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Review
. 2018 Dec 31;122(7):1085-1101.
doi: 10.1093/aob/mcy130.

Sex and the Flower - Developmental Aspects of Sex Chromosome Evolution

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Free PMC article
Review

Sex and the Flower - Developmental Aspects of Sex Chromosome Evolution

Roman Hobza et al. Ann Bot. .
Free PMC article

Abstract

Background: The evolution of dioecious plants is occasionally accompanied by the establishment of sex chromosomes: both XY and ZW systems have been found in plants. Structural studies of sex chromosomes are now being followed up by functional studies that are gradually shedding light on the specific genetic and epigenetic processes that shape the development of separate sexes in plants.

Scope: This review describes sex determination diversity in plants and the genetic background of dioecy, summarizes recent progress in the investigation of both classical and emerging model dioecious plants and discusses novel findings. The advantages of interspecies hybrids in studies focused on sex determination and the role of epigenetic processes in sexual development are also overviewed.

Conclusions: We integrate the genic, genomic and epigenetic levels of sex determination and stress the impact of sex chromosome evolution on structural and functional aspects of plant sexual development. We also discuss the impact of dioecy and sex chromosomes on genome structure and expression.

Figures

Fig. 1.
Fig. 1.
Schematic functional map of the S. latifolia Y chromosome. Study of individuals with chromosomal aberrations revealed three functional regions on the Y chromosome. (A) Wild-type male. (B) Deletion of a distal section (red) of the p arm led to a hermaphrodite. Thus, this functions as the gynoecium-suppressing functional (GSF) region. (C) A proximal area of the p arm (marked in green) produces an asexual phenotype when deleted. For this reason, it has been designated as the stamen-promoting functional (SPF) region. (D) The region important for further anther development is located near to the SPF region. (E) Deletion of male fertility factors (MFFs) residing mainly on the q arm (light blue) but also in proximity to the SPF region on the p arm leads to male sterility.
Fig. 2.
Fig. 2.
Silene latifolia male and female flower development modification phenomena. Wild-type female (A) and male (B) individual flowers; global view (C) and detail (D) of a flower of a male individual with androhermaphrodite phenotype after zebularine treatment (50 μm). The experimental procedure was otherwise identical to the 5-aza-cytidine experiment by Janousek et al. (1996); flower of female (E) and male (F) individuals infected with M. violaceum.
Fig. 3.
Fig. 3.
Comparison of the evolution of dioecy via one-locus- and two-locus-based models. (A) Model of the origin of dioecy from hermaphroditism via gynodioecy – two-locus model. Recessive male sterility alleles (ms) can be either represented by nuclear recessive mutations or can reflect the absence of the dominant fertility restorer in the case where the male sterility-causing cytoplasm is present in all plants in the population. In the next step, the dominant female-suppressing allele (SuF) is recruited on the proto-Y chromosome. Occasional creation of asexual or hermaphrodite plants via recombination is possible. The cessation of the gynoecium is also influenced by genetic background and environment (sub-dioecy). Finally, the recombination between the female suppressor and the male sterility loci is arrested (as a consequence of divergence due to the accumulation of sexually antagonistic mutations and/or chromosomal inversions) and so the generation of asexual or hermaphrodite plants is avoided. This scheme is based on the original model by Charlesworth and Charlesworth (1978). (B) Alternative model of dioecy evolution from the monoecy – one-locus model. According to this model, the suppressors of gynoecium (SuF) and stamen development (or fertility) (SuM) are already present in the monoecious ancestor and their expression is controlled by intrinsic signals (e.g. hormonal signals connected with apical dominance). Because the strength and direction of the intrinsic signals varies along the plant axis, it results in the upper section carrying male flowers and the bottom part bearing female flowers. In this model, it is thought that there is a threshold value of stimuli separating male and female zones. In this situation, the mutations which are able to modify the effects of internal stimuli can cause an increase or decrease in the size of the male and female zones. Paradioecy (the presence of female flowers in ‘proto-males’ and male flowers in ‘proto-females’) can appear in the intermediate stage (not displayed in this scheme). In the extreme case, one sex can be completely absent in a given plant. Interestingly, if a single master sex-switching locus is recruited near the centromere or other non-recombining region, the sex chromosomes can originate in a single step. This scheme is based on the works by Lloyd (1972a, b, 1975, 1980, 1981), Webb (1999), Renner and Won (2001) and Renner (2016). Note: female flowers are shown in red; male flowers are shown in blue; and hermaphrodite flowers are shown as blue with a red middle part. Sex-linked non-recombining regions are shown as blue ovals.
Fig. 4.
Fig. 4.
Chromosomal localization of repetitive DNA in Silene latifolia (A–C) and Rumex acetosa (D–F) determined by fluorescence in situ hybridization. (A) Microsatellite (CA)15 is accumulated on the Y chromosome (red signal), (B) satellite STAR (red signal) is present in the centromeres of all autosomes and the X chromosome, and satellite X-43.1 (green signal) is gathered in both sub-telomeres of all chromosomes with the exception of the Y chromosome possessing only one sub-telomeric signal, (C) The Ogre LTR retrotransposon (red signal) is ubiquitous on all chromosomes except the Y chromosome. (D) A mixture of all mono-, di- and trinucleotide microsatellites (red signal) shows strong accumulation along both Y chromosomes. (E) The (TA)15 microsatellite (red signal) gives a signal at several discrete loci on both Y chromosomes, and the RAYSI satellite (green signal) is present at the distal regions of both Y chromosomes. (F) The Maximus/SIRE LTR retrotransposon (red signal) covers all autosomes and the X chromosome except telomeres/sub-telomeres, but is absent from both Y chromosomes; the RAYSI satellite is localized at several discrete loci on both Y chromosomes (green signal). Scale bars indicate 10 μm.

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