Chromosomes and Sex Differentiation

Chapter

Abstract

Plant species can be classified into two major groups: those that permit self-pollination (autogamy) and those that inhibit self-pollination. In mostly self-pollinating species, harmful recessive mutations with a large effect are efficiently eliminated by selection, while slightly deleterious mutations accumulate as a consequence of the reduced effective population size and effective recombination rates (Wright et al. 2008). In contrast, plants that prevent autogamy are able to mask and retain in their genomes harmful recessive mutations with large effects in spite of more efficient selection against slightly deleterious mutations in this group. In cosexual plants, various mechanisms, such as dichogamy, heterostyly or self-incompatibility, prevent self-pollination. Another mechanism is the evolution of unisexual flowers. Populations can be distinguished according to the localization of unisexual flowers: monoecious (male and female on the same plant), gynomonoecious (hermaphrodite and female flowers on the same plant), andromonoecious (male and hermaphrodite flowers on the same plant), dioecious (male and female flowers on different plants), gynodioecious (female and cosexual individuals), androdioecious (male and cosexual individuals), or trioecious (male, female, and cosexual individuals), as reviewed by Dellaporta and Calderon-Urrea (1993). Gymnosperms are mostly monoecious, but also comprise a relatively high percentage of dioecious species. There are c. 1,010 species of gymnosperms, of which 36 %, namely all 300 species of cycads, Ginkgo biloba, and approximately 80 Gnetales are dioecious (Ming et al. 2011). In contrast, dioecy has been reported in only about 6 % of angiosperm species (Renner and Ricklefs 1995). Interestingly, dioecy is more widespread in tropical species, and an exceptionally high percentage of the dominant woody species of tropical forests are dioecious (Matallana et al. 2005). New cases of dioecy continue to be found because of the phenomenon of cryptic dioecy (Mayer and Charlesworth 1991).

11.1 Evolution of Plant Sexuality

Plant species can be classified into two major groups: those that permit self-pollination (autogamy) and those that inhibit self-pollination. In mostly self-pollinating species, harmful recessive mutations with a large effect are efficiently eliminated by selection, while slightly deleterious mutations accumulate as a consequence of the reduced effective population size and effective recombination rates (Wright et al. 2008). In contrast, plants that prevent autogamy are able to mask and retain in their genomes harmful recessive mutations with large effects in spite of more efficient selection against slightly deleterious mutations in this group. In cosexual plants, various mechanisms, such as dichogamy, heterostyly or self-incompatibility, prevent self-pollination. Another mechanism is the evolution of unisexual flowers. Populations can be distinguished according to the localization of unisexual flowers: monoecious (male and female on the same plant), gynomonoecious (hermaphrodite and female flowers on the same plant), andromonoecious (male and hermaphrodite flowers on the same plant), dioecious (male and female flowers on different plants), gynodioecious (female and cosexual individuals), androdioecious (male and cosexual individuals), or trioecious (male, female, and cosexual individuals), as reviewed by Dellaporta and Calderon-Urrea (1993). Gymnosperms are mostly monoecious, but also comprise a relatively high percentage of dioecious species. In the gymnosperms, approximately 36 %, namely all c. 250 species of cycads, Ginkgo biloba, and c. 50 Gnetales are dioecious (Ming et al. 2011). In contrast, dioecy has been reported in only about 6 % of angiosperm species (Renner and Ricklefs 1995). Interestingly, dioecy is more widespread in tropical species, and an exceptionally high percentage of the dominant woody species of tropical forests are dioecious (Matallana et al. 2005). New cases of dioecy continue to be found because of the phenomenon of cryptic dioecy (Mayer and Charlesworth 1991).

The taxonomic spread of dioecy indicates that it probably originated many times independently. There are several hypotheses that describe the possible evolutionary history of dioecy. The most popular one is that two basic genetic changes had to occur on the way from cosexuality to dioecy (Charlesworth and Charlesworth 1978). One such change caused male sterility and the other was responsible for female sterility. Gynodioecy was likely the intermediate stage towards complete dioecy, since it occurs much more frequently than androdioecy. According to theoretical studies, the evolution of dioecy through androdioecy is also hindered by males in androdioecious populations having to produce at least twice the pollen of hermaphrodites to be maintained in the population (Charlesworth and Charlesworth 1978). Other possible routes to dioecy include direct evolution of dioecy from monoecy, e.g., species of the genus Siparuna (Renner and Won 2001), or evolution of dioecy as a reaction to the loss of autoincompatibility in polyploids (Miller and Venable 2000). The possibility of the evolution of dioecy through heterodichogamy is also theoretically supported (Pannell and Verdú 2006), but there is still no clear example of this route (Renner et al. 2007).

In most dioecious species the male is the heterogametic sex (XY), while females are homogametic (XX). However, there are some exceptions, in which female individuals are heterogametic (ZW), e.g., wild Fragaria (Spigler et al. 2008) and Populus trichocarpa (Tuskan et al. 2006). In some species, sex is determined by a simple Mendelian genetic system based on the segregation of a few loci such as in Fragaria virginiana (Spigler et al. 2008), Ecballium elaterium (reviewed in Mather 1949; Gómez-Campo and Casas-Builla 1965), Mercurialis annua (Hamdi et al. 1987). In others, such as Carica papaya, a short X-Y non-recombining region has recently formed (Yu et al. 2007). These systems are considered to be evolutionary very young. Other dioecious species are evolutionary older, and some of them have evolved heteromorphic sex chromosomes. Heteromorphic sex chromosomes occur in Silene (reviewed by Nicolas et al. 2005) and sorrel (Rumex spp.; reviewed by Ainsworth et al. 1999), some hop species (Humulus spp.; reviewed in Shephard et al. 2000), hemp (Cannabis sativa; reviewed by Menzel (1964) and Sakamoto et al. (2000)), and some Cucurbitaceae species (Kumar and Viseveshwaraiah 1952).

11.2 Sex Chromosomes and Sex Determination Systems in Plants

11.2.1 Sex Determination and Sex Chromosomes in Bryophytes

Monoecious Bryophytes: Intragametophytic Selfing

Self-fertilization has a different adaptive significance and effects in species with combined sexes than in those with separate sexes. In haploid-dominant species such as liverworts, mosses, and hornworts, self-fertilization in the broad sense (intergametophytic selfing—mating of gametophytes derived from the same spore) is possible in species with combined or separate sexes (monoecious and dioecious, respectively). Monoecious species also possess an additional mode of selfing (intragametophytic selfing) that leads to complete homozygosity in one step. Eppley et al. (2007) found that while there were deficiencies of heterozygotes compared to the null expectation in both monoecious and dioecious mosses, monoecious species had significantly higher levels of heterozygote deficiency than dioecious species. Estimates of selfing rates have suggested that selfing occurs frequently in monoecious populations, but only rarely in dioecious populations. However, significant indications of mixed mating or biparental inbreeding were found in many populations of two dioecious species (Polytrichadelphus magellanicus and Breutelia pendula) (Eppley et al. 2007).

Dioecious Mosses and Liverworts (Marchantia polymorpha Main Model)

The sex chromosomes in liverworts and mosses play a direct role in development of gametophyte sex organs. Marchantia polymorpha is a model species that has allowed researchers to better understand sex determination in bryophytes and to reveal similarities in the evolution of sex chromosomes between evolutionary distant species. The dominant phase of the Marchantia polymorpha life cycle is the haploid gametophyte, which is either male or female. The male possesses a Y chromosome, while the female possesses an X. Asexual propagules (gemmae) are produced by the thallus, so sex-specific cultures can be easily maintained. This experimental system allows researchers to monitor the functions of sex-linked genes without interference from the other sex chromosome.

The X and Y chromosomes are heteromorphic; they differ in size, which has made them good candidates for FISH mapping, permitting direct identification of X- and Y-located sequences. Okada et al. (2000) constructed genomic libraries of male and female plants, and isolated seventy putative male-specific PAC clones based on different intensities of their hybridization with male and female DNAs. Y-specificity of one clone (pMM4G7) was confirmed by Southern blots, PCR analysis and FISH (Okada et al. 2000). Another six male-specific clones were isolated using representational difference analysis (Fujisawa et al. 2001). A detailed analysis of some of the Y-specific clones (pMM4G7 and pMM23-130 F12) revealed many repetitive motifs organised in long stretches. Within these specific repeats, a novel gene family (ORF162) was described, which is specifically expressed in male sexual organs and contains a RING motif (Okada et al. 2001). RING finger proteins are known to participate in transcriptional repression and in the ubiquitin-mediated protein turnover processes (Borden 2000). Another five genes amplified on the Y chromosome were described by Ishizaki et al. (2002). One of the five putative genes shows similarity to a male gamete-specific protein of lily (Lilium longiflorum) and is expressed predominantly in male sex organs, suggesting that this gene has a male reproductive function.

In light of this evidence, Ishizaki et al. (2002) have suggested that the Y chromosome evolved by co-amplification of protein-coding genes with unique repeat sequences. Y chromosomes are different from other chromosomes because they do not undergo recombination. Yamato et al. (2007) reported the gene organization of the Y chromosome in M. polymorpha. On the 10 Mb Y chromosome, 64 genes were identified, 14 of which were detected only in the male genome. These genes are expressed in reproductive organs but not in the vegetative thalli, suggesting their participation in male reproductive functions. Another 40 genes on the Y chromosome are expressed in the thalli and the male sexual organs. At least six of these genes have diverged from their X-linked counterparts that are expressed in the thalli and sexual organs in female plants, suggesting that these X- and Y-linked genes have essential cellular functions. These findings indicate that the Y and X chromosomes share the same ancestral autosome and support the prediction that in a haploid organism essential genes on the sex chromosomes are more likely to persist than in a diploid organism (Yamato et al. 2007; see also Rensing et al. 2013, this volume).

11.2.2 Sex Determination in Ferns

Homosporous Ferns (Main Model Ceratopteris richardii)

Environmental sex determination (ESD) is the rule in homosporous ferns (Korpelainen 1998). Sporophytes (the diploid generation) produce free-living gametophytes (the haploid generation) that are potentially bisexual, i.e., they can bear female (archegonia) and male (antheridia) reproductive organs (gametangia) on the same individual. Several environmental factors influence sexual expression. One class of factors, maleness-inducing pheromones, or ‘antheridiogens’ (Schneller et al. 1990), has received much attention. Antheridiogens are gibberellin-like compounds secreted by large, female or bisexual gametophytes that reduce growth and induce maleness in nearby asexual gametophytes.

Other environmental factors that affect sex in ferns, such as nutrients, have received very little attention in most reviews of sex expression in fern gametophytes (Cousens et al. 1988; Korpelainen 1998; see however Raghavan 1989). Three well known patterns described in gametophyte biology illustrate the plasticity of sex expression in homosporous ferns. Firstly, ontogenetic changes in gametophyte sex undergo sequential hermaphroditism, i.e., the unidirectional change in sex during ontogeny. Klekowski (1969) distinguished four types of sequential hermaphroditism: male to bisexual, male to female to bisexual, female to bisexual, and step-wise change from male through bisexual to female. Secondly, the coexistence of gametophytes of different sexes within a population has been repeatedly reported (Klekowski 1969; Hamilton and Lloyd 1991). Thirdly, harsh growing conditions, such as poor substrate or high density, are known to lead to small and male gametophytes (Miller 1968; Rubin and Paolillo 1983; Rubin et al. 1985; Korpelainen 1995; Huang et al. 2004).

Ceratopteris richardii has been the main fern model for sex determination studies because of its rapid life cycle and easy cultivation (Hickok et al. 1987). Haploid gametophytes of the fern Ceratopteris are either male or hermaphroditic. The determinant of sex type is the pheromone antheridiogen, which is secreted by the hermaphrodite and directs male development of young, sexually undetermined gametophytes. Three phenotypic classes of mutations that affect sex-determination have been isolated and include the hermaphroditic (her), the transformer (tra) and feminization (fem) mutations. Eberle and Banks (1996) performed linkage analysis and tests of epistasis among the different mutants to assess the possible interactions among these putative genes. Their results indicate that sex determination in Ceratopteris involves at least seven interacting genes, which may interact with antheridiogen, the primary sex-determining signal.

Two models describing how antheridiogen may influence the activity states of these genes and the sex of the gametophyte have been suggested (Talmor-Neiman et al. 2006). To understand how antheridiogen represses the development of female traits at the genetic level, 16 new mutations that feminize the gametophyte in the presence of antheridiogen were characterized (Strain et al. 2001). Seven are tightly linked to the FEM1 locus, which was previously described by Eberle and Banks (1996). Nine other mutations concern another locus NOTCHLESS1 (NOT1), with mutant plants lacking a meristem notch. Some not1 mutations also affect sporophyte development when homozygous, indicating that the not1 mutations are recessive and that NOT1 is required for normal sporophyte development. The epistatic interactions among FEM1, NOT1, and other sex-determining genes have been revealed (Strain et al. 2001). According to the current model of sex determination in Ceratopteris, the presence of antheridiogen leads to the activation of the FEM1 gene, which not only promotes the differentiation of male traits, but also represses female development by activating the NOT1 gene. NOT1 represses the TRA genes necessary for the development of female traits in the gametophyte (Strain et al. 2001).

Kamachi et al. (2007) examined the effect of photomorphogenically active light on antheridiogen-induced male development of gametophytes of Ceratopteris richardii. These workers also revealed the latent antheridiogen-signal transduction pathway. Although blue light did not affect sensitivity to antheridiogen in wild-type gametophytes, it was found that the gametophytes of the her1 mutant, which are insensitive to antheridiogen, developed into males when grown under blue light in the presence of antheridiogen. The latent antheridiogen-signal transduction pathway is therefore probably activated by blue light. Red light, on the other hand, suppressed male development, and the action of red light seems to dominate that of blue light. The results of experiments with a photomorphogenic mutant also suggest that phytochrome may be involved in the action of red light (Kamachi et al. 2007). Interestingly, while certain KNOX genes function similarly in the development of both seed plant and fern sporophyte meristems despite their differences in structure, KNOX gene expression is not required for the development of the fern gametophyte. It is therefore supposed that the sporophyte and gametophyte meristems of ferns are not regulated by the same developmental mechanisms at the molecular level (Sano et al. 2005). A systemic gene-silencing method suitable for high throughput, reverse genetic analyses of gene function in fern gametophytes has already been developed (Rutherford et al. 2004). This also opens new possibilities for research into sex determination in ferns.

The Heterosporous Ferns and Lycophytes

In contrast to homosporous ferns, heterosporous ferns (e.g., Marsilea, Azolla) and some lycophytes (e.g., Selaginella and Isoetes) form two different types of spores: microspores, which produce male gametophytes, and megaspores which produce female gametophytes. These spores are formed in special structures (microsporangia and megasporangia). In contrast to dioecious bryophytes where the gametophyte type is determined by its genome, the gametophyte type in heterosporous ferns and lycopods is controlled by the type of spore from which it emerged (reviewed in Tanurdzic and Banks 2004). A model for the evolution of heterospory from homospory has been suggested by Haig and Westoby (1988). This model has three phases: (1) a gradual increase in spore size in a homosporous population, (2) the sudden introduction of smaller microspores from sporophytes reproducing predominantly as males, (3) the subsequent divergence in size and specialization of the two spore types. The model proposes that haploid dioecy evolved from pre-existing mechanisms of sex determination, and that endosporic development of megagametophytes arose as a consequence of an increased dependence on spore food reserves for reproduction (Haig and Westoby 1988).

Among the lycophytes, Selaginella has perhaps the greatest potential as a useful comparative system for the study of sex determination and the mechanisms leading to the origin of heterospory in plants because many species in this genus have small genome sizes permitting the efficient use of molecular genetic techniques (reviewed by Tanurdzic and Banks 2004).

11.2.3 Gymnosperms

Monoecious Gymnosperms

Most gymnosperms are monoecious (Givnish 1980). There is a striking correlation between the breeding system and the mechanism of seed dispersal. Almost all gymnosperms are wind pollinated, except cycads, which are beetle-pollinated. Monoecious gymnosperms also rely on wind to disperse their seeds. In contrast, most dioecious gymnosperms possess fleshy fruits and their seeds are dispersed by animals (Givnish 1980). Exceptions to this rule have been reported; for example, trioecious and dioecious populations occur in Pinus edulis (Floyd 1983).

Dioecious Gymnosperms

Phylogenetic analyses indicate that dioecy may have been the ancestral condition in gymnosperms (Mathews et al. 2010). In general though, relatively little attention has been paid to the study of sex determination in dioecious gymnosperms. The main reason for this is likely due to long generation times and/or the large size of both plants and their genomes, which complicate genetic studies (see Leitch and Leitch 2013, this volume). However, a few species have attracted the attention of researchers because of their phylogenetic significance (see also Sect. 14.5 in Murray 2013, this volume).

Ginkgo

The staminate and ovulate trees of Ginkgo biloba possess the same number of chromosomes (2n = 24) and share almost identical chromosome morphology. The only difference is that in the ovulate trees; four chromosomes of the somatic complement have satellites while in the staminate tree only three chromosomes have satellites. In the male plant, the pair of short sub-telocentric chromosomes, only one of which has a satellite, is believed to be the sex chromosomes. An XY type of sex determination is assumed since the male possesses a heteromorphic pair of chromosomes (Lee 1954). To establish the necessary molecular tools to understand the evolution of seeds and pollen, Brenner et al. (2005) created a cDNA library and an EST dataset from the reproductive structures of male (microsporangiate), female (megasporangiate), and vegetative organs (leaves) of Ginkgo biloba. The analysis of this EST database from G. biloba has revealed genes that are potentially unique to gymnosperms. Many of these genes display a degree of homology with fully sequenced clones from the ESTs of a cycad. Other Ginkgo ESTs were found to be similar to developmental regulators in higher plants. This work has set the stage for future studies on Ginkgo as a means to better understand seed and pollen evolution, and resolve the ambiguous phylogenetic relationship of G. biloba to other gymnosperms.

Cycads

In Cycas pectinata, the male and female plants have the same number of chromosomes (2n = 22) with almost identical chromosome morphology. The only difference is that in the female plant two chromosomes of the somatic complement (pair III) have satellites, while in the male the same pair is heteromorphic and only one of its members has a satellite. This distinction becomes clearly visible when the two types of haploid complements are observed in pollen mitosis: one type possesses a satellite chromosome, and the other does not (Abraham and Mathew 1962). The construction of a cDNA library and an extensive EST study has already been started in C. rumphii (Brenner et al. 2003a).

11.2.4 Angiosperm Plants

The ancestral traits of angiosperm flowers are not yet clear; several hypotheses attempt to explain the origin of the hermaphrodite flower, which is currently the most wide spread flower type. According to the “Out Of Male (OOM)/Out Of Female (OOF) hypotheses,” hermaphrodite flowers developed as a modification of strobili containing both male and female flowers (Theissen and Becker 2004). According to the “Mostly Male (MM) theory,” the hermaphrodite flower developed from the male flowers of a gymnosperm ancestor by ectopic formation of ovules (Frohlich and Parker 2000). Different hypotheses for the origin of the angiosperm hermaphrodite flower make different predictions concerning the overlap between the genes expressed in the male and female cones of gymnosperms and the genes expressed in the hermaphrodite flowers of angiosperms. The Mostly Male theory predicts that, of genes expressed primarily in male versus female gymnosperm cones, an excess of male orthologs will be expressed in flowers, excluding ovules, while Out Of Male and Out Of Female theories predict no such excess. Data obtained by Tavares et al. (2010) fit better with the Out Of Male and Out of Female theories. However, it is doubtful that female and male ancestral characteristics of the angiosperm flower can be inferred from the number of expressed genes shared by female and male tissues, as differences between sexes are due to only a few genes or are quantitative (Tavares et al. 2010).

Monoecious Angiosperm Plants

Cucumis melo and C. sativus

Important data concerning the possible mechanisms of sex determination in Cucurbitaceae have been obtained in melons (Cucumis melo). In this mostly monoecious species, sex determination is governed by the genes andromonoecious (a) and gynoecious (g). The dominant allele of the a locus (CmACS-7 gene; 1-aminocyclopropane-1-carboxylic acid synthase) results in an arrest of stamen development (Boualem et al. 2008), while the dominant allele of the g locus causes an arrest of gynoecium development. Monoecious (A-G-) plants bear male flowers on the main stem and andromonoecious (aaG-) plants bear female or hermaphrodite flowers on the axillary branches. Gynoecious (AAgg) and hermaphrodite individuals (aagg) bear only female or hermaphrodite flowers respectively. The insertion of the Gyno-hAT transposon in the proximity of the g gene (CmWIP1) was shown to be a cause of the gynoecious phenotype of several lines (G to g change by hypermethylation of the promoter of the g gene, i.e., CmWIP1). The occasional presence of flowers with stamens and reduced ovaries suggests that DNA hypermethylation of CmWIP1 can be reduced during somatic development of gynoecious plants (Martin et al. 2009). Surprisingly, both CmACS-7 and its homolog from C. sativus are specifically expressed in female buds. The role of 1-aminocyclopropane-1-carboxylic acid synthase in anther arrest seems to be indirect and inter-organ communication is probably responsible for anther arrest (Boualem et al. 2009).

An analysis of the whole genome sequence of C. sativus revealed that the evolution of unisexual flowers in cucurbits may have involved the acquisition of two ethylene-responsive elements (AWTTCAAA) and one flower meristem identity gene LEAFY-responsive element (CCAATGT) of the ACS genes (Huang et al. 2009). Extensive EST analysis in unisexual and bisexual flower buds (using 454 sequencing) showed that six auxin-related genes (auxin can regulate sex expression by stimulating ethylene production) and three short-chain dehydrogenase or reductase genes (homologs to the sex determination gene ts2 in maize) are more highly expressed in unisexual flowers then in hermaphrodite flowers (Huang et al. 2009).

Zea mays

The formation of unisexual flowers in maize requires the selective elimination and sexual maturation of floral organs in an initially bisexual floral meristem. Elimination of pistil primordia occurs in the primary and secondary florets of tassel spikelets and in the secondary florets of ear spikelets. Ill-fated pistil cells undergo a cell death process associated with nuclear degeneration in a specific spatial-temporal pattern that begins in the subepidermis, eventually aborting the entire organ. The sex determination genes tasselseed1 (ts1) and tasselseed2 (ts2) are required for death of pistil cells, and ts1 is required for the accumulation of ts2 mRNA in pistil cells. All pistil primordia express ts2 RNA but functional pistils found in ear spikelets are protected from cell death by the action of the silkless1 (sk1) gene, which blocks tasselseed-induced cell death in the pistil primordia of primary ear florets. This basic model for the control of pistil fate by the action of the ts1-ts2-sk1 pathway was proposed by Calderon-Urrea and Dellaporta (1999). TASSELSEED2 converts steroids with specificities found at positions 3 and 17, and several dicarbonyl and quinone compounds, thus establishing TASSELSEED2 as a plant 3beta/17beta-hydroxysteroid dehydrogenase and carbonyl/quinone reductase. Taken together, the genetic data and the substrate specificities determined suggest that TS2 converts specific plant compounds and acts as a pre-receptor control mechanism in a manner similar to that of mammalian hydroxysteroid dehydrogenases (Wu et al. 2007). Later, studies by Parkinson et al. (2007) identified the role of two other genes in maize sex determination. Genes required to maintain repression (rm6) and mediator of paramutation 1 (mop1; putative RNA-dependent RNA polymerase) are involved in the suppression of the expression of silkless in the male inflorescence. Rmr6 maintains maize’s monoecious pattern of sex determination by restricting the function of the pistil-protecting factor SILKLESS1 from the apical inflorescence (Parkinson et al. 2007). The exact mechanism leading from TASSELSEED2 action to proper tassel formation is still unknown. It is, however, known that further genes are involved in stamen development promotion and gynoecium suppression: indeterminate spikelet1 (known also as Tasselseed6) genes and the group of Squamosa-promoter Binding Protein (SBP) box containing genes. Intron-exon structures as well as phylogenetic data support the division of these family members into six groups. The SBP-box genes upregulated in feminized tassels fall into two groups (out of six groups of SBP-box genes that have been distinguished in Zea mays according to phylogenetic analysis) that share common structural motifs and include the presence of a target site for miR156. Small RNA blots showed that miR156 levels are decreased in both mop1 and ts1 mutants. While there is a correlation between miR156 levels and SBP-box gene transcript levels, this correlation is not absolute, and thus it is hypothesized that decreased levels of miR156 may provide competency for SBP-box gene upregulation by other common factors yet to be identified. A model that suggests a putative link between ts1, ts2, ts4, Ts6, and mop1 in the sex-determination pathway was put forward by Hultquist and Dorweiler (2008). Progress has also been made in the study of the molecular mechanism of action of the putative master gene of sex determination in maize.

Acosta et al. (2009) positionally cloned and characterized the function of the sex determination gene ts1. The TS1 protein encodes a plastid-targeted lipoxygenase with predicted 13-lipoxygenase specificity, which suggests that TS1 may be involved in the biosynthesis of the plant hormone jasmonic acid. In the absence of a functional ts1 gene, lipoxygenase activity was missing and endogenous jasmonic acid concentrations were reduced in developing inflorescences. Application of jasmonic acid to developing inflorescences rescued stamen development in mutant ts1 and ts2 inflorescences, revealing a role for jasmonic acid in male flower development in maize (Acosta et al. 2009; Browse 2009). This suggests that jasmonic acid is likely to be involved in more complex effects than just the control of ts2. An updated model of sex determination in Zea is summarized in Fig. 11.1, which represents improvements to the original scheme suggested by Hultquist and Dorweiler (2008).
Fig. 11.1

Sex determination in maize (Zea mays). This scheme represents an updated “tasselseed based” control pathway of sex determination in maize. Only the variant that occurs in tassel is displayed. The genes that push development in the male direction are written in plain text whereas genes pushing development in the female direction are underlined. The names of gene products and names of mutants that led to gene identification are in brackets. Broken lines (e.g., from silkless1) denote genes not active in male inflorescences. The box symbolizes that the control pathway from tasselseed2 to pistil abortion and stamen promotion remains mostly unknown, though some genes have been identified. The dotted line symbolizes an artificial treatment. As apparent from the scheme, the role of jasmonate is probably more diverse than simply controlling tasselseed2 expression (modified according to Hultquist and Dorweiler 2008)

Dioecious Angiosperm Plants

Genus Silene

Silene latifolia: A Model for the Study of Sex Determination

Silene latifolia (Fig. 11.2a, b) is probably the best-studied plant sexual model. Chromosomes of S. latifolia (formerly Melandrium album) were first described in 1923 (Blackburn 1923; Winge 1923). Shortly after the species was used by Correns to study sex ratio bias (reviewed in Correns 1928a). The nuclear genomes of S. latifolia and S. dioica are relatively large and arranged into 12 chromosome pairs (see Fig. 11.3a–d). The pair of sex chromosomes is the largest in the genome: the Y is 1.4 times longer than the X chromosome. Deletion mutants have been an important tool in studies of sex determination in S. latifolia. For example, the use of deletion mutants has enabled the physical mapping and functional characterization of regions of interest within the sex chromosomes. Historically, spontaneous aberrant Y chromosomes were first studied by Westergaard (1946). By analysing different types of aberrations, he was able to conclude that in S. latifolia three different regions within the Y chromosome were important for correct sex expression in males. The upper region of the q-arm is critical for the suppression of gynoecium formation, the medium region of the Y is necessary for male promotion, and a portion of the q-arm is needed for male fertility (Westergaard 1946).
Fig. 11.2

Examples of model dioecious flowering plants. (a) Silene latifolia female flower, (b) S. latifolia male flower, (c) S. colpophylla female flower, (d) S. colpophylla male flower, (e) Rumex acetosa female flower bud section, (f) R. acetosa male flower bud section. Bars represent 5 mm (a–d) or 5 μm (e–f)

Fig. 11.3

Examples of chromosome preparations of dioecious species with heteromorphic sex chromosomes. (a) Silene latifolia, female metaphase, (b) S. latifolia, male metaphase, (c) S. dioica, female metaphase, (d) S. dioica, male metaphase, (e) Rumex acetosa, female metaphase, (f)R. acetosa, male metaphase. The bar represents 5 μm

The default sex in S. latifolia is female: when the Y is completely missing, flowers form only pistils. Recently, large scale deletions (disruptions) of the Y chromosome were introduced by means of either X-ray or gamma-irradiation. Lebel-Hardenack et al. (2002) irradiated pollen grains using a Siefert X-ray machine, while Farbos et al. (1999) used 60Co as a source of gamma rays. These studies, in addition to the deletion mutants observed already by Westergaard (1946), revealed hermaphrodites and infertile males. This can be taken as confirmation of Westergaard’s model of the Y chromosome in S. latifolia. The model of Y chromosome organization was improved by Zluvova et al. (2007), who showed the existence of male fertility genes close to the stamen promoter.

At present, few experimental data are available concerning the mechanism of gynoecium suppression in males of S. latifolia. Histological studies show a reduction of cell division in the central part of the male flower meristem (Matsunaga et al. 2004) while molecular studies have revealed the role of homologs of Arabidopsis thaliana SHOOTMERISTEMLESS (STM) and CUP SHAPED COTYLEDON (CUC) 1 and CUC2 genes in the arrest of gynoecium development in S. latifolia males (Zluvova et al. 2006). The data of Matsunaga et al. (2004) and Zluvova et al. (2006) suggest that the absence of STM and the presence of CUC 1 and CUC2 transcripts in the central part of the male flower meristem are the cause of reduced meristematic activity in this region. Independent of this pathway, gynoecium development in S. latifolia is also suppressed by the action of the CLAVATA1 gene, a putative member of the CLAVATA-WUSCHEL pathway (Koizumi et al. 2010). The results of Kazama et al. (2009) also indicate a possible role of SUPERMAN-like gene in the suppression of anther development in S. latifolia females.

Silene latifolia: A Model for the Study of Evolutionary Dynamics of Sex Chromosomes

While the majority of findings concerning sex chromosome evolution have come from research performed in human and animal models, a few plant species appear to be more suitable models for sex chromosome evolution owing to their recently evolved sex chromosomes (Table 11.1). Sex chromosomes, along with B chromosomes, are amongst the few parts of a plant genome that are feasible for chromosome painting techniques. While in animals, ordinary autosomes have specific patterns of DNA organization that allow researchers to distinguish individual chromosomes using complex probes, plant genomes are relatively homogenous and generally have few chromosome-specific DNA structures and sequences. In S. latifolia, microdissected sex chromosomes were used by Scutt et al. (1997) to investigate their genomic organization. The experiment was based on a semi-automatic technique of ablation of chromosomes and the mechanical transfer of chromosomes of interest to a membrane (polyester disk). Both X and Y chromosomes were used for DOP-PCR amplification and PCR products were subsequently labelled for FISH experiments (DOP-PCR is the method of choice for amplification of anonymous DNA with partially degenerated primers (Telenius et al. 1992)). Although sex chromosomes in S. latifolia are significantly different in their structure, the use of both probes (X- and Y-derived) revealed no sex chromosome-specific signal pattern. Similar data were obtained from experiments by Matsunaga et al. (1999).
Table 11.1

Comparison of characteristic properties of the most studied plant dioecious models (chrs = chromosomes, F = female, M = male, My = million years)

 

Carica papaya L.

Silene latifolia Poiret.

Rumex acetosa L.

Common name

Papaya

White campion

Sorrel

Family

Caricaceae

Caryophyllaceae

Polygonaceae

Genome size

1C = 0.372 pg

1C = 2.86 pg

1C = 3.55 pg

Karyotype

2n = 18 sex chromosomes homomorphic

2n = 24 (11pairs of autosomes plus 1 pair of sex chromosomes)

2n = 14(15) (6 pairs of autosomes plus XX or XY1Y2)

Heterogametic sex

Male

Male

Male

Sex chrs (F/M)

Not detected

XX/XY (Blackburn 1923)

XX/XY1Y2 (Kihara and Ono 1923)

Size of sex chrs

Not detected

The largest Y (9 %), the second X (8 %), smaller autosomes

The largest X (13 %), the second Y1 + Y2 (25 %), small autosomes

Chromatin of sex chrs

Non-recombining region of the Y heterochromatic (Zhang et al. 2008)

Standard as in autosomes (Grant et al. 1994)

The Ys are heterochromatic, histone H4-underacetylated (Lengerova and Vyskot 2001)

Age of sex chrs

2–3 My (Zhang et al. 2008)

Less than 5–10 My (Filatov 2005)

15–20 My (Jamilena et al. 2008)

Type of sex determination

Dominant Y in males (mammalian type)

Dominant Y in males (mammalian type)

X/A ratio (F = 1, M = 0.5) (Drosophila type)

Accumulation of Y-repeats

In the non-recombining region of the Y

Plastid DNA, DNA repeats, retrotransposons, microsatellites (Kejnovsky et al. 2009)

Y-specific repeats, microsatellites (Jamilena et al. 2008)

Availability of X-genes

Full genome sequence available (Liu et al. 2004)

At least 10 X (and) Y linked publically available genes

No sex chromosome linked genes available yet

A novel approach, which combined microdissection techniques and FISH procedures, was used by Hobza et al. (2004). To avoid any impurities during the dissection process, all manipulations were carried out with a laser beam using the PALM MicroLaser system (Fig. 11.4). The hybridization procedure was significantly shortened (1 h), and the amount of probe was decreased to a low concentration (30 ng/slide). Specific signals were observed using both X and Y probes. The differential labelling patterns of S. latifolia sex chromosomes under specific FISH conditions show rapid evolution of repetitive elements in the early stages of sex chromosome divergence (Hobza et al. 2004).
Fig. 11.4

Laser microdissection on Silene latifolia and Rumex acetosa metaphase chromosomes. The S. latifolia Y chromosome is localized under the inverted microscope (a). The membrane is cut around the selected chromosome using a laser microbeam, and the chromosome Y (b) and X (c) is transferred into the cap of a PCR tube. Similarly, the R. acetosa X chromosome is selected and separated from the rest of the chromosomes by microdissection (df)

Manual dissection of sex chromosomes was also successfully applied in experiments by Delichere et al. (1999), leading to the discovery of the first active gene to be isolated from a plant Y chromosome. Hernould et al. (1997) also performed microdissection, using an inverted microscope with extended microneedles operated by an electric micromanipulator. The glass tips of microneedles carrying chromosome fragments were broken off and pooled in an Eppendorf tube for subsequent experiments. Delichere et al. (1999) used 10 microdissected Y chromosomes as a template for DOP-PCR. The amplified DNA was used as a probe for screening a premeiotic male flower cDNA library to select Y-linked expressed sequences. To verify Y-linkage, segregation analysis was performed. Individual Y chromosome-derived clones were hybridized with restricted genomic DNA from male and female parental plants as well as their progeny. Out of the 115 clones selected after hybridization of complex Y probes with the cDNA library, only five clones revealed sex linkage after segregation experiments. A later study reported a level of DNA polymorphism in the Y-linked copy of the gene SlX1/SlY1 that was twenty times lower than the X-linked copy. These data were the first to suggest that processes involved in Y chromosome degeneration were also acting in the relatively young chromosomes of S. latifolia (Filatov et al. 2000).

In spite of their relatively young age it was shown that there is a similar gradient in silent site divergence between the X and Y copies of sex-linked genes on the sex chromosomes S. latifolia (Nicolas et al. 2005; Bergero et al. 2007). Silene latifolia Y-linked genes tend to evolve faster at the protein level than their X-linked homologs, and they have lower expression levels. Analysis of several Y-linked gene introns suggest they act as sites for transposable-element accumulation, which likely accounts for their increased length (Marais et al. 2008). These signs of degeneration are similar to those observed in animal Y-linked and neo-Y chromosome genes. Cermak et al. (2008) carried out a global survey of all of the major types of transposable elements in Silene latifolia. The localization of elements by FISH revealed that most of the Copia elements had accumulated on the Y chromosome. Surprisingly, one type of Gypsy element, which was similar to the Ogre elements known from legumes, was almost absent on the Y chromosome but otherwise uniformly distributed on all chromosomes. Other types of elements were ubiquitous on all chromosomes. Moreover, Cermak et al. (2008) isolated and characterized two new tandem repeats. One of them, STAR-C, was localized at the centromeres of all chromosomes except the Y chromosome, where it was present on the p-arm. Its variant, STAR-Y, which carries a small deletion, was specifically localized on the q-arm of the Y chromosome. FISH analysis of other Silene species revealed that some elements (e.g., Ogre-like elements) are confined to the section Elisanthe while others (e.g., Copia or Athila-like elements) are also present in more distantly related species. The unique pattern of repeat distribution found on the Y chromosome, where some elements have accumulated while other elements are conspicuously absent, probably reflects the different forces shaping the evolution of the Y chromosome (Cermak et al. 2008). Kubat et al. (2008) have shown that microsatellites accumulate in the q-arm of the Y chromosome (the arm containing the pseudoautosomal region) and this agrees with the findings of other authors (Morgante et al. 2002) showing that microsatellites are preferentially located in non-repetitive sequences.

However, repetitive sequences are not the only types of DNA to accumulate in the non-recombinant part of plant Y chromosomes. Sequence analysis has revealed that one of the Y chromosome-derived BACs contains part of the plastid genome, indicating that these plastid sequences have been transferred to the Y chromosome and may also contribute to its large size. Kejnovsky et al. (2006) found that plastid sequences located on the Y chromosome had higher rates of divergence in non-genic regions than in genic regions, which showed only very low (max 0.9 %) divergence from their plastid homologs.

The study of the Y chromosome-derived library has also revealed a case of horizontal gene transfer of a DNA fragment from the bacterium—Ralstonia solanacearum to the genome of S. latifolia. The homologs of this fragment (MK14) contain sequences that show similarities to a gene coding bacterial sulphate adenylyltransferase (CysN) and to a gene encoding uroporphyrin-III C-methyltransferase (nirE) (Talianova 2009). The reaction catalysed by sulphate adenylyltransferase constitutes the first enzymatic step in sulphate utilization following the uptake of sulphate (Leyh et al. 1992). Uroporphyrin-III C-methyltransferase in bacteria is involved in the biosynthesis of corrinoids such as vitamin B12, sirohaem and coenzyme F430 (Vévodová et al. 2004). The homologs of this fragment were subsequently found also in species that do not possess sex chromosomes, suggesting that the Y chromosome is unlikely to be more prone to the accumulation of horizontally acquired genes than regular autosomes.

Other Silene Species

Silene is a large genus, where the majority of species possess 12 pairs of chromosomes. In some dioecious species there is one pair of sex chromosomes plus 11 pairs of autosomes. This pattern which is supported by molecular data (Nicolas et al. 2005; Bergero et al. 2007), suggests that one pair of autosomes evolved into the pair of sex chromosomes in subgenus Behenantha, section Melandrium (classification according to Rautenberg et al. 2010). In contrast, the origin of sex chromosomes in subgenus Silene (classification according to Eggens et al. 2007, and Rautenberg et al. 2010) is probably different as indicated by the phylogenetic and genetic mapping data in S. colpophylla. Though many species share the same number of chromosomes, there are big differences in genome size among Silene species. For example, S. vulgaris and S. pendula belong to a group of small-genomed species (about 2 pg/C), while S. latifolia and S. chalcedonica possess relatively large genomes (3–5 pg/C, respectively). These differences raise questions about the mechanisms that have contributed to genome size evolution. Recent data indicate that there are large blocks of subtelomeric heterochromatin missing in some of the smaller genomes, which may account for much of these differences (Cermak et al. 2008). Subgenus Behenantha contains only five dioecious species: S. latifolia, S. dioica, S. diclinis, S. marizii, and S. heuffelii. Subgenus Silene contains several dioecious and subdioecious species, the best studied being S. otites and S. colpophylla (Fig. 11.2c, d) of the former section Otites, Wrigley (1986), now subsection Otites of the section Siphonomorpha, according to Oxelman (2010). Dioecy in section Melandrium is of monophyletic origin: the same pair of autosomes evolved into sex chromosomes in all species. In section Otites, genetic and phylogenetic analyses have been conducted to understand the sex-determining system and the origin of sex chromosomes in S. colpophylla (Mrackova et al. 2008). Here, it was shown that genes that are sex-linked in S. latifolia are also linked to each other in S. colpophylla, but they are not sex-linked. This finding demonstrates that the sex chromosomes in S. colpophylla (which are homomorphic) evolved from a different pair of autosomes than in S. latifolia. Phylogenetic analyses also support the view that the sex determination system of S. colpophylla, although it is XX/XY (similarly to section Melandrium), evolved independently in section Otites (Mrackova et al. 2008).

Genus Rumex

Various types of reproductive systems occur in Rumex: hermaphroditism, polygamy, gynodioecy, monoecy and dioecy (reviewed in Navajas-Pérez et al. 2005). In dioecious Rumex species, two different sex-chromosomal systems and sex-determining mechanisms have been described: XX/XY with an active Y chromosome (e.g., Rumex acetosella) and XX/XY1Y2 with sex determination based on the X/A ratio (e.g., Rumex acetosa, Figs. 11.2e, f and 11.3e, f). There is one exceptional species, Rumex hastatulus, which has two chromosomal “races”: the Texas race possessing XX/XY system and the North Carolina race with an XX/X Y1Y2 system. In this species, the X/A ratio controls sex determination, but the presence of the Y chromosome is necessary for male fertility (Smith 1963). In R. acetosa repetitive sequence similarity between both Y chromosomes suggests that they probably originated from one Y chromosome that underwent centromere fission and gave rise to a pair of metacentric chromosomes possessing identical chromosomal arms (isochromosomes). These isochromosomes were subsequently modified by deletions (Rejon et al. 1994). A recent phylogenetic study (Navajas-Pérez et al. 2005) indicates that all dioecious Rumex species evolved from a common hermaphroditic ancestor. The switch from a sex-determining mechanism based on the active role of the Y chromosome to a mechanism based on the X/A ratio occurred at least twice (Navajas-Pérez et al. 2005). The role of the X/A ratio in the sex determination of R. acetosa (reviewed by Parker and Clark 1991) resembles the sex-determining system of Drosophila, where the primary genetic sex-determining signal is provided by the ratio of X-linked genes to autosomal genes (Pomiankowski et al. 2004).

Hemp (Cannabis sativa)

Cannabis sativa or hemp is one of the few dioecious plant species possessing heteromorphic sex chromosomes, albeit the size difference between the X and Y chromosome is small (reviewed in Peil et al. 2003). Males are heterogametic (XY) and females homogametic (XX). The sex-determining system is the Drosophila type: the ratio of Xs to autosomes determines the sex rather than the active Y chromosome (revieved by Parker and Clark 1991). In contrast to other dioecious models (e.g., Silene latifolia and Rumex acetosa) the Y chromosome of C. sativa probably does not contain the genes necessary for male fertility. After stamen induction by ethylene synthesis inhibiting drugs (silver nitrate and silver thiosulphate anionic complex), fertile stamens develop in genetically female plants of hemp (Mohan Ram and Sett 1982). Sex determination in hemp is therefore probably under control of plant hormones, as changes in their levels often lead to sex changes (Chailakhyan and Khryanin 1978, 1979). Some features of Y chromosome degeneration have been found in hemp, for example, an accumulation of LINE-like retrotransposons at the terminal region of the longer arm of the Y chromosome has been reported (Sakamoto et al. 2000). Several genes that are involved in sex determination and/or sexual dimorphism have been identified using cDNA AFLP (Moliterni et al. 2004).

Hop (Humulus lupulus)

In spite of its agronomical importance, relatively little is known about the sex determination mechanism in hops. It is known that hops possess heteromorphic sex chromosomes and sex determination of XX/XY1Y2 i.e., sex determination is based on the ratio of the dosage of X chromosomes and autosomes (Parker and Clark 1991). Shephard et al. (2000) showed that obvious sex-related differences were already present in the plant at the stage of initiation of inflorescences suggesting that the genes involved in sex determination are probably already at work in advance of floral organogenesis (Shephard et al. 2000). Numerous sex-specific markers have been isolated in H. lupulus (Jakse et al. 2008) and a linkage map is available together with cytogenetic methods to distinguish between hop chromosomes (Karlov et al. 2003).

Papaya (Carica papaya)

Papaya is a favorite dioecious model because of its small nuclear genome size and importance as a crop. Papaya is polygamic and forms three basic sexual types: males, females, and hermaphrodites. Sex in papaya is determined by a single locus, which may have three different alleles (M1—male, M2—hermaphrodite, and m—female) (Storey 1969). Males must have the M1 dominant allele, while hermaphrodites possess the M2 allele and mm forms females. The combination of any two dominant alleles leads to seed abortion. Since males are heterogametic and females are homogametic, the sex determination can be classified as the XY type with a dominant Y chromosome. A large amount of DNA polymorphisms near the sex locus led to the recent discovery of the Y chromosome in papaya (Ma et al. 2004). There is a small 4–5 Mb region, called the MSY (male specific region Y), which harbors the primary sex-determining genes. Yu et al. (2007) proposed the hypothesis that recombination suppression in the sex-determining region of the Y chromosome is the result of its close proximity to the centromere.

Meadow-rue (Thalictrum dioicum)

Meadow-rue is a common weed in the Ranunculaceae family. The unisexual flowers lack any rudiments of the opposite sex since developmental arrest occurs very early during floral ontogeny. Thalictrum dioicum has homomorphic sex chromosomes and sex is genetically determined by a few loci. Males are heterogametic, and the genetic system of sex determination looks like the dominant Y system that is present in Silene latifolia and humans. The Y chromosomes in dioecious species of Thalictrum are probably not largely degenerate since YY males are viable even when no X copy is present in T. fendleri (Kuhn 1939). In dioecious plants like T. dioicum and Spinacia oleracea (see below), where vestiges of the opposite sex organs are missing, homeotic MADS-box genes are good candidates for sex determination genes. In T. dioicum, Di Stilio et al. (2005) isolated the organ identity genes (Agamous, Apetala3, and Pistillata) and showed that they had been duplicated and had diverged in expression. Efficient virus-induced gene silencing (VIGS), using tobacco rattle virus (TRV) vectors, has been achieved, permitting deep analysis of sex determination mechanisms (Di Stilio et al. 2010).

Spinach (Spinacia oleracea)

Spinach is predominantly a dioecious species. However, genetically-determined monoecious lines also exist (Janick and Stevenson 1954), and sex expression also depends on environmental influences. For example, high temperatures promote maleness in monoecious lines (reviewed in Iizuka and Janick 1962). The sex-determining system is XX/XY (reviewed in Haga 1934). X and Y chromosomes are of similar size and morphology, but some Y chromosomes lack a 45S rDNA locus (Lan et al. 2006). Sex determination in S. oleracea is based on a single locus with three alleles: X, Xm and Y (Janick and Stevenson 1954). The allele Xm is incompletely dominant because XmXm individuals are monoecious, but individuals with XmX produce a higher proportion of pistillate flowers. The Y allele is completely dominant, and thus XY and XmY plants show the male phenotype.

The exact molecular basis of the sex determination system in S. oleracea is unknown. However, a study of the B class floral identity genes SpAPETALA3 and SpPISTILLATA in S. oleracea showed their effect on sexual dimorphism and suggested a role in sex determination (Pfent et al. 2005). The gene SpAgamous is involved in sex-specific gynoecium control in spinach (Sather et al. 2005). Interestingly, sexual dimorphism in this species can vary in intensity depending on the presence of a special locus located on the Y chromosome that causes a “bracted male” phenotype showing a habit different from female plants (reviewed in Iizuka and Janick 1962). Indeed, there are many indications that the sex chromosomes of S. oleracea are young, but this does not necessarily imply that the sex determination system is also young and it is possible that the sex determination system is derived from monoecy. In this case, a single gene controlling the number and/or position of male and female flowers could have been directly transformed into a sex determining gene by sexually antagonistic selection. Given the small size of the spinach genome, it is suitable for basic genomic studies (Khattak et al. 2006) and recent RNAi technology applying a VIGS approach has permitted a functional genomic strategy to be adopted. Such studies showed how the suppression of B class genes led to sex reversal via a homeotic transformation of stamens into carpels (Sather et al. 2010) confirming the view that sex determination in spinach is based on the regulation of B class gene expression.

Mercurialis annua

Mercurialis annua has a simple genetically-based sex determining system. There seem to be three unlinked loci—A/a, B1/b1, and B2/b2—which act complementarily. The male plants usually need the dominant A allele and at least one dominant B allele. Moreover, in Mercurialis sex can be modulated by exogenously applied growth regulators. In females, the presence of trans-zeatin was shown. An application of auxin leads to masculinisation of female flowers (Hamdi et al. 1987). Khadka et al. (2002) reported the characterization of a previously identified male-specific DNA marker, OPB01-1562, from the diploid dioecious M. annua. RNA blot hybridization with OPB01-1562 and MARL-1 detected a transcript that was expressed strongly in the stems and flowers of females but not males. The M. annua female-expressed (Mafex) transcript may thus play a role in sex determination (Khadka et al. 2005).

Hybridization and polyploidy are widely believed to be important sources of evolutionary novelty in plant evolution (see for review, Soltis et al. 2010; Fawcett et al. 2013, this volume). Both can lead to novel gene combinations and/or novel patterns of gene expression, which in turn provide the variation on which natural selection can act. Obbard et al. (2006) used nuclear and plastid gene trees, in conjunction with morphological data and genome size measurements, to show that both processes have been important in shaping the evolution of Mercurialis. Their results indicate that hexaploid populations of M. annua, in which the otherwise rare sexual system androdioecy is common (the occurrence of males and hermaphrodites), is of allopolyploid origin involving hybridization between a monoecious autotetraploid lineage of M. annua and the related dioecious diploid species M. huetii—an event that brought together the genes for specialist males with those for hermaphrodites (Obbard et al. 2006). Dorken and Pannell (2008) found that the progeny sex ratio is strongly dependent on density, with fewer males produced when plants are grown at low density. This occurred in part because of a flexible adjustment in pollen production by hermaphrodites, which produced more pollen when grown at low density than at high density. These results provide support for the prediction that environmental conditions govern sex ratios through their effects on the relative fertility of unisexual versus hermaphrodite individuals (Dorken and Pannell 2008).

Bryonia dioica: The First Dioecious Model in Which the Genetic Basis of Sex Determination was Elucidated

Most species of the Cucurbitaceae family comprising c. 800 species have unisexual flowers, 460 are monoecious, and 340 are dioecious. Some species produce a mixture of bisexual, female, and male flowers in various intra- and inter-individual patterns, and populations can be andromonoecious, androdioecious, gynomonoecious or gynodioecious (Kocyan et al. 2007). Phylogenetic studies suggest that dioecy is the ancestral state in this family (Zhang et al. 2006). However, as various switches to monoecy or to other types of reproductive systems, including androdioecy, have occurred during the evolution of Cucurbitaceae, it is therefore difficult to precisely ascertain how old the sex chromosomes in a given species are (Renner et al. 2007). The best-studied genus containing dioecious species is Bryonia. Genetic crosses between the dioecious B. dioica and the monoecious B. alba in 1903 provided the first clear evidence for Mendelian inheritance of sexual phenotypes (dioecy) and made B. dioica the first organism for which the XY sex-determination was experimentally proven (Correns 1928b). Applying molecular tools to this system, Oyama et al. (2009) showed that the size of the non-recombining region may differ between the north-European and southern-European populations. Important data concerning the possible mechanisms of flower sex determination in monoecious Cucurbitaceae were recently obtained in melons (C. melo) and in the cucumber (C. sativus, see Sect. 11.2.4.1.1 in this chapter).

Date Palm (Phoenix dactylifera)

The date palm is a dioecious species displaying strong dimorphism between pistillate and staminate flowers. Siljak-Yakovlev et al. (1996) described a cytological method using chromomycin staining that demonstrates the occurrence of sex chromosomes based on distinctive nucleolar heterochromatin. This offers the possibility of identifying male and female individuals by a simple analysis of root meristems. This observation has been extended by in situ rDNA hybridization, confocal microscopy and dual-label flow cytometry of nuclei (Siljak-Yakovlev et al. 1996). The mechanism of arrest of gynoecium development in the date palm appears to be similar to that in Silene latifolia. The earliest sex-related difference in flower buds is observed when the number of cells in the gynoecium of pistillate flowers is higher than that in their staminate counterparts. In the pistillate flower, staminodes (sterile stamens) display precocious arrest of development followed by cell differentiation. In the staminate flower, pistillodes (sterile gynoecium) undergo some degree of differentiation, but their development ceases shortly after the ovule has been initiated. Staminode and pistillode cells exhibit nuclear integrity although they do not show any accumulation of histone H4 gene transcripts. These results suggest that the developmental arrest of sterile sex organs and the subsequent unisexuality of date palm flowers result from a cessation of cell division and precocious cell differentiation rather than from cell death (Daher et al. 2010).

11.3 Sexual Dimorphism

Sexual dimorphism, the sex-specific expression of some genes not involved directly in sex determination, presumably results from different modes of selection operating in males and females: males are limited in their reproductive success by access to mates, whereas females are more limited by resources (Bateman 1948; Jones et al. 2002). In animals, the evolution of sexual dimorphism is primarily driven by competition between males and selection for traits recognized by females as indicators of male fitness (reviewed by Hall et al. 2000). Similar principles may be at work in animal-pollinated plants. In S. latifolia, odor-compounds involved in pollinator attraction differ significantly between sexes, suggesting that selection for higher attractiveness among competing males is mediated by the sensory ecology of the pollinator (Waelti et al. 2009). In addition, males produce on average up to 16 times more flowers than pollinated females (Laporte and Delph 1996). This difference in flower number may be driven by a combination of male competition and, at least partly, by a higher consumption of resources by developing seeds in pollinated female flowers, which results in a trade-off between seed size and flower number. The difference in flower number is less pronounced in non-pollinated females, which produce on average only four times fewer flowers than males (Laporte and Delph 1996; Steven et al. 2007). It also seems reasonable to expect that differences in the vegetative parts of plants evolved in concert with the flower types or architecture of inflorescences carried by the plant. Many sexually-dimorphic traits could evolve as a consequence of their correlation with other sexually dimorphic traits and so they need not be of adaptive value (Dawson and Geber 1999). For instance, correlations between flower size and the size of the stem leaves have been reported in many species (reviewed by Dawson and Geber 1999). Variation in sex-limited genes with pleiotropic effects and/or linkage between sex-limited loci also occurs in S. latifolia (Steven et al. 2007). These authors statistically predicted that selection for increased flower number in males along with weak selection for increased flower size in females could lead to dimorphic evolution in several other traits including leaf mass.

Almost all of the sexually dimorphic traits in S. latifolia described so far become apparent only after the initiation of flowering. Notable exceptions to this include: sex-dimorphism in the long-term survival of buried seeds and burial induced dormancy in S. latifolia (Purrington and Schmitt 1995), and sex-dimorphism in emergence time and time to flowering (Doust et al. 1987; Purrington and Schmitt 1998). Zluvova et al. (2010) provided molecular evidence that sexually dimorphic gene expression is present in S. latifolia at the rosette stage, a long time before the initiation of flowering.

Recently, Janoušek and Mrackova (2010) have taken up the so far neglected question of how a system based on two separate sex-controlling pathways regulated by genes present on the Y chromosome (Charlesworth and Charlesworth 1978) is transformed into a system controlled by the X/A ratio in some species (as in some species of Rumex). They suggest the following scenario. In the first step (Fig. 11.5a), dioecy evolves from gynodioecy via a gynoecium-suppressing gene in the proximity of the male fertility controlling gene. This process is promoted by sexually antagonistic selection. The original theory (Charlesworth and Charlesworth 1978) supposes just one male sterility mutation, implying that the male fertility locus of the gynodioecious ancestor is identical with the anther-promoting gene of the resulting dioecious species. The possibility of a step-wise shift in stamen arrest was discussed by Zluvova et al. (2005), but does not essentially change the predictions of the model. In a second step (Fig. 11.5b), sexually antagonistic selection continues and improves the linkage of the sex-determining loci. Sex chromosomes that are created by this process can continue to accumulate sexually antagonistic alleles (Rice 1984). Even in species that are at this stage of sex determination, it is possible to find early expressed sexual dimorphism (e.g., Silene latifolia; Zluvova et al. 2010).
Fig. 11.5

The evolution of the sex-determining pathways in plants. (a) The theory of the origin of dioecy via male sterility as suggested by Charlesworth and Charlesworth (1978). Both the gynoecium suppressor and the stamen (anther) promoter act independently, but their coordination is achieved by their proximity on the Y chromosome or by their location in the non-recombining region of the Y chromosome. (b) Formation of sex chromosomes. Accumulation of sexually antagonistic genes (SAG) and the reduction of recombination frequency between gynoecium suppressing and male fertility controlling genes creates sex chromosomes. For simplicity, only one sexually antagonistic gene is presented. SAG-F means a sexually antagonistic allele advantageous for females, and SAG-M means a male advantageous sexually antagonistic allele of the same gene. (c) A sexually antagonistic gene(s)-based switch in the sex-determining pathway. Sexual dimorphism (controlled by SAG-M) is improved step-by-step and starts to act before the Y-linked genes involved in female and stamen development. At a certain stage, the expression of both the gynoecium suppressor and the stamen promoter becomes sex limited as a consequence of their adaptation to sex specific expression profiles of other genes. (d) The restructuring of the sex chromosomes. The gynoecium suppressor and stamen promoting gene(s) are lost from the Y chromosome and transferred to the autosome(s). (e) The origin of an X/A based sex-determining system. SAG-M is lost from the Y chromosome and transferred to an autosome. The X/A ratio becomes crucial for sex determination as SAG-M pushes development toward the male direction in contrast to SAG-F that pushes development toward the female direction

In the third step (Fig. 11.5c), sex-determining genes start to accommodate to the sex-specific gene expression patterns controlled by the sexually antagonistic gene(s) (SAG) and their expression starts to be controlled by these genes. Eventually, the gene(s) that previously controlled sexual dimorphism become(s) sex-determining gene(s). It is known that sexually antagonistic genes evolve fast (reviewed in Qvarnström and Bailey 2009) and a good example of this in plants is the Y-linked genes from S. latifolia. The lack of a Y chromosome in S. latifolia cannot be completely compensated for by the presence of the genome of the related species S. viscosa, and anther defects in hybrids between S. latifolia and S. viscosa resemble two different mutants lacking part of the Y chromosome (Zluvova et al. 2005). The active role of the Y chromosome in sex determination is still preserved because the new sex-determining locus is still located on the Y chromosome. An important difference from the previous stages is that connection between the control of stamen promotion and anther suppression is established. This creates new possibilities for the evolution of the sex-determining system. In a plant species possessing this kind of sex determination, a single master gene mutation should be able to cause a male to female transformation.

In the fourth step (Fig. 11.5d), two things could have happened. The original sex-determining loci could be lost from the Y chromosome by chance or the translocation of the original sex-determining region to the autosomes could be supported by Y chromosome degeneration due to the absence of recombination. Since stamen promotion and gynoecium suppression are already controlled by the single controlling pathway, the genotypes possessing a translocation of these genes to autosomes can be selected for because they can escape from the process of degeneration. The change of the position of these genes does not influence the sexual phenotype, as they have sex-limited expression and are controlled by the gene derived from the gene that initially controlled only sexual dimorphism.

In the fifth step (Fig. 11.5e), the secondary sex-determining locus loses its controlling role as well, and control of sex determination is co-opted by alternative mechanisms, such as an X/A ratio mechanism. The switch could be similar to the mechanisms described in fishes and insects (reviewed by Schütt and Nöthiger 2000; Volff et al. 2007). One of the genes, “a slave” in the sex-determining pathway located on the X chromosome, can become “a master”. Simultaneously, the function of this new master gene is influenced by genes located on autosomes. An important prerequisite of this kind of transformation of the sex-determining system is that stamen promotion and gynoecium suppression are controlled by the same pathway. This fifth step in the evolution of the sex-determining pathway may have been reached in hemp (Cannabis), hop (Humulus), and sorrel (Rumex).

Veltsos et al. (2008) performed computer modelling experiments in order to explain spread of neo-sex chromosomes in the grasshopper Podisma pedestris. In this species, neo-X chromosomes (autosomes fused to original X) and neo-Y chromosomes (unfused autosome) have spread and become fixed in a large geographical territory. Computer modelling experiments showed that the continuous invasion of the neo-Y chromosome (carrying a sexually antagonistic allele) in the hybrid zone can cause selection in favour of the neo-X chromosome. Afterwards, also the neo-Y chromosome that is, in the initial phase, continuously removed by selection can be selected for as a consequence of the neo-X accumulation. Interestingly, the same mechanism may be involved in the spread and fixation of the degenerated Y chromosomes. It is apparent that, in many plant (e.g., Carica papaya, Silene latifolia, and Asparagus officinalis, reviewed by Ming et al. 2007) and animal species (e.g., most mammals, reviewed by Wilhelm et al. 2007) this evolution is not complete because many species still rely on an active role of the Y chromosome in sex determination.

Instability of sex expression and/or cytologically homomorphic sex chromosomes are sometimes taken as a sign of the primitive status of the evolution of sex-determining systems (e.g., Vyskot and Hobza 2004). Data obtained in the animal models, however, suggest that even very advanced sex-determining systems (as in mammals) can show a considerable plasticity of sex expression (e.g., Bianchi 2002). Only comparative sequencing and phylogenetic analyses can answer the question of the age of sex-determining pathways.

11.4 The Current Status of Research and Prospects for the Future

An overview of currently used approaches for studying sex determination in plants and their inter-connection is provided in Fig. 11.6. Separation of the chromosome(s) by microdissection and chromosome sorting is the most straightforward technique for isolating chromosome-specific DNA. The use of these techniques enabled researchers to isolate the first active plant Y-linked gene (Delichere et al. 1999). Moreover, the construction and utilization of chromosome-specific libraries and the use of sorted chromosomes as complex probes has improved our knowledge of sex chromosomes, mainly in Rumex acetosa and Silene latifolia. However, only the few species with morphologically different chromosomes are suitable for dissection techniques.
Fig. 11.6

A diagrammatic sketch of the methods frequently used for the isolation and characterization of sex-linked DNA. Dissection of chromosomes is the method of choice for generating complex probes for FISH (fluorescence in situ hybridization), constructing chromosome-specific libraries and as a tool for mapping DNA markers using specific chromosomes as a template. A subtractive approach (e.g., RDA—representational difference analysis) is used for the isolation of sample-specific DNA (e.g., in the comparison of male and female genomic DNA or the comparison of sex-specific expression patterns). Nowadays, traditional molecular subtractive methods are replaced by comparisons of different DNA databases. Genetic mapping is still the basic method for analysis of DNA markers and their linkage to phenotypically interesting mutations (AFLP—amplified fragment length polymorphisms; RAPD—Random Amplification of Polymorphic DNA). A combination of genetic maps with information on complete genome sequences is a key approach for the identification and isolation of novel genes and the deduction of their function

High-throughput sequencing methods accelerate whole-genome sequencing (Tuskan et al. 2006; Ming et al. 2008) and permit the construction of huge EST and genomic databases. Comparisons of different pools of sequenced samples (males versus females, generative tissue versus vegetative tissue) may help identify sex-determining genes and to characterize sex expression pathways (Blavet et al. 2011).

Important questions regarding the basic biological processes affecting the evolution of sex chromosomes that could be answered in the next decade are: How do sex chromosomes degenerate? Is degeneration of genes in non-recombining regions really a one-way ticket as it is in many animal species? Is dosage compensation a general phenomenon for regulating the level of expression in organisms with degenerating sex chromosomes?

Notes

Acknowledgment

This research was supported by the Grant Agency of the Czech Republic (grants P501/10/0102, 522/09/0083, and 521/08/0932).

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© Springer-Verlag Wien 2013

Authors and Affiliations

  1. 1.Institute of BiophysicsAcademy of Sciences of the Czech RepublicBrnoCzech Republic
  2. 2.Laboratory of Plant Developmental Genetics, Institute of BiophysicsAcademy of Sciences of the Czech RepublicBrnoCzech Republic

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