Plant sex determination and sex chromosomes

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The Diversity of Sex in Flowering Plants

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Sex Determination in Plants

Most dioecious plant species are believed to derive from hermaphrodite ancestors. The regulatory pathways that have been modified during evolution of the hermaphrodite ancestors and led to the emergence of dioecious species with separate sexes still remain unknown. Sex latifolia is a dioecious plant species harbouring XY sex chromosomes. To identify the molecular mechanisms involved in female organ suppression in male flowers of Determination.

Our phylogenetic analyses suggest that sex identified true orthologs for both types of genes. Determination expression analyses showed a conserved expression pattern for these genes between S.

Both orthologs showed clear differences in their expression pattern between males and females or hermaphrodites suggesting their possible involvement in the sex determination pathway in Plants. Mechanisms underlying sex determination in plants are largely unknown. Silene latifolia is a dioecious species with separate male and female individuals which harbours XY determihation chromosomes and constitutes determination important model for sex determination in plants.

Several attempts determination identify the corresponding genes and the regulatory pathways controlled by these have been unsuccessful. In the dioecious species Silene latifoliaplants whorls of floral organs are observed in both male and female plants meristems, as it is the case for any hermaphrodite species: sepals, plats, stamens male reproductive organs and carpels female reproductive organs.

At determinatipn early stage, the flower meristem is similar in male and female plants undifferentiated. As soon as all floral organ primordia are initiated, the female territory in the centre of the flower meristem is significantly smaller in male compared to female flower buds. Later, a filament sex in male plants, in place of female organs. In female flower buds, stamens are initiated but rapidly degenerate, determination five fused carpels female organs develop in the centre.

Since we observed a vetermination arrest in cell proliferation in the early determinatoon flower meristem, we suspected a precocious arrest of the flower meristem in male individuals. We therefore decided to look for the orthologs in Silene latifoliadetermination two central genes in meristem function in A.

We performed comparative in situ hybridization on young flower buds from male, female and hermaphrodite mutant plants obtained by deleting portion of determinarion Y chromosome 9using Determination and SlCUC as probes. In addition, our results reveal a clear difference se the pattern of determinahion between males and females or hermaphrodites, before any morphological difference become plants.

These observations reflect an early arrest of meristem function in male flowers and could be the cause of the lack of cell divisions observed. Our results kn SlSTM plnts SlCUC strong candidates for being involved in sex determination in Silene sex and therefore open new perspective for molecular mechanism of sex determination platns plants in general.

National Center plants Biotechnology InformationU. Journal Plannts Plant Signal Behav v. Plant Signal Behav. Author information Article notes Copyright and License information Disclaimer.

Corresponding author. Received Dec 19; Accepted Dec Abstract Most dioecious plant species are believed to derive from hermaphrodite ancestors. Key Words: floral meristem, sex determination, shoot-meristemless, cup shaped cotyledon. Sex Determination in Plants Mechanisms underlying sex determination in plants are largely unknown. Candidate Genes Since we observed a whorl-specific arrest in cell proliferation in the early male flower meristem, we suspected a precocious arrest of the flower meristem in male individuals.

References 1. Guttman DS, Charlesworth D. An X-linked gene with a degenerate Y-linked homologue in a dioecious plant. SlY1sex first active gene cloned from a plant Y chromosome, encodes plants WD-repeat protein. EMBO J. Low variability in a Y -linked plant gene and its implications for Y-chromosome evolution. A gradual process of recombination restriction in the evolutionary history dex the sex chromosomes in dioecious plants.

PLoS Biol. Comparison of MADS box gene expression in developing male and sex flowers of the dioecious plant white campion. Plant Cell. Sex organ determination and differentiation in the dioecious plant Melandrium album Silene latifolia : A cytological and histological analysis. Sex Plant Reprod.

Takada S, Tasaka M. Embryonic shoot apical sex formation in higher plants. J Plant Res. Sexual dimorphism in white campion: Complex determinatipn of carpel determination is revealed sex Y chromosome deletions. Support Center Support Center. External link. Please review our privacy policy.


Plants have evolved a diverse array of strategies for sexual reproduction, particularly through the modification of male and female organs at distinct points in development. The immense variation in sexual systems across the land plants provides a unique opportunity to study the genetic, epigenetic, phylogenetic, and ecological underpinnings of sex determination. Here, we reflect on more than a century of research into flowering plant sex determination, placing a particular focus on the foundational genetic and cytogenetic observations, experiments, and hypotheses.

Building on the seminal work on the genetics of plant sex, modern comparative genomic analyses now allow us to address longstanding questions about sex determination and the origins of sex chromosomes. Flowering plants have evolved a remarkable array of sexual systems. Although the Mendelian basis of sex inheritance in dioecious plants has been long studied, there have been several recent exciting breakthroughs in understanding the molecular basis for sex determination in dioecious species e.

As we work to place these recent sex into a coherent framework for understanding plant sex chromosome plants and the implications for sex chromosome research more broadly, it is an opportune time to consider the last century of research into sex differences and sex chromosomes in plants.

In doing so, we find the same ecological and genetic questions that motivate our current research were relevant to botanists more than a century ago: why do so many sex forms exist across the plant phylogeny; why do some dioecious plant species exhibit heteromorphic sex determination while others have indistinguishable sex chromosomes; and what are the sex-determining factors that differentiate males and females at the genic level?

The sex of our understanding of plant sexual diversity began not with genetics, but instead through observations of floral structure paired with natural history. Linnaeus himself artificially organized the kaleidoscopic diversity of floral forms in the Systema Sexuale by grouping species into 24 classes based on the number and arrangement of stamens in the flower Linnaeus Coupled with the diversity of floral forms between different species, immense sexual variation has been found to exist within species and even within individual plants over time.

Wehrli published a comprehensive review including more than 80 species and spanning literature from to that elaborately described observations of sexual transitions and phenomena such as year-to-year shifts in sexual sex, male to hermaphrodite flower conversions, and the formation of male flowers on typically female plants, among many others.

Haring observed similar plasticity in willows Salicaceaedescribing the structural transitions during the complete conversion of males to females, and females to males. Darwin also thought deeply about this overwhelming diversity and instability of floral sex forms in The Different Forms of Flowers on Plants of the Same Speciesand although too plants to discuss in entirety here Barretthe dedicated most of a chapter to discuss the conversion of hermaphroditic flowers to alternative forms.

Darwin proposed that the determination from hermaphroditism to dioecy in plants could occur through an androdioecy mixed males and hermaphrodites or gynodioecy mixed females and hermaphrodites intermediate stage, a model that persisted as the basis for much sex determination research in plants Darwin The turn of the 19th century marked a paradigm shift in the history of classical genetics, and with sex came the foundations for the study of inheritance.

Correns connected the results with his own research on pea and corn hybrids, and in parallel with Hugo de Vries and Erich Tschermak, he proposed models to explain observed segregation ratios Rheinberger Correns cleverly leveraged well-chosen plant species sex address different questions, and in addition to his study determination hybrids in pea and corn, also had established interests in sex variation. Correns employed crosses in dioecious Bryonia dioica Cucurbitaceae to infer that distinct pollen types produce male and female offspring in a Mendelian fashion.

Correns later surmised that a sex-determining factor must be homozygous in one sex and heterozygous in the other, a pivotal inference in the early development of sex determination research. The plasticity of these determination sex forms, paired with the emergence of a chromosomal inheritance theory and a Mendelian understanding of sex determination, motivated active investigation of the cytogenetic divergence between male and female forms in land plants with stable sex phenotypes.

With a growing appreciation of the Mendelian nature of sex inheritance, the morphological diversity of chromosomes separating male and female sexes became obvious through sex analyses. Following quickly on the heels of animal research e. Soon afterwards, Blackburnand Winge independently described L. An obvious question motivated the next stages of research: what genetic factors on a sex-specific chromosome determine sex? Botanists doing cytological research first hypothesized that the difference in chromatin content between males and females with heteromorphic sex chromosomes was a key determinant, but this did not explain sex determination in males and females of many species with cytologically indistinguishable homomorphic chromosomes Winge Researchers returned their attention to the identification of sex determination genes that may reside on either homomorphic or plants sex chromosomes in males and females.

Cytological investigation of hermaphrodite mutants in S. Westergaard, identified S. Identifying the causal sex determination gene or genes on plant sex chromosomes has been an active and often perplexing field of research in the community.

Over the last century, a 2-gene model for the sex of an autosomal pair into a young sex sex pair Westergaard ; Charlesworth and Charlesworth has garnered much attention. In this model, a neo-Y chromosome could evolve if a dominant allele that suppresses femaleness pistil development does not recombine with an allele of a gene that promotes maleness anther development.

While elegant in its simplicity, until recently there has been little direct evidence to support this model. With the emergence of genomic tools, there have been an expanding number of model plant determination for investigating the evolution of plants chromosomes and sex determination genes.

Plants, and particularly flowering plants, are unique in the sense that numerous transitions between sexual systems have occurred across the phylogeny Tree of Sex Consortium We now understand that male and female floral organogenesis in plants is regulated by an assortment of genes, transcription factors, small RNAs, hormones, environmental factors, and epigenetic marks that interact for proper androecium and gynoecium development Chuck et al.

In light of this more precise understanding of the diverse developmental pathways influencing sex function, the particular male and female sterility mutations on a sex chromosome pair that initially drive a hermaphroditic species to dioecy plants be expected to differ across all determination evolved sex chromosomes Ainsworth ; Diggle et al.

As a result, every novel sex chromosome system poses unique challenges when identifying plants candidate sex determination genes. While there is little reason to expect independently derived plant sex chromosomes to harbor the same sex determination genes, there is reason to expect common evolutionary themes in the evolution of sex chromosome structure Ming et al.

A hallmark of a typical plant nuclear sex chromosome is a nonrecombining region flanked by recombining pseudo-autosomal region s PAR. The physical size of the nonrecombining region relative to the PAR is highly variable across sex chromosome systems Otto et al.

Hemizygous sex chromosomes Y or W are hypothesized to grow as a consequence of irreversible transposon, satellite repeat, and organellar DNA accumulation in the nonrecombining region as well as possible translocation of genes contributing to male or female fitness. This prediction does not hold for some plant, bird, snake, and frog lineages though, which have maintained small nonrecombining regions on homomorphic sex chromosome pairs for long periods of time Bergero and Charlesworth ; Otto et al.

As it currently stands, identifying global trends across plant sex chromosomes is difficult given the small sample size of sequenced dioecious plant genomes.

Comparative analysis of independently derived sex chromosome systems is forthcoming but sequencing and assembling repeat-rich, nonrecombining sex determination regions remains challenging. With technological advances including plants sequencing and physical mapping approaches, future comparative work across dioecious lineages will sex whether sex chromosome evolution is driven by changes in one or more points in the developmental pathways of male and female floral organs.

At the same time, comparative analyses within dioecious plant groups will allow plants to elucidate conditions under which the size of nonrecombining regions may be expected to be stable or dynamic. Several plant species and genera have been particularly important to our understanding of the evolution of sex chromosomes and sex determination genes.

The power of plants for studying the evolution of sex determination genes on sex chromosomes comes not from a single species, but rather by holistically studying the repeated evolution and subsequent diversity of sex plants across the flowering plant phylogeny. While by no means an exhaustive or all-inclusive list, the establishment of genomic research into melon Cucumis meloasparagus Asparagus officinalispapaya Carica papayawhite campion S. Here, we give a concise overview of several recent advances in these species, and in particular focus on the diverse set of approaches used to identify putative sex determination candidates that have both refined and expanded our views on the evolution of sex determination mechanisms.

Nearly all species in the Cucurbitaceae family are either monoecious or dioecious, with repeated transitions between the 2 sexual systems that are not associated with a sex chromosome.

Melons are monoecious, producing mostly male flowers on a plant, yet female flowers develop on younger lateral branches.

Earlier work on sex determination in melon implicated ethylene gas as a feminizing agent; in the absence of ethylene gas, female flowers produced stamens, suggesting a role for ethylene in the active suppression of stamen development Byers et al.

A succession of more recent studies Boualem et al. In addition to suppressing carpel development, the CmWIP1 gene promotes stamen development in male flowers, and a naturally occurring transposon-induced knockdown leads to exclusively female flowers on a plant gynoecy Determination et al.

Caucasian persimmon is the first XY sex chromosome pair to have a well-characterized sex determination gene identified in a nonrecombining region of the Y chromosome Akagi et al.

In particular, this study shows the unique power of whole genome sequencing paired with novel comparisons of male and female kmer distributions to identify and assemble male-specific sequences in the absence of a fully sequenced and assembled genome.

Through the male-specific kmer-based assembly of a pseudo-reference nonrecombining region and gene annotation, with additional evidence from male and female RNA-seq differential expression, the OGI and MeGI class I homeodomain transcription factors were identified as a putative sex-determining gene pair. Heterologous transformations of MeGI overexpression constructs into Arabidopsis showed stunted and male-sterile phenotypes resulting from MeGI -driven suppression of anther development, elegantly displaying the power of comparative functional genomics in more tractable species and the relative conservation of the anther development pathway across phylogenetically divergent angiosperms.

Dioecy evolved from hermaphroditism once or potentially twice roughly 2 million years ago in the genus Asparagusconcordant with a range shift from South Africa to North Africa, Europe, and Asia Kuhl et al. Developmentally, both males and females initiate hermaphroditic flowers, but XX females lose their anthers sometime during tapetum development and pollen determination while XY males rarely form flowers with fully developed stylar tubes Caporali et al.

Colchicine treatment of anthers can produce viable YY doubled haploid genotypes, suggesting that little degeneration has occurred sex the Y Ferrie and Caswell, The viability of the YY genotype allows for the production of all-XY male F1 progeny, which typically have a higher yield and lifespan relative to XX females Falloon and Nikoloff The sex determination region has been genetically mapped to a single locus of the A. These genomic regions are largely dominated by recently transposed LTR retroelements and are quite gene-poor, which hampers traditional genome walking Vitte et al.

The ability to culture entirely homozygous XX and YY individuals reduces the complexity of de novo genome assembly, and recently a de novo genome assembly, optical map, and genetic map and annotation for A. Several independently derived male-to-hermaphrodite mutants including Co gamma irradiation and spontaneous mutants implicate a single uncharacterized gene with a Domain of Unknown Function DUF in the roughly 1 Mb hemizygous nonrecombining region as a suppressor of pistil development.

Also inside this male-specific region is a tapetum-related gene, Tapetum Development and Function 1with an Arabidopsis knockout phenotype similar to anther sterility that occurs in asparagus females. The YY genotype is inviable which indicates that a greater degree of Y chromosome degeneration has occurred compared to garden asparagus.

The Y h chromosome is an alternate form of the Y that specifies hermaphroditism, but the Y and Y h chromosomes only differ by 1. Intense genomic research in papaya have yielded a highly contiguous sex chromosome pair assembly combined with a sex of resequenced accessions, genetic markers, expression data, and population-level analyses Ming et al.

Owing to the complexity of floral development and the large number of genes plants the papaya sex determination region, no genes have yet been directly implicated in sex determination in papaya. A candidate gene, Short Vegetative Phase-like has been proposed as a female suppressor, but functional confirmation is still necessary Ueno et al.

White campion S. It is perhaps no surprise that with such a rich ecological determination genetic research history, S. The Y chromosome is cytologically distinct; it has expanded to nearly 1.

The nonrecombining region plants the Y is large, and there is evidence that Y-specific degeneration has occurred at the gene level Guttman and Charlesworth ; Filatov and Charlesworth ; Bergero et al. The identification of sex determination genes in S. There is also debate over whether or not, and to what degree, sex chromosome dosage compensation is occurring in S. Fragaria virginianathe Virginia wild strawberry, is an octoploid subdioecious species with female, male, and hermaphrodite sexes.

The region that suppresses male development is dominant to the female fertility region, meaning that females are the heterogametic ZW sex. Significant QTL for sexually dimorphic traits such as variation in fruit set have been found on the proto-sex chromosome Spigler sex al.

Given that the sex loci are not perfectly linked and can recombine, the strawberry proto-sex chromosome represents a critically important intermediate stage between gynodioecy and full dioecy Moore An array of sequence data has been generated for numerous diploid and octoploid gynodioecious Fragaria species and hybrids in an effort to more finely map sterility loci.

A genome assembly and annotation are available for diploid Fragaria vesca ssp vesca Shulaev et al. None of the contained genes have known function in male sterility, which suggests that genes have previously unknown function or alternative mechanisms may be responsible for sterility. Interestingly, male sterility is not consistently mapped to the same syntenic block across all gynodioecious Fragaria species, suggesting that male sterility has either been repeatedly independently evolved, the same sterility locus been translocated to different regions across species, or the same sterility phenotype is determination the control of different genes Govindarajulu et determination.

The seemingly labile nature of sterility mutations in Fragaria may be related to repeated polyploidization events in the genus, which have been implicated in both the transition to dioecy as well as the reversion back to hermaphroditism Ashman et al.

The dioecious Populus and Salix lineages diverged within the Salicaceae at least 45 million years ago Manchester et al. Populus and Salix sex chromosomes are, however, homomorphic with small nonrecombining regions. Further, whereas perhaps most Populus species have an XY sex determination system Kersten et al. Further, within Populus, the position of the sex determination region has been reported as mapping toward the telomere in some species e. The small size of the nonrecombining regions and variation in the hemizygous sex, together with synteny analyses have led some to hypothesize multiple determination origins for sex chromosomes within Salix and Populus Hou et al.

However, as acknowledged by the authors of these studies, translocation of currently unknown sex determination genes could result in the formation and perhaps turnover of neo-sex chromosomes e.

Genomic rearrangements and the origin of neo-sex chromosomes has also been hypothesized within Silene Howell et al. Just as in persimmon, the absence of an assembled genome does not necessarily inhibit the identification plants putative sex determination genes. By leveraging transcriptome sequencing and SNP calling in a diverse panel of related males and females, Hough et al.

This novel combination of cross-species comparisons, transcriptome-based SNP segregation analysis, expression analysis, and molecular evolutionary comparisons showcases the utility of transcriptome sequencing and assembly paired with thoughtful experimental designs to extract large volumes of sex-linked data from single experiments.

The degeneration of Y chromosomes. Charlesworth, D, Guttman, DS The evolution of dioecy and plant sex chromosome systems. BIOS, Oxford, pp 25— Repeated DNA and heterochromatin structure in Rumex acetosa. Heredity , 70 : — Correns, C Handb Vererbungswissenschaft , 2 : 1— A rapid means of sex identification in Silene latifolia by use of flow cytometry.

Plant Mol Biol Reporter , 9 : — Darwin, CR John Murray: London. SlY1, the first active gene cloned from a plant Y chromosome, encodes a WD-repeat protein. EMBO J , 18 : — Evolution of reproductive systems in the genus Silene.

Proc R Soc B , : — Isolation of Y chromosome-specific sequences from Silene latifolia and mapping of male sex determining genes using representational difference analysis. Sexual dimorphism in white campion: complex deletion on the Y chromosome results in a floral asexual type. DNA diversity in sex linked and autosomal genes of the plant species Silene latifolia and S. Molec Biol Evol , 18 : — Evolution of a plant Y-chromosome: variability in a Y-linked gene of Silene latifolia.

Nature , : — Different kinds of male flowers in the dioecious plant Asparagus officinalis L. Sex Plant Reprod , 6 : 16— Restricted gene flow and subpopulation differentiation in Silene dioica. Heredity , 80 : — Genetics of sex determination in flowering plants.

Devel Genet , 15 : — Guttman, DS, Charlesworth, D An X-linked gene has a degenerate Y-linked homologue in the dioecious plant Silene latifolia. Haigh, J The accumulation of deleterious genes in a population. Theor Pop Biol , 14 : — Comparison of MADS box gene expression in developing male and female flowers of the dioecious plants white campion. Plant Cell , 6 : — Sex determination in Actinidia. Sex-linked markers and progeny sex ratio in diploid A. Sex Plant Repro , 10 : — Heilbuth, JC Lower species richness in dioecious clades.

Kin-structured colonization and small-scale genetic differentiation in Silene dioica. Evolution , 53 : — Four evolutionary strata on the human X chromosome. Science , : — Sexual dimorphism in white campion: complex control of carpel number is revealed by Y chromosome deletions. Lengerova, M, Vyskot, B Sex chromatin and nucleolar analyses in Rumex acetosa L.

Protoplasma , : — Lewis, D The evolution of sex in flowering plants. Biolog Rev , 17 : 46— Lloyd, DG Female-predominant sex ratios in angiosperms. Heredity , 32 : 35— Lloyd, DG a. Breeding systems in Cotula. Dioecious populations. New Phytol , 74 : — Lloyd, DG b. The transmission of genes via pollen and ovules in gynodioecy angiosperms. Theoret Pop Biol , 9 : — Gender allocations in outcrossing cosexual plants. Sinauer: Sunderland, Mass, pp — Modification of the gender of seed plants in varying conditions.

Evol Biol , 17 : — Theoret Appl Genet , 98 : 86— Isolation and developmental expression of male reproductive organ-specific genes in a dioecious campion, Melandrium album Silene latifolia. Plant J , 10 : — McCauley, DE Contrasting the distribution of chloroplast DNA and allozyme polymorphism among local populations of Silene alba : implications for studies of gene flow in plants.

Muller, HJ The relation of recombination to mutational advance. Mut Res , 1 : 2—9. Nei, M Molecular Evolutionary Genetics. Columbia University Press: New York. Nordborg, M A model of genetic modification in gynodioecious plants. Proc Roy Soc Lond B , : — The Y chromosome in the liverwort Marchantia polymorpha has accumulated unique repeat sequences harboring a male-specific gene. Parker, JS Sex-chromosome and sex differentiation in flowering plants.

Chromosomes Today , 10 : — Identification of sex in hop Humulus lupulus using molecular markers. Cytogenetic and molecular analysis of the multiple sex-chromosome system of Rumex acetosa. Heredity , 72 : — Dioecy and its correlates in the flowering plants.

Am J Bot , 82 : — Rice, WR Genetic hitch-hiking and the evolution of reduced genetic activity of the Y sex chromosome. The accumulation of sexually antagonistic genes as a selective agent promoting the evolution of reduced recombination between primitive sex-chromosomes. Evolution , 41 : — The influence of population size and isolation on gene flow by pollen in Silene alba.

Evolution , 53 : 63— The effect of hitchhiking on genes linked to a balanced polymorphism in a subdivided population. Genet Res , 76 : 63— High-stringency subtraction for the identification of differentially regulated cDNA clones.

Biotechniques , 23 : Smith, BW The mechanism of sex determination in Rumex hastatulus. Genetics , 48 : — Mol Biol Evol , 16 : — Taylor, DR Sex segregation ratio and gender expression in the genus Actinidia.

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Sex Plant Repr , 3 : — Y chromosome specific markers and the evolution of dioecy in the genus Silene. Download references. Correspondence to D Charlesworth. Reprints and Permissions. Charlesworth, D. Plant sex determination and sex chromosomes. Heredity 88, 94— doi Download citation. Journal of Experimental Botany The American Naturalist Genome Research BMC Plant Biology Scientific Reports Advanced search.

Skip to main content. Abstract Sex determination systems in plants have evolved many times from hermaphroditic ancestors including monoecious plants with separate male and female flowers on the same individual , and sex chromosome systems have arisen several times in flowering plant evolution.

Access through your institution. Buy or subscribe. Download PDF. Introduction: why are plant sex chromosomes of particular interest? Table 1 Sex and gender systems of sexually reproducing flowering plants Full size table.

Figure 1. Full size image. The genetics of sex determination in plants, and plant sex chromosomes Sex inheritance and sex chromosomes in plants are strikingly similar to those in animals. Figure 2. Why are sex determining loci linked? Figure 3. Evolution of sex chromosomes The theory outlined here explains the evolution of a rarely recombining chromosome region containing the sex determining genes, an incipient sex chromosome system. Have plant Y chromosomes degenerated? Molecular genetics of plant Y chromosomes Our understanding of the evolution of plant sex chromosomes and sex determination should be advanced by the use of molecular markers, so several groups are searching for these.

Discussion With the availability of molecular techniques, we may now hope to understand more about how sex chromosomes evolve. Google Scholar Caballero, A Google Scholar Charlesworth, D Google Scholar Charlesworth, B Google Scholar Darwin, CR There is also debate over whether or not, and to what degree, sex chromosome dosage compensation is occurring in S.

Fragaria virginiana , the Virginia wild strawberry, is an octoploid subdioecious species with female, male, and hermaphrodite sexes. The region that suppresses male development is dominant to the female fertility region, meaning that females are the heterogametic ZW sex. Significant QTL for sexually dimorphic traits such as variation in fruit set have been found on the proto-sex chromosome Spigler et al. Given that the sex loci are not perfectly linked and can recombine, the strawberry proto-sex chromosome represents a critically important intermediate stage between gynodioecy and full dioecy Moore An array of sequence data has been generated for numerous diploid and octoploid gynodioecious Fragaria species and hybrids in an effort to more finely map sterility loci.

A genome assembly and annotation are available for diploid Fragaria vesca ssp vesca Shulaev et al. None of the contained genes have known function in male sterility, which suggests that genes have previously unknown function or alternative mechanisms may be responsible for sterility. Interestingly, male sterility is not consistently mapped to the same syntenic block across all gynodioecious Fragaria species, suggesting that male sterility has either been repeatedly independently evolved, the same sterility locus been translocated to different regions across species, or the same sterility phenotype is under the control of different genes Govindarajulu et al.

The seemingly labile nature of sterility mutations in Fragaria may be related to repeated polyploidization events in the genus, which have been implicated in both the transition to dioecy as well as the reversion back to hermaphroditism Ashman et al.

The dioecious Populus and Salix lineages diverged within the Salicaceae at least 45 million years ago Manchester et al.

Populus and Salix sex chromosomes are, however, homomorphic with small nonrecombining regions. Further, whereas perhaps most Populus species have an XY sex determination system Kersten et al. Further, within Populus, the position of the sex determination region has been reported as mapping toward the telomere in some species e.

The small size of the nonrecombining regions and variation in the hemizygous sex, together with synteny analyses have led some to hypothesize multiple independent origins for sex chromosomes within Salix and Populus Hou et al.

However, as acknowledged by the authors of these studies, translocation of currently unknown sex determination genes could result in the formation and perhaps turnover of neo-sex chromosomes e. Genomic rearrangements and the origin of neo-sex chromosomes has also been hypothesized within Silene Howell et al.

Just as in persimmon, the absence of an assembled genome does not necessarily inhibit the identification of putative sex determination genes. By leveraging transcriptome sequencing and SNP calling in a diverse panel of related males and females, Hough et al.

This novel combination of cross-species comparisons, transcriptome-based SNP segregation analysis, expression analysis, and molecular evolutionary comparisons showcases the utility of transcriptome sequencing and assembly paired with thoughtful experimental designs to extract large volumes of sex-linked data from single experiments. A major impediment to the identification of sex determination genes is the ability to accurately assemble the full genomic sequence of a sex chromosome pair.

Highly homomorphic sex chromosomes may not be divergent enough to separately assemble using shotgun genomic reads, while more heteromorphic and divergent sex chromosomes often suffer from an increased accumulation of repetitive elements which cannot currently be assembled without high coverage and longer read data. Flow sorting and laser microdissection have been used to specifically isolate heteromorphic sex chromosomes Veuskens et al.

With more modern de novo long read sequencing and assembly strategies e. Despite considerable advances in genome sequencing and assembly methods, the assembly of sex chromosomes will continue to be difficult. A consequence of suppressed or nonrecombination in sex chromosomes is that repetitive DNA can rapidly proliferate. This has 2 important consequences; first, the proliferation of repetitive DNA can interfere with gene function, leading to the degeneration of a sex chromosome, and second, by making them intractable regions for highly contiguous genome assembly and annotation due to the high degree of similar or near-identical repetitive DNA.

RNA-Seq can instead be utilized as a powerful and cost-effective approach to identifying sex-specific transcripts. Reconstructing a floral transcriptome de novo is much less demanding than assembling a complex plant genome, which is often rife with the remnants of polyploidization events and repetitive element proliferations Kejnovsky et al.

After isolating biologically replicated RNA from floral tissues during the arrest of male and female development, short read sequencing e.

In addition to SNP marker development, transcript expression levels can be quantified and differentially expressed transcripts between sexes can be identified e. Transcripts that are both sex-linked and differentially expressed between sexes are likely promising candidate sex determination loci. Other high-throughput methods for sex-linked marker identification include genotype-by-sequence GBS e.

Comparisons of male and female whole genome shotgun read coverage can also be used to quickly infer sex linkage Vicoso and Bachtrog Once sex-linked genes have been identified, a large challenge remains in characterizing their functions and putative roles in floral development, with the ultimate goal of identifying the master regulator s of sterility.

Fortunately, many floral gene regulatory networks appear to be conserved in androecium and gynoecium development across the angiosperms Whipple et al. Arabidopsis thaliana is an invaluable study species for heterologous investigation of candidate sex determination genes as typified by the persimmon sex determination story.

Loss-of-function mutations e. If orthologs can be identified in A. A major caveat to heterologous analyses is that while even distant orthologs are proposed to retain function Nehrt et al. A more direct approach to functional characterization of sex-determining gene candidates is through gene expression analyses in the species of interest. Functional analysis involving gene expression knockdowns of candidate sex determination genes is feasible in species without transformation protocols.

Virus-induced gene silencing VIGS is one powerful option, where a target gene is expressed inside a viral vector that is known to infect the host plant. Other options include forward screens such as chemically mutagenizing large seed populations with ethyl methanesulfonate EMS to induce point mutations, or using gamma radiation to induce large chromosomal deletions and specifically look for mutations in candidate sex determination genes reviewed in Sikora et al.

The concept of a model system is rapidly changing, though, and CRISPR-Cas9 gene editing and knockdown strategies are readily available for plant species which are able to be transformed Doudna and Charpentier The last years of sex determination research in flowering plants have culminated in a new era of truly accessible genomics.

As we unravel the mechanisms of sex determination across diverse sets of sex chromosomes, we must also reflect on how recent discoveries should continue to shape our models describing the evolution of young sex chromosomes.

Ultimately, the identification of sex determination genes is difficult in every sex chromosome system due to the challenges of sequencing nonrecombining, repeat-rich sex determination regions and the developmental complexity of floral organs.

Given the independent, repeated evolution of dioecy and sex chromosomes across the land plants, the genes involved in sex determination are likely not the same across distantly related dioecious species. As the cost of sequencing continues to decrease while the quality and length of reads increases, we should expect to see more high quality plant sex chromosome assemblies in additional species spread across all flowering plants.

Cheaper sequencing also opens the door to focused and increased sampling of genomes within a genus that displays sexual system variation, particularly if used for comparative analyses of sex chromosomes to ancestral autosome reconstructions.

Identifying nucleotide variation or genic mutations between closely related autosomes and evolutionarily young sex chromosomes can provide circumstantial evidence for candidate sex determination genes. In conjunction with more rapid genome editing techniques, these types of focused comparative analyses could lead to faster identification of sex determination genes in additional species. A more pressing gap in plant sex chromosome knowledge is understanding how and why young Y or W chromosomes age over time.

Since genes with male-biased gene expression have been recruited to Y chromosomes over time in humans Skaletsky et al. Sequencing and assembling several phylogenetically dispersed sex chromosomes derived from the same ancestral autosome is necessary to explore the stability of nonrecombining regions and sex determination genes as Y and W sex chromosomes age. Genome assembly is just a first step, though, and sex biologists need to embrace integrated application of bioinformatic, functional i.

We thank Katie Peichel, Susanne Renner, and an anonymous reviewer for their critical comments. We also thank the American Genetic Association for conference travel funding that inspired this review. Oxford University Press is a department of the University of Oxford. It furthers the University's objective of excellence in research, scholarship, and education by publishing worldwide. Sign In or Create an Account.

Sign In. Advanced Search. Article Navigation. Close mobile search navigation Article Navigation. Volume Article Contents. The Diversity of Sex in Flowering Plants. Melon Cucumis melo. Persimmon Diospyros lotus.

Garden Asparagus Asparagus officinalis. Papaya Carica papaya. White Campion S. Strawberry Fragaria spp. Sorrel Rumex. Oxford Academic. Google Scholar. Jim Leebens-Mack. Address correspondence to A. Harkess at the address above, or e-mail: aharkess uga. Corresponding Editor: Catherine Peichel. Cite Citation.

Permissions Icon Permissions. Abstract Plants have evolved a diverse array of strategies for sexual reproduction, particularly through the modification of male and female organs at distinct points in development. Environmental regulation of sex determination in oil palm: current knowledge and insights from other species. Search ADS. Boys and girls come out to play: the molecular biology of dioecious plants. Revisiting the dioecy-polyploidy association: alternate pathways and research opportunities.

Genomic degradation of a young Y chromosome in Drosophila miranda. Preservation of the Y transcriptome in a million-year-old plant sex chromosome system. A large pseudoautosomal region on the sex chromosomes of the frog Silurana tropicalis. The cytological aspects of the determination of sex in the dioecious forms of Lychnis. A conserved mutation in an ethylene biosynthesis enzyme leads to andromonoecy in melons.

The andromonoecious sex determination gene predates the separation of Cucumis and Citrullus Genera. A cucurbit androecy gene reveals how unisexual flowers develop and dioecy emerges. Ethylene: a natural regulator of sex expression of Cucumis melo L. Development of male and female flower in Asparagus officinalis. Search for point of transition from hermaphroditic to unisexual developmental pathway. Identification of five new genes on the Y chromosome of Drosophila melanogaster.

Structure and evolution of Apetala3, a sex-linked gene in Silene latifolia. The ortholog conjecture is untestable by the current gene ontology but is supported by RNA sequencing data.

Molecular evolution constraints in the floral organ specification gene regulatory network module across 18 angiosperm genomes. Google Preview. Multiple developmental processes underlie sex differentiation in angiosperms. Isolation of Y chromosome-specific sequences from Silene latifolia and mapping of male sex determining genes using representational difference analysis.

Asparagus : value of individual plant yield and fern characteristics as selection criteria. Isolated microspore culture techniques and recent progress for haploid and doubled haploid plant production. Substitution rates in the X- and Y-linked genes of the plants, Silene latifolia and S.

Identification of two markers linked to the sex locus in dioecious Asparagus officinalis plants. Signaling and transcriptional control of reproductive development in Arabidopsis. Recent Y chromosome divergence despite ancient origin of dioecy in poplars Populus. An X-linked gene with a degenerate Y-linked homologue in a dioecious plant.

Abnorme Katzchenbildung bei Salix caprea L. Oester Bot Zeit. Sex-biased gene expression in dioecious garden asparagus Asparagus officinalis. Different autosomes evolved into sex chromosomes in the sister genera of Salix and Populus. Genetic degeneration of old and young Y chromosomes in the flowering plant Rumex hastatulus.

The role of repetitive DNA in structure and evolution of sex chromosomes in plants. The sex-linked region in Populus tremuloides Turesson corresponds to a pericentromeric region of about two million base pairs on P. Microsatellite accumulation on the Y chromosome in Silene latifolia. Molecular phylogeny of the genus Asparagus Asparagaceae explains interspecific crossability between the garden asparagus A.

Systema naturae per regna tria naturae:secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis in Latin 10th ed. Evolutionary diversity and turn-over of sex determination in teleost fishes.

A transposon-induced epigenetic change leads to sex determination in melon. Semi-automatic laser beam micro dissection of the Y chromosome and analysis of Y chromosome DNA in a dioecious plant, Silene latifolia. The draft genome of the transgenic tropical fruit tree papaya Carica papaya Linnaeus.

A sex-determination system is a biological system that determines sex development of sexual characteristics in an organism. Most organisms that create their offspring using sexual reproduction have two sexes. Occasionally, there are hermaphrodites in place of one or both sexes. There are also some sex that are only one sex due to parthenogenesisthe act of a female reproducing without fertilization.

In many species, sex determination is genetic: males and females have different alleles or even different genes that specify their sexual morphology. The sexual differentiation is generally triggered by a main gene a "sex locus"with a multitude sex other genes following in a domino effect. In other cases, sex of a fetus is determined by environmental variables such as temperature.

The details of some sex-determination systems are not yet fully understood. Hopes for future fetal biological system analysis include complete-reproduction-system initialized signals that can be measured during pregnancies to more accurately determine whether a determined sex of a fetus is male, or female.

Such analysis of biological systems could also signal whether the fetus is hermaphrodite, which includes total or partial of both male and female reproduction organs.

Some species sex as various plants and fish do not have a fixed sex, and instead go through life cycles and change sex based on genetic cues during corresponding life stages of their type. This could be due to environmental factors such as seasons and temperature. Human fetus genitals can sometimes develop abnormalities sex maternal determination due to mutations in the fetuses sex-determinism system, resulting in the fetus becoming intersex.

Sex determination was discovered in the mealworm by the American geneticist Nettie Stevens in In this system, most females have two of the same kind of sex chromosome XXwhile most males have two distinct sex chromosomes XY. The X and Y sex chromosomes are different in shape and size from each other, unlike the rest of the chromosomes autosomesand are sometimes called allosomes. In some species, such as humans, organisms remain sex indifferent for a time after they're created; in others, however, such as fruit flies, sexual differentiation occurs as soon as the egg is fertilized.

Some species including humans have a gene SRY on the Y chromosome that determines maleness. In Y-centered sex determination, the SRY gene is the main gene in determining male characteristics, but multiple genes are required to develop testes. In XY mice, lack of the plants DAX1 on the X chromosome results in sterility, but in humans it causes adrenal hypoplasia congenita. Some species, such as fruit fliesuse the presence plants two X chromosomes to determine femaleness.

Some fish have variants of the XY sex-determination systemas well plants the regular system. For example, while having an XY format, Xiphophorus nezahualcoyotl and X. At least one monotremethe platypuspresents a particular sex determination scheme that in some ways resembles that of the ZW sex chromosomes of birds and lacks the SRY gene. Although it plants an XY system, the platypus' sex chromosomes share no homologues with eutherian sex chromosomes. However, homologues to the avian DMRT1 gene on platypus sex chromosomes X3 and X5 suggest that it is possible the sex-determining gene for the platypus is the same one that is involved in bird sex-determination.

More research must be conducted in order to determine the exact sex determining gene of the platypus. In this variant of the XY system, females have two copies of the sex chromosome XX but males have only one X0.

The 0 denotes the absence of a second sex chromosome. Generally in this method, the sex is determined by amount of genes expressed across the two chromosomes.

This system is observed in a number of insects, including the grasshoppers and crickets of order Orthoptera and in cockroaches order Blattodea. A small determination of mammals also lack a Y chromosome. These include the Amami spiny determination Tokudaia osimensis and the Tokunoshima spiny rat Tokudaia tokunoshimensis and Sorex araneusa shrew species.

Transcaucasian mole voles Ellobius lutescens also have a form of XO determination, in which both sexes lack a second sex chromosome. The nematode C. These genes reduce male gene activation and increase it, respectively. The ZW sex-determination system is found determination birds, some reptiles, and some insects sex other organisms. The ZW sex-determination system is reversed compared to the XY system: females have two different kinds of chromosomes ZWand males have two of the same kind of chromosomes ZZ.

In the chicken, this was found to be dependent on the expression of DMRT1. In the case of the chicken, their Z chromosome is more similar to humans' autosome 9. This is due to the fact that the haploid eggs double their chromosomes, resulting in ZZ or WW.

The ZZ become males, but the WW are not viable and are not brought to term. In some Bryophyte and some algae species, the gametophyte stage of the life cycle, rather than being hermaphrodite, occurs as separate male or female individuals that produce male and female gametes respectively. When meiosis occurs in the sporophyte generation of the life cycle, the sex chromosomes known sex U and V assort in spores that carry either the U chromosome and give rise to female gametophytes, or the V chromosome and give rise to male gametophytes.

Haplodiploidy is found in insects belonging to Hymenopterasuch as ants and bees. Unfertilized eggs develop into haploid individuals, which plants the males. Diploid individuals are generally female but may be sterile males. Males cannot have sons or fathers. This may be significant for the development of eusocialityas it increases the significance of kin selectionbut it is debated. This allows them to create more workers, sex on the determination of the colony.

Many other sex-determination systems exist. In some species of reptiles, including alligatorssome turtlesand the tuatarasex is determined by the temperature at which the egg is incubated during a temperature-sensitive period. There are no examples of temperature-dependent sex determination TSD in birds.

Megapodes had formerly been thought to exhibit this phenomenon, but were found to actually have different temperature-dependent embryo mortality rates for each sex. The specific temperatures required to produce each sex are known as the female-promoting temperature and the male-promoting temperature.

It is unknown how exactly temperature-dependent sex determination evolved. For example, a warmer area could be more suitable for nesting, so more females are produced to increase the amount that nest next season. There are other environmental sex plants systems including location-dependent determination systems as seen in the marine worm Bonellia viridis — larvae become males if they make physical contact with a female, and females if they end up on the bare sea floor.

This is triggered by the presence of a chemical produced by the females, bonellin. In tropical clown fishthe dominant individual in a group becomes female while the other ones are male, and bluehead wrasses Thalassoma bifasciatum are the reverse.

Some species, however, have no sex-determination system. Hermaphrodite species include the common earthworm and certain species of snails. A few species of fish, reptiles, and insects reproduce by parthenogenesis and are female altogether.

There are some reptiles, such as the boa constrictor and Komodo dragon that can reproduce both sexually and asexually, depending on whether a mate is available. Other unusual systems include those of the swordtail fish [ clarification needed determination ; [11] the Chironomus midges [ clarification needed ] determination citation needed ] ; the platypuswhich has 10 sex chromosomes [12] but lacks the mammalian sex-determining gene SRY, meaning that the process of sex determination in the platypus remains unknown; [13] the juvenile hermaphroditism of zebrafishwith an unknown trigger; [11] and the platyfishwhich has W, X, and Y chromosomes.

The accepted hypothesis of XY and ZW sex chromosome evolution is that they evolved at the same time, in two different branches. All sex plants started out as an original autosome of an original amniote that relied upon temperature to determine the sex of offspring. After the mammals separated, the branch further split into Lepidosauria and Archosauromorpha. These two groups both evolved the ZW system separately, as evidenced by the existence of different sex chromosomal locations.

The regions of the X and Y chromosomes that are still homologous to one another are known as the pseudoautosomal region. There are some species, such as the medaka fish, that evolved sex plants separately; their Y chromosome never inverted and can still swap genes with the X. These species' sex chromosomes are relatively primitive and unspecialized. From Wikipedia, the free encyclopedia. A biological system that determination the development of sexual characteristics in an organism.

Main article: XY sex-determination system. Main article: X0 sex-determination system. Main article: ZW sex-determination system. Main article: Haplodiploidy. Main article: Temperature-dependent sex determination.

Further information: Environmental sex determination. Retrieved 7 June Proceedings of the American Philosophical Society.

Nature Education. Retrieved 8 December Cellular and Molecular Life Sciences. Current Science. New England Journal of Medicine. American Journal of Medical Genetics. Microbiology and Molecular Biology. Mechanisms of Development. Bibcode : Natur. Ashley; D. Graves Chromosome Res. Kuwabara; Peter G. Okkema; Judith Kimble April Molecular Biology of the Cell.

September Genome Res.

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In plants that produce no flowers and are homosporous, sex determination is manifest in the gametophyte generation with the production of. Sex determination systems in plants have evolved many times from hermaphroditic ancestors (including monoecious plants with separate male.

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