Genomic structure and evolution of the mating type locus in the green seaweed Ulva partita

Tomokazu Yamazaki,Ryogo Suzuki,Shinichi Miyamura,Shigeyuki Kawano,Yutaka Suzuki,Masahira Hattori,Sumio Sugano,Kazuyoshi Kuwano,Kensuke Ichihara,Atsushi Toyoda,Kenshiro Oshima

doi:10.1038/s41598-017-11677-0

Abstract

The evolution of sex chromosomes and mating loci in organisms with UV systems of sex/mating type determination in haploid phases via genes on UV chromosomes is not well understood. We report the structure of the mating type (MT) locus and its evolutionary history in the green seaweed Ulva partita, which is a multicellular organism with an isomorphic haploid-diploid life cycle and mating type determination in the haploid phase. Comprehensive comparison of a total of 12.0 and 16.6 Gb of genomic next-generation sequencing data for mt− and mt+ strains identified highly rearranged MT loci of 1.0 and 1.5 Mb in size and containing 46 and 67 genes, respectively, including 23 gametologs. Molecular evolutionary analyses suggested that the MT loci diverged over a prolonged period in the individual mating types after their establishment in an ancestor. A gene encoding an RWP-RK domain-containing protein was found in the mt− MT locus but was not an ortholog of the chlorophycean mating type determination gene MID. Taken together, our results suggest that the genomic structure and its evolutionary history in the U. partita MT locus are similar to those on other UV chromosomes and that the MT locus genes are quite different from those of Chlorophyceae.

Highlights

Sexual reproduction systems in eukaryotes can be divided into two types, in terms of determining sex/mating type in the haploid phase (UV systems) or in the diploid phase (XY/ZW systems)[1]
The highly adjacent mating type-specific (MTS) region was located in the middle of mt− scaffold 632 over ~1.0 Mb, and this region was well mapped using short-read nucleotide sequences generated from the mt−, but not the mt+, genome and RNA-seq reads (Supplementary Fig. 3, 4th and 5th lanes)
The size of the U. partita mating type (MT) locus (~1.0–1.5 Mb; Fig. 1 and 2) resembles that of the sex-determining regions (SDRs) of Volvox, which is a UV system with a dominating haploid phase in a life cycle showing phasic heteromorphism and gamete dimorphism, and the brown alga Ectocarpus, which is a UV system with a haploid-diploid life cycle with phasic heteromorphism and gamete dimorphism[9,17]

Summary

Introduction

Sexual reproduction systems in eukaryotes can be divided into two types, in terms of determining sex/mating type in the haploid phase (UV systems) or in the diploid phase (XY/ZW systems)[1]. In the XY/ZW systems of mammals, insects, and plants, the structures of XY/ZW chromosomes and their evolution correspond reasonably well with predictions based on population genetics theory, whereby the suppressed recombination of the two chromosomes results in degeneration through Muller’s ratchet, background selection, the Hill-Robertson effect with weak selection, and the “hitchhiking” of deleterious alleles along with favorable mutations[2,3] These theoretical predictions are constructed under the postulate that both sex chromosomes (XY or ZW) are heterozygous in the diploid phase and that they are distributed separately into the gametes (egg and sperm) via meiosis. With regard to green algal evolution, it is of interest to examine the conservation of MID among the distinct taxonomic classes Chlorophyceae and Ulvophyceae

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