Translocation heterozygosity and the origin of dioecy in Viscum

Abstract

SUMMARYSex-associated and floating translocation complexes are characteristic of dioecious species of Viscum, but are virtually absent in monoecious species. In most of the dioecious species, fixed sex-associated translocation complexes are present, with the male being the heterozygous sex. The sex-associated multivalent is usually 04 (ring-of-four) or 06, rarely 08. In only a few of the dioecious species are sex-associated translocations not apparent. Most of the dioecious species are also polymorphic for floating translocations, producing one or more additional multivalents ranging from 04 to 012. Floacing translocations may be more frequent in species which do not have sex-associated translocations. Supernumerary chromosomes are also present in several species. Sex ratios are at unity in most dioecious species, but female-biased ratios as low as 052 and male-biased ratios as high as 140 may occur in some species. The high correlation between dioecy and translocation heterozygosity suggests that translocations are primarily associated with the origin and establishment of dioecy, and any role they play in the maintenance of biased sex ratios through meiotic drive is probably secondary. A model is presented in which male-and female-determining factors are non-alIelic, and sex-associated translocations serve to stabilise dioecy by bringing the sex factors into linkage.Subsequent structural rearrangements within a sex-associated translocation complex may bring the sex factors together in one chromosome pair, releasing floating translocations. The high frequencies of floating translocation heterozygosity in some species indicate that such heterozygosity has adaptive value.

The orientation behaviour of multiple chromosome configurations in acridid grasshoppers

“…Heterozygous interchanges may form a permanent feature of the meiotic mechanism in one of three situations: (i) as a system of permanent heterozygosity in which, in a given population, all individuals, regardless of sex, develop multiple configurations at meiosis (Cleland 1972); (ii) in the form of a persistent polymorphism where multiples are present in a proportion of both sexes within a population (John 1983); and (iii) as a sex-linked and sex-limited system of heterozygosity where multiples occur only in the heterogametic sex and include a sex-linked component (Wiens and Barlow 1979;Procunier 1982;Rowel1 1985). In sexually reproducing species all these situations are characterized by three universal meiotic properties: (i) the partially homologous members of the interchange system regularly associate in the form of the maximum, ring or chain, multiple; (ii) the chiasmata necessary for maintaining the maximum multiple are excluded from the segments between the centromeres and the sites of exchange, the so-called interstitial segments of simple interchange multiples; and (iii) the maximum multiple consistently orients at first metaphase in such a way that in a high frequency of meiocytes (>70%) all the noninterchanged members move to one pole at first anaphase with the interchanged chromosomes all passing to the opposite pole.…”

Permanent translocation heterozygosity in dioecious Baccharis coridifolia DC. (Asteraceae)

“…In some dioecious plants permanent translocation heterozygosity has been produced, at least in the male sex, through the association of the translocations with the sex determination system and a translocation multivalent is characteristic of the heterozygous sex (B arlow 1981). The mistletoe genus Viscum shows permanent sex‐associated translocation heterozygosity in most of its dioecious species, distributed through Africa, Europe and Asia ( Wiens and Barlow 1973, 1975; W iens and B arlow 1979; B arlow and W iens 1975, 1976; B arlow et al 1978; B arlow 1981; B arlow and M artin 1984). In these species male plants have a multivalent at meiosis, ranging from 4 to 6, 8, 10 or 12 chromosomes.…”

Revisiting the Dioecy-Polyploidy Association: Alternate Pathways and Research Opportunities

“…Transposition of genes can also lead to novel expression patterns and phenotypes [Muñoz and Sankoff, 2012], including loss of function phenotypes (male and female sterile plants). Translocations and inversions could not only lead to male sterility (or female sterility), but translocations can bring male and female sterility loci together [Wiens and Barlow, 1979;Goldberg et al, 2010], and rearrangements can reduce recombination. As linkage between male and female sterility loci and recombination suppression between them are key features of nascent sex chromosomes [see Ming et al, 2011 for review], genomic rearrangements can facilitate the creation of a sex-determining region.…”