Most cited article - PubMed ID 8602166
Epigenetic control of sexual phenotype in a dioecious plant, Melandrium album
Sex chromosomes have evolved in many plant species with separate sexes. Current plant research is shifting from examining the structure of sex chromosomes to exploring their functional aspects. New studies are progressively unveiling the specific genetic and epigenetic mechanisms responsible for shaping distinct sexes in plants. While the fundamental methods of molecular biology and genomics are generally employed for the analysis of sex chromosomes, it is often necessary to modify classical procedures not only to simplify and expedite analyses but sometimes to make them possible at all. In this review, we demonstrate how, at the level of structural and functional genetics, cytogenetics, and bioinformatics, it is essential to adapt established procedures for sex chromosome analysis.
- Keywords
- Bioinformatics, chromosome dissection, cytogenetics, dioecious plants, epigenetics, functional genetics, sex chromosomes, tandem repeats, transposable elements,
- MeSH
- Chromosomes, Plant * genetics MeSH
- Sex Chromosomes * genetics MeSH
- Plants genetics MeSH
- Computational Biology methods MeSH
- Publication type
- Journal Article MeSH
- Review MeSH
In a minority of flowering plants, separate sexes are genetically determined by sex chromosomes. The Y chromosome has a non-recombining region that degenerates, causing a reduced expression of Y genes. In some species, the lower Y expression is accompanied by dosage compensation (DC), a mechanism that re-equalizes male and female expression and/or brings XY male expression back to its ancestral level. Here, we review work on DC in plants, which started as early as the late 1960s with cytological approaches. The use of transcriptomics fired a controversy as to whether DC existed in plants. Further work revealed that various plants exhibit partial DC, including a few species with young and homomorphic sex chromosomes. We are starting to understand the mechanisms responsible for DC in some plants, but in most species, we lack the data to differentiate between global and gene-by-gene DC. Also, it is unknown why some species evolve many dosage compensated genes while others do not. Finally, the forces that drive DC evolution remain mysterious, both in plants and animals. We review the multiple evolutionary theories that have been proposed to explain DC patterns in eukaryotes with XY or ZW sex chromosomes. This article is part of the theme issue 'Sex determination and sex chromosome evolution in land plants'.
- Keywords
- Y degeneration, cis-regulatory sequence divergence, dosage balance, dosage-sensitive genes, imprinting, sex chromosomes,
- MeSH
- Dosage Compensation, Genetic * MeSH
- Evolution, Molecular MeSH
- Sex Chromosomes * genetics MeSH
- Plants genetics MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Review MeSH
Switches in heterogamety are known to occur in both animals and plants. Although plant sex determination systems probably often evolved more recently than those in several well-studied animals, including mammals, and have had less time for switches to occur, we previously detected a switch in heterogamety in the plant genus Silene: section Otites has both female and male heterogamety, whereas S. latifolia and its close relatives, in a different section of the genus, Melandrium (subgenus Behenantha), all have male heterogamety. Here we analyse the evolution of sex chromosomes in section Otites, which is estimated to have evolved only about 0.55 MYA. Our study confirms female heterogamety in S. otites and newly reveals female heterogamety in S. borysthenica. Sequence analyses and genetic mapping show that the sex-linked regions of these two species are the same, but the region in S. colpophylla, a close relative with male heterogamety, is different. The sex chromosome pairs of S. colpophylla and S. otites each correspond to an autosome of the other species, and both differ from the XY pair in S. latifolia. Silene section Otites species are suitable for detailed studies of the events involved in such changes, and our phylogenetic analysis suggests a possible change from female to male heterogamety within this section. Our analyses suggest a possibility that has so far not been considered, change in heterogamety through hybridization, in which a male-determining chromosome from one species is introgressed into another one, and over-rides its previous sex-determining system.
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.
BACKGROUND: S. latifolia is a model organism for the study of sex chromosome evolution in plants. Its sex chromosomes include large regions in which recombination became gradually suppressed. The regions tend to expand over time resulting in the formation of evolutionary strata. Non-recombination and later accumulation of repetitive sequences is a putative cause of the size increase in the Y chromosome. Gene decay and accumulation of repetitive DNA are identified as key evolutionary events. Transposons in the X and Y chromosomes are distributed differently and there is a regulation of transposon insertion by DNA methylation of the target sequences, this points to an important role of DNA methylation during sex chromosome evolution in Silene latifolia. The aim of this study was to elucidate whether the reduced expression of the Y allele in S. latifolia is caused by genetic degeneration or if the cause is methylation triggered by transposons and repetitive sequences. RESULTS: Gene expression analysis in S. latifolia males has shown expression bias in both X and Y alleles. To determine whether these differences are caused by genetic degeneration or methylation spread by transposons and repetitive sequences, we selected several sex-linked genes with varying degrees of degeneration and from different evolutionary strata. Immunoprecipitation of methylated DNA (MeDIP) from promoter, exon and intron regions was used and validated through bisulfite sequencing. We found DNA methylation in males, and only in the promoter of genes of stratum I (older). The Y alleles in genes of stratum I were methylation enriched compared to X alleles. There was also abundant and high percentage methylation in the CHH context in most sequences, indicating de novo methylation through the RdDM pathway. CONCLUSIONS: We speculate that TE accumulation and not gene decay is the cause of DNA methylation in the S. latifolia Y sex chromosome with influence on the process of heterochromatinization.
- Keywords
- DNA methylation, Epigenetics, Immunoprecipitation, Sex chromosomes, Sex-linked genes, Silene latifolia, Sodium bisulfite, Y degeneration,
- MeSH
- Chromosomes, Plant * MeSH
- DNA, Plant chemistry MeSH
- Gene Expression MeSH
- Plant Leaves metabolism MeSH
- DNA Methylation * MeSH
- Evolution, Molecular * MeSH
- Sequence Homology, Nucleic Acid MeSH
- Silene genetics metabolism MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- DNA, Plant MeSH
Transient 5-azacytidine treatment of leaf explants from potato plants with transcriptionally silenced transgenes allows de novo regeneration of plants with restored transgene expression at the whole plant level. Transgenes introduced into plant genomes frequently become silenced either at the transcriptional or the posttranscriptional level. Transcriptional silencing is usually associated with DNA methylation in the promoter region. Treatments with inhibitors of maintenance DNA methylation were previously shown to allow reactivation of transcriptionally silenced transgenes in single cells or tissues, but not at the whole plant level. Here we analyzed the effect of DNA methylation inhibitor 5-azacytidine (AzaC) on the expression of two silenced reporter genes encoding green fluorescent protein (GFP) and neomycin phosphotransferase (NPTII) in potato plants. Whereas no obvious reactivation was observed in AzaC-treated stem cuttings, transient treatment of leaf segments with 10 μM AzaC and subsequent de novo regeneration of shoots on the selective medium with kanamycin resulted in the production of whole plants with clearly reactivated expression of previously silenced transgenes. Reactivation of nptII expression was accompanied by a decrease in cytosine methylation in the promoter region of the gene. Using the plants with reactivated GFP expression, we found that re-silencing of this transgene can be accidentally triggered by de novo regeneration. Thus, testing the incidence of transgene silencing during de novo regeneration could be a suitable procedure for negative selection of transgenic lines (insertion events) which have an inclination to be silenced. Based on our analysis of non-specific inhibitory effects of AzaC on growth of potato shoots in vitro, we estimated that AzaC half-life in the culture media is approximately 2 days.
- Keywords
- 5-Azacytidine, De novo regeneration, Methylation, Reactivation, TGS, Transgene silencing,
- MeSH
- Azacitidine pharmacology MeSH
- Plants, Genetically Modified drug effects genetics metabolism MeSH
- DNA Methylation drug effects genetics MeSH
- Gene Expression Regulation, Plant drug effects genetics MeSH
- Solanum tuberosum drug effects genetics metabolism MeSH
- Transgenes drug effects genetics MeSH
- Gene Silencing MeSH
- Green Fluorescent Proteins genetics metabolism MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Azacitidine MeSH
- Green Fluorescent Proteins MeSH
