Plant sex determination and sex chromosomes

For centuries scientists have been intrigued by the origin of dioecy in plants, characterizing sex-specific development, uncovering cytological differences between the sexes, and developing theoretical models. However, through the invention and continued improvements in genomic technologies, we have truly begun to unlock the genetic basis of dioecy in many species. Here we broadly review the advances in research on dioecy and sex chromosomes. We start by first discussing the early works that built the foundation for current studies and the advances in genome sequencing that have facilitated more-recent findings. We next discuss the analyses of sex chromosomes and sex-determination genes uncovered by genome sequencing. We synthesize these results to find some patterns are emerging, such as the role of duplications, the involvement of hormones in sex-determination, and support for the two-locus model for the origin of dioecy. Though across systems, there also many novel insights into how sex chromosomes evolve, including different sex-determining genes and routes to suppressed recombination. We propose the future of research in plant sex chromosomes should involve interdisciplinary approaches, combining cutting-edge technologies with the classics to unravel the patterns that can be found across the hundreds of independent origins.

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The Diversity of Plant Sex Chromosomes Highlighted through Advances in Genome Sequencing

Genes ◽

10.3390/genes12030381 ◽

2021 ◽

Vol 12 (3) ◽

pp. 381

Author(s):

Sarah Carey ◽

Qingyi Yu ◽

Alex Harkess

Keyword(s):

Sex Determination ◽

Genome Sequencing ◽

Sex Chromosomes ◽

Theoretical Models ◽

Genomic Technologies ◽

Interdisciplinary Approaches ◽

Suppressed Recombination ◽

Plant Sex Chromosomes ◽

Plant Sex

For centuries, scientists have been intrigued by the origin of dioecy in plants, characterizing sex-specific development, uncovering cytological differences between the sexes, and developing theoretical models. Through the invention and continued improvements in genomic technologies, we have truly begun to unlock the genetic basis of dioecy in many species. Here we broadly review the advances in research on dioecy and sex chromosomes. We start by first discussing the early works that built the foundation for current studies and the advances in genome sequencing that have facilitated more-recent findings. We next discuss the analyses of sex chromosomes and sex-determination genes uncovered by genome sequencing. We synthesize these results to find some patterns are emerging, such as the role of duplications, the involvement of hormones in sex-determination, and support for the two-locus model for the origin of dioecy. Though across systems, there are also many novel insights into how sex chromosomes evolve, including different sex-determining genes and routes to suppressed recombination. We propose the future of research in plant sex chromosomes should involve interdisciplinary approaches, combining cutting-edge technologies with the classics to unravel the patterns that can be found across the hundreds of independent origins.

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The Diversity and Evolution of Sex Chromosomes in Frogs

Genes ◽

10.3390/genes12040483 ◽

2021 ◽

Vol 12 (4) ◽

pp. 483

Author(s):

Wen-Juan Ma ◽

Paris Veltsos

Keyword(s):

Sex Determination ◽

Sex Chromosomes ◽

Chromosome Evolution ◽

Sex Chromosome ◽

Comparative Genomic ◽

Ancestral State ◽

Heteromorphic Sex Chromosomes ◽

Genomic Studies ◽

Evolutionary Trajectories ◽

Heterogametic Sex

Frogs are ideal organisms for studying sex chromosome evolution because of their diversity in sex chromosome differentiation and sex-determination systems. We review 222 anuran frogs, spanning ~220 Myr of divergence, with characterized sex chromosomes, and discuss their evolution, phylogenetic distribution and transitions between homomorphic and heteromorphic states, as well as between sex-determination systems. Most (~75%) anurans have homomorphic sex chromosomes, with XY systems being three times more common than ZW systems. Most remaining anurans (~25%) have heteromorphic sex chromosomes, with XY and ZW systems almost equally represented. There are Y-autosome fusions in 11 species, and no W-/Z-/X-autosome fusions are known. The phylogeny represents at least 19 transitions between sex-determination systems and at least 16 cases of independent evolution of heteromorphic sex chromosomes from homomorphy, the likely ancestral state. Five lineages mostly have heteromorphic sex chromosomes, which might have evolved due to demographic and sexual selection attributes of those lineages. Males do not recombine over most of their genome, regardless of which is the heterogametic sex. Nevertheless, telomere-restricted recombination between ZW chromosomes has evolved at least once. More comparative genomic studies are needed to understand the evolutionary trajectories of sex chromosomes among frog lineages, especially in the ZW systems.

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Cytogenetic Analysis of the Asian Box Turtles of the Genus Cuora (Testudines, Geoemydidae)

Genes ◽

10.3390/genes12020156 ◽

2021 ◽

Vol 12 (2) ◽

pp. 156

Author(s):

Lorenzo Clemente ◽

Sofia Mazzoleni ◽

Eleonora Pensabene ◽

Tomáš Protiva ◽

Philipp Wagner ◽

...

Keyword(s):

Sex Determination ◽

Sex Chromosomes ◽

Wide Distribution ◽

Iucn Red List ◽

Telomeric Repeats ◽

Rdna Loci ◽

Box Turtles ◽

Genotypic Sex Determination ◽

Poorly Differentiated ◽

Almost All

The Asian box turtle genus Cuora currently comprises 13 species with a wide distribution in Southeast Asia, including China and the islands of Indonesia and Philippines. The populations of these species are rapidly declining due to human pressure, including pollution, habitat loss, and harvesting for food consumption. Notably, the IUCN Red List identifies almost all species of the genus Cuora as Endangered (EN) or Critically Endangered (CR). In this study, we explore the karyotypes of 10 Cuora species with conventional (Giemsa staining, C-banding, karyogram reconstruction) and molecular cytogenetic methods (in situ hybridization with probes for rDNA loci and telomeric repeats). Our study reveals a diploid chromosome number of 2n = 52 chromosomes in all studied species, with karyotypes of similar chromosomal morphology. In all examined species, rDNA loci are detected at a single medium-sized chromosome pair and the telomeric repeats are restricted to the expected terminal position across all chromosomes. In contrast to a previous report, sex chromosomes are neither detected in Cuoragalbinifrons nor in any other species. Therefore, we assume that these turtles have either environmental sex determination or genotypic sex determination with poorly differentiated sex chromosomes. The conservation of genome organization could explain the numerous observed cases of interspecific hybridization both within the genus Cuora and across geoemydid turtles.

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The maintenance of polygenic sex determination depends on the dominance of fitness effects which are predictive of the role of sexual antagonism

G3 Genes|Genome|Genetics ◽

10.1093/g3journal/jkab149 ◽

2021 ◽

Author(s):

Richard P Meisel

Keyword(s):

Sex Determination ◽

Sex Chromosomes ◽

House Fly ◽

Sexual Antagonism ◽

Antagonistic Effects ◽

Fitness Effects ◽

Y Chromosomes ◽

Sexually Antagonistic Selection ◽

The Individual ◽

Polygenic Sex Determination

Abstract In species with polygenic sex determination, multiple male- and female-determining loci on different proto-sex chromosomes segregate as polymorphisms within populations. The extent to which these polymorphisms are at stable equilibria is not yet resolved. Previous work demonstrated that polygenic sex determination is most likely to be maintained as a stable polymorphism when the proto-sex chromosomes have opposite (sexually antagonistic) fitness effects in males and females. However, these models usually consider polygenic sex determination systems with only two proto-sex chromosomes, or they do not broadly consider the dominance of the alleles under selection. To address these shortcomings, I used forward population genetic simulations to identify selection pressures that can maintain polygenic sex determination under different dominance scenarios in a system with more than two proto-sex chromosomes (modeled after the house fly). I found that overdominant fitness effects of male-determining proto-Y chromosomes are more likely to maintain polygenic sex determination than dominant, recessive, or additive fitness effects. The overdominant fitness effects that maintain polygenic sex determination tend to have proto-Y chromosomes with sexually antagonistic effects (male-beneficial and female-detrimental). In contrast, dominant fitness effects that maintain polygenic sex determination tend to have sexually antagonistic multi-chromosomal genotypes, but the individual proto-sex chromosomes do not have sexually antagonistic effects. These results demonstrate that sexual antagonism can be an emergent property of the multi-chromosome genotype without individual sexually antagonistic chromosomes. My results further illustrate how the dominance of fitness effects has consequences for both the likelihood that polygenic sex determination will be maintained as well as the role sexually antagonistic selection is expected to play in maintaining the polymorphism.

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A 180 Myr-old female-specific genome region in sturgeon reveals the oldest known vertebrate sex determining system with undifferentiated sex chromosomes

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2020.0089 ◽

2021 ◽

Vol 376 (1832) ◽

pp. 20200089

Author(s):

Heiner Kuhl ◽

Yann Guiguen ◽

Christin Höhne ◽

Eva Kreuz ◽

Kang Du ◽

...

Keyword(s):

Sex Determination ◽

Sex Chromosomes ◽

Sex Chromosome ◽

Specific Sequence ◽

Genome Region ◽

Acipenser Ruthenus ◽

Determination System ◽

Sex Determination System ◽

Female Specific ◽

Polyploidization Event

Several hypotheses explain the prevalence of undifferentiated sex chromosomes in poikilothermic vertebrates. Turnovers change the master sex determination gene, the sex chromosome or the sex determination system (e.g. XY to WZ). Jumping master genes stay main triggers but translocate to other chromosomes. Occasional recombination (e.g. in sex-reversed females) prevents sex chromosome degeneration. Recent research has uncovered conserved heteromorphic or even homomorphic sex chromosomes in several clades of non-avian and non-mammalian vertebrates. Sex determination in sturgeons (Acipenseridae) has been a long-standing basic biological question, linked to economical demands by the caviar-producing aquaculture. Here, we report the discovery of a sex-specific sequence from sterlet ( Acipenser ruthenus ). Using chromosome-scale assemblies and pool-sequencing, we first identified an approximately 16 kb female-specific region. We developed a PCR-genotyping test, yielding female-specific products in six species, spanning the entire phylogeny with the most divergent extant lineages ( A. sturio, A. oxyrinchus versus A. ruthenus, Huso huso ), stemming from an ancient tetraploidization. Similar results were obtained in two octoploid species ( A. gueldenstaedtii, A. baerii ). Conservation of a female-specific sequence for a long period, representing 180 Myr of sturgeon evolution, and across at least one polyploidization event, raises many interesting biological questions. We discuss a conserved undifferentiated sex chromosome system with a ZZ/ZW-mode of sex determination and potential alternatives. This article is part of the theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part I)’.

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Do male and female heterogamety really differ in expression regulation? Lack of global dosage balance in pygopodid geckos

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2020.0102 ◽

2021 ◽

Vol 376 (1833) ◽

pp. 20200102 ◽

Cited By ~ 2

Author(s):

Michail Rovatsos ◽

Tony Gamble ◽

Stuart V. Nielsen ◽

Arthur Georges ◽

Tariq Ezaz ◽

...

Keyword(s):

Sex Determination ◽

Sex Chromosomes ◽

Gene Dosage ◽

Regulatory Mechanisms ◽

Gene Copy ◽

Male And Female ◽

Gene Dose ◽

Female Heterogamety ◽

Dosage Balance ◽

Male Heterogamety

Differentiation of sex chromosomes is thought to have evolved with cessation of recombination and subsequent loss of genes from the degenerated partner (Y and W) of sex chromosomes, which in turn leads to imbalance of gene dosage between sexes. Based on work with traditional model species, theory suggests that unequal gene copy numbers lead to the evolution of mechanisms to counter this imbalance. Dosage compensation, or at least achieving dosage balance in expression of sex-linked genes between sexes, has largely been documented in lineages with male heterogamety (XX/XY sex determination), while ZZ/ZW systems are assumed to be usually associated with the lack of chromosome-wide gene dose regulatory mechanisms. Here, we document that although the pygopodid geckos evolved male heterogamety with a degenerated Y chromosome 32–72 Ma, one species in particular, Burton's legless lizard ( Lialis burtonis ), does not possess dosage balance in the expression of genes in its X-specific region. We summarize studies on gene dose regulatory mechanisms in animals and conclude that there is in them no significant dichotomy between male and female heterogamety. We speculate that gene dose regulatory mechanisms are likely to be related to the general mechanisms of sex determination instead of type of heterogamety. This article is part of the theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part II)’.

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ZZ/ZW Sex Determination with Multiple Neo-Sex Chromosomes is Common in Madagascan Chameleons of the Genus Furcifer (Reptilia: Chamaeleonidae)

Genes ◽

10.3390/genes10121020 ◽

2019 ◽

Vol 10 (12) ◽

pp. 1020 ◽

Cited By ~ 3

Author(s):

Rovatsos ◽

Altmanová ◽

Augstenová ◽

Mazzoleni ◽

Velenský ◽

...

Keyword(s):

Sex Determination ◽

Sex Chromosomes ◽

Comparative Genomic ◽

Telomeric Sequences ◽

Female Heterogamety ◽

Chromosomal Variability ◽

Determination System ◽

Hybridization In Situ ◽

Sex Determination System

Chameleons are well-known, highly distinctive lizards characterized by unique morphological and physiological traits, but their karyotypes and sex determination system have remained poorly studied. We studied karyotypes in six species of Madagascan chameleons of the genus Furcifer by classical (conventional stain, C-banding) and molecular (comparative genomic hybridization, in situ hybridization with rDNA, microsatellite, and telomeric sequences) cytogenetic approaches. In contrast to most sauropsid lineages, the chameleons of the genus Furcifer show chromosomal variability even among closely related species, with diploid chromosome numbers varying from 2n = 22 to 2n = 28. We identified female heterogamety with cytogenetically distinct Z and W sex chromosomes in all studied species. Notably, multiple neo-sex chromosomes in the form Z1Z1Z2Z2/Z1Z2W were uncovered in four species of the genus (F. bifidus, F. verrucosus, F. willsii, and previously studied F. pardalis). Phylogenetic distribution and morphology of sex chromosomes suggest that multiple sex chromosomes, which are generally very rare among vertebrates with female heterogamety, possibly evolved several times within the genus Furcifer. Although acrodontan lizards (chameleons and dragon lizards) demonstrate otherwise notable variability in sex determination, it seems that female heterogamety with differentiated sex chromosomes remained stable in the chameleons of the genus Furcifer for about 30 million years.

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