A widespread inversion polymorphism conserved among Saccharomyces species is caused by recurrent homogenization of a sporulation gene family

Abstract

Saccharomyces genomes are highly collinear and show relatively little structural variation, both within and between species of this yeast genus. We investigated the only common inversion polymorphism known in S. cerevisiae, which affects a 24-kb ‘flip/flop’ region containing 15 genes near the centromere of chromosome XIV. The region exists in two orientations, called reference (REF) and inverted (INV). Meiotic recombination in this region is suppressed in crosses between REF and INV orientation strains such as the BY x RM cross. We find that the inversion polymorphism is at least 17 million years old because it is conserved across the genus Saccharomyces. However, the REF and INV isomers are not ancient alleles but are continually being re-created by re-inversion of the region within each species. Inversion occurs due to continual homogenization of two almost identical 4-kb sequences that form an inverted repeat (IR) at the ends of the flip/flop region. The IR consists of two pairs of genes that are specifically and strongly expressed during the late stages of sporulation. We show that one of these gene pairs, YNL018C/YNL034W, codes for a protein that is essential for spore formation. YNL018C and YNL034W are the founder members of a gene family, Centroid, whose members in other Saccharomycetaceae species evolve fast, duplicate frequently, and are preferentially located close to centromeres. We tested the hypothesis that Centroid genes are a meiotic drive system, but found no support for this idea.

Highly complete long-read genomes reveal pangenomic variation underlying yeast phenotypic diversity

“…S1 ). Of interest, we detected the recently described recurrent inversion of 24 kb on Chr XIV ( Salzberg et al 2022 ); two strains had the reference orientation, and 14 strains had the inversion. We also detected a novel tandem repeat specific to strain YJM454 that amplified the uncharacterized open reading frame (ORF) YGR201C to 27 copies ( Supplemental Fig.…”

VRPG: an interactive visualization framework for reference-projected pangenome graph

“…This flip/flop inversion region is flanked by two 4.2-kb inverted repeat (IR) regions and remains polymorphic in S . cerevisiae and its sister species in the genus Saccharomyces [17]. For example, within S. cerevisiae , our previous study revealed that the Sake strain Y12 shared conserved synteny with the S .…”

Horizontal transfer and recombination fuel Ty4 retrotransposon evolution inSaccharomyces

“…These WGAs were generated mostly with long-read sequencing data (PacBio or ONT), however we also included three WGAs generated with short-read sequencing data for S. cerevisiae that showed evidence of Tsu4 internal regions (strain 245 from (Marsit et al ., 2015); strains AFQ and CDM from (Peter et al ., 2018)) and two WGAs generated with short-read sequencing data for S. arboricola (strain H-6 from (Liti et al ., 2013) and strain ZP960 from (Peris et al ., 2023)) that represent the best available WGAs for this species. In total, we analyzed 183 S. cerevisiae WGAs (Marsit et al ., 2015; Yue et al ., 2017; Peter et al ., 2018; O’Donnell et al ., 2023), 12 S. paradoxus WGAs (Yue et al ., 2017; Eberlein et al ., 2019; Chen et al ., 2022b), two S. mikatae WGAs (this study), two S. jurei WGAs (Naseeb et al ., 2018), three S. kudriavzevii WGAs (Boonekamp et al ., 2018; Salzberg et al ., 2022), two S. arboricola WGAs (Liti et al ., 2013; Peris et al ., 2023), two S. uvarum WGAs (Chen et al ., 2022a; Salzberg et al ., 2022), and four S. eubayanus WGAs (Brickwedde et al ., 2018; Brouwers et al ., 2019; Mardones et al ., 2022).…”