Control of yeast retrotransposons mediated through nucleoporin evolution.

Paul A Rowley,Sara L Sawyer,Suzanne B Sandmeyer,Kurt Patterson,Cédric Feschotte

doi:10.1371/journal.pgen.1007325

Abstract

Yeasts serve as hosts to several types of genetic parasites. Few studies have addressed the evolutionary trajectory of yeast genes that control the stable co-existence of these parasites with their host cell. In Saccharomyces yeasts, the retrovirus-like Ty retrotransposons must access the nucleus. We show that several genes encoding components of the yeast nuclear pore complex have experienced natural selection for substitutions that change the encoded protein sequence. By replacing these S. cerevisiae genes with orthologs from other Saccharomyces species, we discovered that natural sequence changes have affected the mobility of Ty retrotransposons. Specifically, changing the genetic sequence of NUP84 or NUP82 to match that of other Saccharomyces species alters the mobility of S. cerevisiae Ty1 and Ty3. Importantly, all tested housekeeping functions of NUP84 and NUP82 remained equivalent across species. Signatures of natural selection, resulting in altered interactions with viruses and parasitic genetic elements, are common in host defense proteins. Yet, few instances have been documented in essential housekeeping proteins. The nuclear pore complex is the gatekeeper of the nucleus. This study shows how the evolution of this large, ubiquitous eukaryotic complex can alter the replication of a molecular parasite, but concurrently maintain essential host functionalities regarding nucleocytoplasmic trafficking.

Highlights

The presence of Ty retrotransposons (Tys) in all species of Saccharomyces yeasts suggest that they have likely been coevolving together for about 20 million years [1,2]
We show that the genes encoding certain nuclear pore components in yeast have evolved to alter the mobility of Ty retrotransposons
We find that adaptive changes in NUP82 and NUP84 affect Ty replication, yet have accumulated under the constraints of strict conservation of nucleoporin host functions during Saccharomyces speciation

Summary

Introduction

The presence of Ty retrotransposons (Tys) in all species of Saccharomyces yeasts suggest that they have likely been coevolving together for about 20 million years [1,2]. Because Tys are strictly intracellular parasites, both the host (yeast) and Tys are aligned in benefitting from a controlled, sustained relationship that does not place the host at an evolutionary disadvantage [3] This might even be thought of as a symbiotic relationship because, unlike most pathogenic viruses of higher eukaryotes, Tys are a force for genetic plasticity, driving adaptive changes within the yeast genome in response to changes in environmental conditions [4]. For this reason, it is thought that both Tys and the host genome have evolved mechanisms to attenuate unchecked Ty replication that would place an excessive burden on the host cell [3,5,6,7,8,9,10]. Regardless of whether a Ty is thought of as a symbiont, or a “tamed” parasite, one can imagine that the host-parasite relationship must be finely tuned within each yeast species, with different evolutionary strategies emerging over evolutionary time (in both yeast and Ty) to control Ty replication

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