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Recurrent allopolyploidization, Y-chromosome introgression and the evolution of sexual systems in the plant genus Mercurialis.

ABSTRACT: The plant genus Mercurialis includes dioecious, monoecious and androdioecious species (where males coexist with hermaphrodites). Its diversification involved reticulate evolution via hybridization and polyploidization. The Y chromosome of the diploid species Mercurialis annua shows only mild signs of degeneration. We used sequence variation at a Y-linked locus in several species and at multiple autosomal and pseudoautosomal loci to investigate the origin and evolution of the Y chromosome across the genus. Our study provides evidence for further cases of allopolyploid speciation. It also reveals that all lineages with separate sexes (with one possible exception) share the same ancestral Y chromosome. Surprisingly, males in androdioecious populations of hexaploid M. annua carry a Y chromosome that is not derived from either of its two putative progenitor lineages but from a more distantly related perennial dioecious lineage via introgression. These results throw new light on the evolution of sexual systems and polyploidy in Mercurialis and secure it as a promising model for further study of plant sex chromosomes. This article is part of the theme issue 'Sex determination and sex chromosome evolution in land plants'.

SUBMITTER: Gerchen JF

PROVIDER: S-EPMC8935306 | biostudies-literature | 2022 May

REPOSITORIES: biostudies-literature

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Recurrent allopolyploidization, Y-chromosome introgression and the evolution of sexual systems in the plant genus Mercurialis.

Gerchen J F JF Veltsos P P Pannell J R JR

Philosophical transactions of the Royal Society of London. Series B, Biological sciences 20220321 1850

The plant genus Mercurialis includes dioecious, monoecious and androdioecious species (where males coexist with hermaphrodites). Its diversification involved reticulate evolution via hybridization and polyploidization. The Y chromosome of the diploid species Mercurialis annua shows only mild signs of degeneration. We used sequence variation at a Y-linked locus in several species and at multiple autosomal and pseudoautosomal loci to investigate the origin and evolution of the Y chro ...[more]

PMID: 35306889

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Project description:Genome rearrangements are associated with eukaryotic evolutionary processes ranging from tumorigenesis to speciation. Such rearrangements are especially common following the shock of interspecific hybridization, and some of these could be expected to have strong selective value. To test this expectation we created de novo interspecific yeast hybrids between two diverged but largely syntenic species, Saccharomyces cerevisiae and S. uvarum, then experimentally evolved them under continuous ammonium limitation. We discovered that a characteristic interspecific genome rearrangement arose multiple times in independently evolved populations. We uncovered nine different breakpoints, all occurring in a ~1 kb region of chromosome 14, and all producing an “interspecific fusion junction” within the MEP2 gene coding sequence, such that the 5’ portion derives from S. cerevisiae and the 3’ portion derives from S. uvarum. In most cases the rearrangements altered both chromosomes, resulting in what can be considered to be an introgression of a several-kb region of S. uvarum into an otherwise intact S. cerevisiae chromosome 14, while the S. uvarum chromosome 14 experienced an interspecific reciprocal translocation at the same breakpoint within MEP2, yielding a chimaeric chromosome. The net result is the presence in the cell of two MEP2 fusion genes having identical breakpoints. Given that MEP2 encodes for a high-affinity ammonium permease, that MEP2 fusion genes arise repeatedly under ammonium-limitation, and that three independent evolved isolates carrying MEP2 fusion genes are each more fit than their common ancestor, the novel MEP2 fusion genes are very likely adaptive under ammonium limitation. Our results suggest that when homoploid hybrids form, the admixture of two genomes enables swift and otherwise unlikely evolutionary innovations. Furthermore, the architecture of the MEP2 rearrangement suggests a model for rapid introgression, a phenomenon seen in numerous eukaryotic phyla, that does not invoke repeated backcrossing to one of the parental species. Nomenclature: GSY86 TimeZeroInoculum = ancestral interspecific hybrid used to inoculate ammonium-limited chemostats into 3 replicate vessels A, B, C. 150gen = various single-clone isolates from 150 generations of evolutions from vessels A, B or C. 200gen = various isolates from 200 generations of evolutions from vessels A, B or C.

Dataset Information

Recurrent allopolyploidization, Y-chromosome introgression and the evolution of sexual systems in the plant genus Mercurialis.

Publications

Recurrent allopolyploidization, Y-chromosome introgression and the evolution of sexual systems in the plant genus <i>Mercurialis</i>.

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