On the Questionable Existence of Sex Chromosomes in the Angiosperms

Abstract Degenerative mutations in non-recombining regions, such as in sex chromosomes, may lead to differential expression between alleles if mutations occur stochastically in one or the other allele. Reduced allelic expression due to degeneration has indeed been suggested to occur in various sex-chromosome systems. However, whether an association occurs between specific signatures of degeneration and differential expression between alleles has not been extensively tested, and sexual antagonism can also cause differential expression on sex chromosomes. The anther-smut fungus Microbotryum lychnidis-dioicae is ideal for testing associations between specific degenerative signatures and differential expression because 1) there are multiple evolutionary strata on the mating-type chromosomes, reflecting successive recombination suppression linked to mating-type loci; 2) separate haploid cultures of opposite mating types help identify differential expression between alleles; and 3) there is no sexual antagonism as a confounding factor accounting for differential expression. We found that differentially expressed genes were enriched in the four oldest evolutionary strata compared with other genomic compartments, and that, within compartments, several signatures of sequence degeneration were greater for differentially expressed than non-differentially expressed genes. Two particular degenerative signatures were significantly associated with lower expression levels within differentially expressed allele pairs: upstream insertion of transposable elements and mutations truncating the protein length. Other degenerative mutations associated with differential expression included nonsynonymous substitutions and altered intron or GC content. The association between differential expression and allele degeneration is relevant for a broad range of taxa where mating compatibility or sex is determined by genes located in large regions where recombination is suppressed.

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Evolution of Sex Chromosome Heteromorphy in Geographic Populations of the Japanese Tago’s Brown Frog Complex

Cytogenetic and Genome Research ◽

10.1159/000512964 ◽

2021 ◽

pp. 1-9

Author(s):

Chiao Kuwana ◽

Hiroyuki Fujita ◽

Masataka Tagami ◽

Takanori Matsuo ◽

Ikuo Miura

Keyword(s):

Sex Chromosomes ◽

Sex Chromosome ◽

Mitochondrial Gene ◽

Population Level ◽

Chromosome 7 ◽

Geographic Population ◽

Geographic Populations ◽

Western Japan ◽

Brown Frog ◽

Eastern Japan

The sex chromosomes of most anuran amphibians are characterized by homomorphy in both sexes, and evolution to heteromorphy rarely occurs at the species or geographic population level. Here, we report sex chromosome heteromorphy in geographic populations of the Japanese Tago’s brown frog complex (2n = 26), comprising Rana sakuraii and R. tagoi. The sex chromosomes of R. sakuraii from the populations in western Japan were homomorphic in both sexes, whereas chromosome 7 from the populations in eastern Japan were heteromorphic in males. Chromosome 7 of R. tagoi, which is distributed close to R. sakuraii in eastern Japan, was highly similar in morphology to the Y chromosome of R. sakuraii. Based on this and on mitochondrial gene sequence analysis, we hypothesize that in the R. sakuraii populations from eastern Japan the XY heteromorphic sex chromosome system was established by the introduction of chromosome 7 from R. tagoi via interspecies hybridization. In contrast, chromosome 13 of R. tagoi from the 2 large islands in western Japan, Shikoku and Kyushu, showed a heteromorphic pattern of constitutive heterochromatin distribution in males, while this pattern was homomorphic in females. Our study reveals that sex chromosome heteromorphy evolved independently at the geographic lineage level in this species complex.

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