Sex chromosome evolution in haploid plants: Microchromosomes, disappearing chromosomes, and giant chromosomes

Abstract

As in many diploid organisms with genetic sex determination, haploid-dominant organisms have also evolved sex chromosomes or extensive genomic regions that lack genetic recombination. An understanding of sex chromosome evolution should explain the causes and consequences of such regions in both diploids and haploids. However, haploids have been little studied, even though differences from sex chromosomes in diploids carry implications concerning the evolution of suppressed recombination in diploid organisms, and make predictions about genome evolution in the sex-linked regions of haploids that can now be tested by approaches using genome sequences. I review these ideas, and the current empirical evidence concerning them, in more detail than recent reviews focusing on progress in understanding the mechanisms involved in sex determination. I also discuss evidence that one specific prediction, that genetic degeneration should be minor in haploids, is not upheld. I suggest that this prediction does not take account of all processes leading to gene loss from sex-linked regions and that profound degeneration may evolve if sex-linked genes become duplicated to autosomes, a process that also appears to occur in diploids. I emphasize types of data that are needed to make progress in testing several of the ideas described.

Keywords: duplication; genetic degeneration; microchromosomes; recombination; turnovers.

Fig. 1.

Diagram to show the life-cycle stages in plants with haploid-dominant plants, such bryophytes, with separate sexes (termed dioicous), and the intact inheritance, without recombination, of both the male and female-determining fully sex-linked regions (unlike the situation in diploid organisms with genetic sex determination, in which recombination occurs in the homogametic sex, XX in species in which males are the heterozygous sex, so that only the Y-linked region fails to recombine). In haploids, as in diploids, the autosomes recombine. In some angiosperms, however, recombination is infrequent in extensive pericentromeric regions, which form distinctive repeat-rich genomic regions of compartments on each chromosome, with correspondingly low gene densities. As outlined in the text, current evidence from bryophytes does not suggest the presence of extensive pericentromeric regions.

Fig. 2.

Numbers of genes annotated on all chromosomes in five liverwort (Marchantiales, in the two Left-hand columns) and five moss species, with the sex chromosome colored in blue for the V and pink for the U; green indicates that the sex of the sequenced individual is unknown. The four liverwort species shown at the top have n = 9 chromosomes, and the M. polymorpha UV pair is chromosome 9, and the homologous chromosome in the monoicous Ricciocarpos natans is probably derived from this V (for Lunularia cruciata, the diagram shows chromosome sizes, as gene numbers are also unknown). In Riccia cavernosa and Riccia fluitans, no chromosome 9 is found, though chromosome 9 genes are found on autosomes, and chromosome 5 is small. In the moss species, the sexes are known only in C. purpureus. (For species not mentioned in the text, information is in refs. and , and GenBank accession number GCA_948567375.1).

Fig. 3.

Diagram to show how part of a sex chromosome can become deleted after “movements” of sex-linked genes to autosomes, through initial duplication, followed by loss of the progenitors from the sex-linked region (see text).