Adaptation of the autosomal part of the genome on the presence of dioecy

We have attempted to answer the question of whether the presence of sex chromosomes in the genome can affect the evolution of the autosomal part of the genome. As a model, we used dioecious plants from the section Otites of the genus Silene. We have observed a rise in adaptive evolution in the autosomal and pseudoautosomal parts of the genome, which are associated with the evolution of dioecy. This rise is caused neither by the accumulation of sexually antagonistic genes in the pseudoautosomal region nor by the co-evolution of genes acting in mitochondria (in spite of the fact that the dioecy evolved in this case most likely from cytoplasmic male sterility). Thus, this rise in the amount of positively selected codons is most likely caused by the adaptive evolution of genes involved in the specialization of the autosomal part of the genome on the dioecy as described in sex-allocation theory.

The Diversity and Dynamics of Sex Determination in Dioecious Plants

The diversity of inflorescences among flowering plants is captivating. Such charm is not only due to the variety of sizes, shapes, colors, and flowers displayed, but also to the range of reproductive systems. For instance, hermaphrodites occur abundantly throughout the plant kingdom with both stamens and carpels within the same flower. Nevertheless, 10% of flowering plants have separate unisexual flowers, either in different locations of the same individual (monoecy) or on different individuals (dioecy). Despite their rarity, dioecious plants provide an excellent opportunity to investigate the mechanisms involved in sex expression and the evolution of sex-determining regions (SDRs) and sex chromosomes. The SDRs and the evolution of dioecy have been studied in many species ranging from Ginkgo to important fruit crops. Some of these studies, for example in asparagus or kiwifruit, identified two sex-determining genes within the non-recombining SDR and may thus be consistent with the classical model for the evolution of dioecy from hermaphroditism via gynodioecy, that predicts two successive mutations, the first one affecting male and the second one female function, becoming linked in a region of suppressed recombination. On the other hand, aided by genome sequencing and gene editing, single factor sex determination has emerged in other species, such as persimmon or poplar. Despite the diversity of sex-determining mechanisms, a tentative comparative analysis of the known sex-determining genes and candidates in different species suggests that similar genes and pathways may be employed repeatedly for the evolution of dioecy. The cytokinin signaling pathway appears important for sex determination in several species regardless of the underlying genetic system. Additionally, tapetum-related genes often seem to act as male-promoting factors when sex is determined via two genes. We present a unified model that synthesizes the genetic networks of sex determination in monoecious and dioecious plants and will support the generation of hypothesis regarding candidate sex determinants in future studies.

Variation in mtDNA haplotypes suggests a complex history of reproductive strategy in Cannabis sativa

ABSTRACTCannabis is one example in angiosperms that appears to have a recent origin of dioecy and X/Y sex chromosomes. Several evolutionary explanations for this transition have been proposed, with the most parsimonious beginning with a mitochondrial mutation leading to cytoplasmic male sterility (CMS). Our study utilized 73 Cannabis sativa whole genome shotgun libraries to reveal eight different mtDNA haplotypes. The most common haplotype contained 60 of the 73 individuals studied and was composed of only dioecious individuals. However, other haplotypes contained a mix of dioecious and monoecious individuals, so haplotype alone does not predict dioecy. From these haplotype groupings we further examined the fully annotated mitochondrial genomes of four hemp individuals and looked for genetic variation affecting reproductive strategy (e.g., monoecious vs. dioecious strategies). Specifically, we searched for markers associated with CMS and for gene rearrangements within these mitochondrial genomes. Our results revealed highly syntenic mitochondrial genomes that contained approximately 60 identifiable sequences for protein coding genes, tRNAs and rRNAs and no obvious rearrangements or chimeric genes. We find no clear evidence that the different reproductive patterns are due to easily identifiable CMS mutations. Our results refute the simplest hypothesis that there was a single recent origin of dioecy in a monoecious ancestor. Instead, the story of the evolution of dioecy is likely much more complex. Further exploration of the nuclear and mitochondrial genomes and their interaction is required to fully understand Cannabis’ mating strategies and the possible existence of CMS in this species.

Inferring the genetic basis of sex determination from the genome of a dioecious nightshade

ABSTRACTDissecting the genetic mechanisms underlying dioecy (i.e. separate female and male individuals) is critical for understanding the evolution of this pervasive reproductive strategy. Nonetheless, the genetic basis of sex determination remains unclear in many cases, especially in systems where dioecy has arisen recently. Within the economically important plant genus Solanum (∼2000 species), dioecy is thought to have evolved independently at least 4 times across roughly 20 species. Here, we generate the first genome sequence of a dioecious Solanum and use it to ascertain the genetic basis of sex determination in this species. We de novo assembled and annotated the genome of S. appendiculatum (assembly size: ∼750 Mb; scaffold N50: 0.92 Mb; ∼35,000 genes), identified sex-specific sequences and their locations in the genome, and inferred that males in this species are the heterogametic sex. We also analyzed gene expression patterns in floral tissues of males and females, finding ∼100 genes that are differentially expressed between the sexes. These analyses, together with observed patterns of gene-family evolution specific to S. appendiculatum, consistently implicate a suite of genes from the regulatory network controlling pectin degradation and modification in the expression of sex. Furthermore, the genome of a species with a relatively young sex determination system provides the foundational resources for future studies on the independent evolution of dioecy in this speciose clade.

Sex-Related Differences in Growth, Herbivory, and Defense of Two Salix Species

Sex-related differences in sex ratio, growth, and herbivory are widely documented in many dioecious plants. The common pattern is for males to grow faster than females and to be less well-defended against herbivores, but Salix is an exception. To study sex-related differences in the patterns of resource allocation for growth and defense in willows, we conducted a large-scale field experiment to investigate the flowering sex ratio, mortality, growth traits, insect herbivory and content of defensive substances in three Salix populations comprising two species. Results demonstrate that the two Salix suchowensis Cheng populations have a female bias in the sex ratio, whereas no bias is found in the S. triandra L. population. Male individuals in the S. suchowensis populations have significantly higher mortality rates than females. However, the mortality rate of S. triandra population has no gender difference. This finding may be one of the explanations for the difference in sex ratio between the two species. The females are larger in height, ground diameter, and biomass, and have a higher nutritional quality (N concentration) than males in both species. Nevertheless, slow-growing males have a higher concentration of the defense chemical (total phenol) and lower degrees of insect herbivory than females. Additionally, biomass is positively correlated with herbivory and negatively correlated with defense in the two willow species. It is concluded that the degrees of herbivory would have a great influence on resource allocation for growth and defense. Meanwhile, it also provides important implications for understanding the evolution of dioecy.

Two antagonistic effect genes mediate separation of sexes in a fully dioecious plant

Plant sex determining systems and sex chromosomes are often evolutionarily young. Here, we present the early stage of sex chromosome in a fully dioecious plant, P. deltoides, by determining separate sequences of the physically small X- and Y-linked regions. Intriguingly, two Y genes are absent from the X counterpart. One gene represses female structures by producing siRNAs that block expression of a gene necessary for development of female structures, via RNA-directed DNA methylation and siRNA-guided mRNA cleavage. The other gene generates long non-coding RNA transcripts that, in males, soak up miRNAs that specifically inhibit androecium development. Transformation experiments in Arabidopsis thaliana show that the two genes affect gynoecium and androecium development independently and antagonistically. Sex determination in the poplar therefore has the properties proposed for the first steps in the evolution of dioecy in flowering plants, with two genes whose joint effects favor close linkage, as is observed in poplar.

Pleiotropic effects of sex-determining genes in the evolution of dioecy in two plant species

One reason for studying sex chromosomes of flowering plants is that they have often evolved separate sexes recently, and the genomes of dioecious species may not yet have evolved adaptations to their changes from the ancestral state. An unstudied question concerns the relative importance of such adaptation, versus the effects of the mutations that led to separate sexes in the first place. Theoretical models for such an evolutionary change make the prediction that the mutations that created males must have sexually antagonistic effects, not only abolishing female functions, but also increasing male functions relative to the ancestral functional hermaphrodites. It is important to test this critical assumption. Moreover, the involvement of sexual antagonism also implies that plant sex-determining genes may directly cause some of the sexual dimorphisms observed in dioecious plants. Sex-determining genes are starting to be uncovered in plants, including species in the genera Diospyros and Actinidia (families Ebenaceae and Actinidiaceae, respectively). Here, we describe transgenic experiments in which the effects of the very different male-determining genes of these two dioecious species were studied in a non-dioecious plant, Nicotiana tabacum . The results indeed support the critical assumption outlined above.

Two Y chromosome-encoded genes determine sex in kiwifruit

ABSTRACTDioecy, the presence of male and female individuals, has evolved independently in multiple flowering plant lineages. Although theoretical models for the evolution of dioecy, such as the “two-mutation” model, are well established, little is known about the specific genes determining sex and their evolutionary history. Kiwifruit, a major tree crop consumed worldwide, is a dioecious species. In kiwifruit, we had previously identified a Y-encoded sex-determinant candidate gene acting as the suppressor of feminization (SuF), named Shy Girl (SyGI). Here, we identified a second Y-encoded sex-determinant that we named Friendly boy (FrBy), which exhibits strong expression in tapetal cells. Gene-editing and complementation analyses in Arabidopsis thaliana and Nicotiana tabacum indicated that FrBy acts for the maintenance of male (M) functions, independently of SyGI, and that these functions are conserved across angiosperm species. We further characterized the genomic architecture of the small (< 1 Mb) male specific region of the Y-chromosome (MSY), which harbors only two genes significantly expressed in developing gynoecia and androecia, respectively: SyGI and FrBy. Resequencing of the genome of a natural hermaphrodite kiwifruit revealed that this individual is genetically male but carries deletion(s) of parts of the Y-chromosome, including SyGI. Additionally, expression of FrBy in female kiwifruit resulted in hermaphrodite plants. These results clearly indicate that Y-encoded SyGI and FrBy act independently as the SuF and M factors in kiwifruit, respectively, and provide insight into the evolutionary path leading to a two-factor sex determination system but also a new breeding approach for dioecious species.

Origen, mantenimiento y evolución del ginodioicismo

One of the main characteristics of Angiosperms is the great diversity of reproductive systems they present. Gynodioecy, namely the coexistence of hermaphrodite and female plants in the same population, is an example of such diversity. In this study we present the main characteristics of gynodioecious species, such as the large variation in female frequency among populations. We examine the three forms by which male sterility can be originated and transmitted, and their consequences for the evolutionary dynamics. We present and discuss the hypothesis that would explain the maintenance of females in populations, since due to the lack of male function, they need to produce more or better seeds than hermaphrodites to avoid a disadvantage. We analyze the main evolutionary routes beginning from a hermaphroditic condition, and the existing evidences that suggest gynodioecy as the main path in the evolution of dioecy. Finally, we analyze the present state of the investigation of reproductive systems in Mexico, using as an example the study of the gynodioecy.