Clade- and species-specific features of genome evolution in the Saccharomycetaceae

FEMS Yeast Research, 15, 2015, fov035 doi: 10.1093/femsyr/fov035 Advance Access Publication Date: 11 June 2015 Minireview MINIREVIEW Kenneth H. Wolfe1,∗ , David Armisén2,3 , Estelle Proux-Wera2,4 , Seán S. ÓhÉigeartaigh2,5 , Haleema Azam2 , Jonathan L. Gordon2,6 and Kevin P. Byrne1 1 UCD Conway Institute, School of Medicine and Medical Science, University College Dublin, Dublin 4, Ireland, Smurfit Institute of Genetics, Trinity College Dublin, Dublin 2, Ireland, 3 Institut de Génomique Fonctionnelle de Lyon, ENS de Lyon - CNRS UMR 5242 - INRA USC 1370, 46 allée d’Italie, 69364 Lyon cedex 07, France, 4 Science for Life Laboratory, Dept. of Biochemistry and Biophysics, Stockholm University, Box 1031, SE-17121 Solna, Sweden, 5 Centre for the Study of Existential Risk, University of Cambridge, CRASSH, Alison Richard Building, 7 West Road, Cambridge, CB3 9DT, UK and 6 CIRAD, UMR CMAEE, Site de Duclos, Prise d’eau, F-97170, Petit-Bourg, Guadeloupe, France 2 ∗ Corresponding author: UCD Conway Institute, School of Medicine and Medical Science, University College Dublin, Dublin 4, Ireland. Tel: +353-1-7166712; E-mail: One sentence summary: The authors review species-specific evolutionary attributes of yeast genomes. Editor: Jens Nielsen ABSTRACT Many aspects of the genomes of yeast species in the family Saccharomycetaceae have been well conserved during evolution. They have similar genome sizes, genome contents, and extensive collinearity of gene order along chromosomes. Gene functions can often be inferred reliably by using information from Saccharomyces cerevisiae. Beyond this conservative picture however, there are many instances where a species or a clade diverges substantially from the S. cerevisiae paradigm—for example, by the amplification of a gene family, or by the absence of a biochemical pathway or a protein complex. Here, we review clade-specific features, focusing on genomes sequenced in our laboratory from the post-WGD genera Naumovozyma, Kazachstania and Tetrapisispora, and from the non-WGD species Torulaspora delbrueckii. Examples include the loss of the pathway for histidine synthesis in the cockroach-associated species Tetrapisispora blattae; the presence of a large telomeric GAL gene cluster in To. delbrueckii; losses of the dynein and dynactin complexes in several independent yeast lineages; fragmentation of the MAT locus and loss of the HO gene in Kazachstania africana; and the patchy phylogenetic distribution of RNAi pathway components. Keywords: evolution; comparative genomics; Kazachstania; Naumovozyma; Tetrapisispora; Torulaspora INTRODUCTION Yeast species provide remarkable opportunities to study genomic evolution. In the two decades since the sequence of Saccharomyces cerevisiae was first reported (Goffeau et al. 1996), three major areas of research into yeast genome evolution have devel- oped. First, studies such as mutation accumulation experiments have provided a view of mutational processes and rates at unprecedented resolution, both in Saccharomyces (Lynch et al. 2008; Nishant et al. 2010; Zhu et al. 2014) and in other yeasts (Polakova et al. 2009; Friedrich et al. 2015). Second, population genomics Received: 5 May 2015; Accepted: 29 May 2015  C FEMS 2015. This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs licence (http://creativecommons.org/licenses/by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any medium, provided the original work is not altered or transformed in any way, and that the work is properly cited. For commercial re-use, please contact 1 Clade- and species-specific features of genome evolution in the Saccharomycetaceae 2 FEMS Yeast Research, 2015, Vol. 15, No. 5 some 2. In any non-WGD species in the Saccharomycetaceae, the gene order along any section of chromosome is usually similar to the ancestral order. Discontinuities correspond to genomic rearrangements, either in the non-WGD species or on the lineage of the ancestor (i.e. the post-WGD lineage prior to the occurrence of the WGD). In any post-WGD species, there are two genomic regions corresponding to each chromosomal region in the ancestor. Each of these regions contains a subset of the ancestral genes, usually without rearrangement of gene order, and some ancestral genes remain in duplicate (ohnologs) and thus appear on both chromosomal regions of the post-WGD species. We now have a genome sequence from at least one species in almost every known genus of the family Saccharomycetaceae as defined by Kurtzman (2011) (Fig. 1). The only genera classified in this family that have not yet been sequenced are Zygotorulaspora (a sister clade to Torulaspora and Zygosaccharomyces; Kurtzman 2003) and Cyniclomyces whose phylogenetic position is uncertain and which may be basal to the family (Boundy-Mills and Miller 2011). Outside this family (Kurtzman 2003; Kurtzman and Robnett 2013), we have relatively limited genomic data from the closest outgroup genera such as Hanseniaspora/Kloeckera (Giorello et al. 2014), Saccharomycodes, Wickerhamomyces (Schneider et al. 2012a,b) and Cyberlindnera (Tomita et al. 2012; Freel et al. 2014). Although genome evolution in the sequenced Saccharomycetaceae species has largely been conservative, with similar genes being arranged in similar ways along the chromosomes of each species, the exceptions to this rule—the differences between the species—can often be of interest and can point to differences in the biology of the species that own the genomes. In this review, we focus on aspects that are unique to the genome of a particular species or genus. We focus in particular on seven genomes that we sequenced in 2011, from three post-WGD genera (Naumovozyma, Kazachstania and Tetrapisispora) and one nonWGD genus (Torulaspora). We have previously described the evolution of the mating-type (MAT) loci of these species (Gordon et al. 2011a), but here we comment on some of their other features. Summary statistics of these genomes is given in Table 1. Saccharomycetaceae genomes We sampled three post-WGD genera that had not previously been extensively studied: Naumovozyma, Kazachstania and Tetrapisispora (Kurtzman 2003). Together with the recent sequencing of genomes in the Nakaseomyces clade (including Candida glabrata and its asexual relatives) by Gabaldon et al. (2013), these data mean that we now have a genome sequence for every known post-WGD genus, and multiple genomes for all post-WGD genera except Vanderwaltozyma (Fig. 1). The genome of Naumovozyma castellii had been sequenced to draft level by Cliften et al. (2003, 2006) and it had been shown to be a postWGD species with differential gene loss as compared to S. cerevisiae (Langkjaer et al. 2003; Scannell, Butler and Wolfe 2007a). We completed the genome sequence of the type strain of N. castellii (CBS 4309; this species was previously also called Saccharomyces castellii and Na (...truncated)