwan Yun

doi:10.1371/journal.pone.0092180

Abstract

Fungi have evolved a remarkable diversity of reproductive strategies. Some of these, most notably those of the model fungi, have been well studied but others are poorly understood. The latter is also true for uni-directional mating type switching, which has been reported in only five fungal genera, including Ceratocystis. Mating type switching allows a self-fertile fungal isolate to produce both self-fertile and self-sterile offspring. This study considered the molecular nature of uni-directional mating type switching in the type species of Ceratocystis, C. fimbriata. To do this, the genome of C. fimbriata was first examined for the presence of mating type genes. Three mating genes (MAT1-1-1, MAT1-2-1 and MAT1-1-2) were found in an atypical organisation of the mating type locus. To study the effect that uni-directional switching has on this locus, several self-sterile offspring were analysed. Using a combination of next generation and conventional Sanger sequencing, it was shown that a 3581 base pair (bp) region had been completely deleted from the MAT locus. This deletion, which includes the entire MAT1-2-1 gene, results in the permanent loss of self-fertility, rendering these isolates exclusively self-sterile. Our data also suggest that the deletion mechanism is tightly controlled and that it always occurs at the same genomic position. Two 260 bp direct repeats flanking the deleted region are strongly implicated in the process, although the exact mechanism behind the switching remains unclear.

Highlights

The key role that reproduction plays in the survival of a species has undoubtedly contributed to the remarkably broad range of reproductive strategies encountered across the fungal kingdom [1,2,3]
Recent technological advances such as generation sequencing and improved bioinformatic capabilities have provided tools to expand these studies to include the molecular nature of reproductive strategies in more fungi, including non-model species. These studies have led to the discovery of mating strategies that differ significantly from those of model species [11,12]. They have broadened our understanding of sexual reproduction in the fungal kingdom, thereby contributing to knowledge regarding the evolution of sex in eukaryotes in general [13,14,15]
The process that allows self-fertile isolates to give rise to both self-fertile and selfsterile forms after sexual reproduction is known as uni-directional mating type switching [22]

Summary

Introduction

The key role that reproduction plays in the survival of a species has undoubtedly contributed to the remarkably broad range of reproductive strategies encountered across the fungal kingdom [1,2,3] Several of these are found in model fungal species where they have been intensively studied and used to formulate broad hypotheses regarding mating in the fungi [4,5,6,7,8,9,10]. In the homothallic fungus N. pannonica this is accomplished by the presence of both mating idiomorphs in the same haploid genome [20] Other species such as N. tetrasperma employ a novel mating system where two copies of the haploid genome, each carrying different mating idiomorphs, occur in a single ascospore, which germinates to produce a self-fertile culture. This mating system is referred to as pseudohomothallism [2,8,21]

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