A phylogenomic inventory of meiotic genes; evidence for sex in Giardia and an early eukaryotic origin of meiosis

Sexual reproduction in eukaryotes is accomplished by meiosis, a complex and specialized process of cell division that results in haploid cells (e.g., gametes). The stereotypical reductive division in meiosis is a major evolutionary innovation in eukaryotic cells, and delineating its history is key to understanding the evolution of sex. Meiosis arose early in eukaryotic evolution, but when and how meiosis arose and whether all eukaryotes have meiosis remain open questions. The known phylogenetic distribution of meiosis comprises plants, animals, fungi, and numerous protists. Diplomonads including Giardia intestinalis (syn. G. lamblia) are not known to have a sexual cycle; these protists may be an early-diverging lineage and could represent a premeiotic stage in eukaryotic evolution. We surveyed the ongoing G. intestinalis genome project data and have identified, verified, and analyzed a core set of putative meiotic genes-including five meiosis-specific genes-that are widely present among sexual eukaryotes. The presence of these genes indicates that: (1) Giardia is capable of meiosis and, thus, sexual reproduction, (2) the evolution of meiosis occurred early in eukaryotic evolution, and (3) the conserved meiotic machinery comprises a large set of genes that encode a variety of component proteins, including those involved in meiotic recombination.     

Ancestral Eukaryotes Reproduced Asexually,Facilitated by Polyploidy: A Hypothesis

The notion that eukaryotes are ancestrally sexual has been gaining attention. This idea comes in part from the discovery of sets of “meiosis‐specific genes” in the genomes of protists. The existence of these genes has persuaded many that these organisms may be engaging in sex, even though this has gone undetected. The involvement of sex in protists is supported by the view that asexual reproduction results in the accumulation of mutations that would inevitably result in the decline and extinction of such lineages. It is argued that this phenomenon can be obviated by polyploidy and that the “meiosis‐specific genes” are used in other processes, including polyploidy control and homologous recombination, independent of meiosis. These phenomena account for the finding that these genes are expressed in cultures devoid of apparent cell fusion events. Hence, it is also proposed that asexual, and not sexual, reproduction is the ancestral condition.     

The evolution of meiotic sex and its alternatives

Meiosis is an ancestral, highly conserved process in eukaryotic life cycles, and for all eukaryotes the shared component of sexual reproduction. The benefits and functions of meiosis, however, are still under discussion, especially considering the costs of meiotic sex. To get a novel view on this old problem, we filter out the most conserved elements of meiosis itself by reviewing the various modifications and alterations of modes of reproduction. Our rationale is that the indispensable steps of meiosis for viability of offspring would be maintained by strong selection, while dispensable steps would be variable. We review evolutionary origin and processes in normal meiosis, restitutional meiosis, polyploidization and the alterations of meiosis in forms of uniparental reproduction (apomixis, apomictic parthenogenesis, automixis, selfing) with a focus on plants and animals. This overview suggests that homologue pairing, double-strand break formation and homologous recombinational repair at prophase I are the least dispensable elements, and they are more likely optimized for repair of oxidative DNA damage rather than for recombination. Segregation, ploidy reduction and also a biparental genome contribution can be skipped for many generations. The evidence supports the theory that the primary function of meiosis is DNA restoration rather than recombination.     

Tetrahymena meiosis: Simple yet ingenious

The presence of meiosis, which is a conserved component of sexual reproduction, across organisms from all eukaryotic kingdoms, strongly argues that sex is a primordial feature of eukaryotes. However, extant meiotic structures and processes can vary considerably between organisms. The ciliated protist Tetrahymena thermophila, which diverged from animals, plants, and fungi early in evolution, provides one example of a rather unconventional meiosis. Tetrahymena has a simpler meiosis compared with most other organisms: It lacks both a synaptonemal complex (SC) and specialized meiotic machinery for chromosome cohesion and has a reduced capacity to regulate meiotic recombination. Despite this, it also features several unique mechanisms, including elongation of the nucleus to twice the cell length to promote homologous pairing and prevent recombination between sister chromatids. Comparison of the meiotic programs of Tetrahymena and higher multicellular organisms may reveal how extant meiosis evolved from proto-meiosis.     

Variation and evolution of meiosis

Meiosis arose in the evolution of primitive unicellular organisms as a part of sexual process. One type of meiosis, the so-called classical type, predominates in all kingdoms of eukaryotes. Meiosis is controlled by hundreds of genes, both shared with mitosis and specifically meiotic ones. In a wide range of taxa, which in some cases include kingdoms, meiotic genes and features obey Vavilov's law of homologous variation series. Synaptonemal complexes (SCs) temporarily binding homologous chromosomes at prophase I, ensure precise and equal crossing over and interference. SC proteins have 60-80% homology within the class of mammals but differ from the corresponding proteins in fungi and plants. Thus, nonhomologous SC proteins perform similar functions in different taxa. Some recombination enzymes in fungi and insects have common epitopes. The molecular mechanism of recombination is inherited by eukaryotes from prokaryotes and operates in special compartments: SC recombination nodules. Chiasmata, i.e., physical crossovers of nonsister chromatids, are preserved in bivalents until metaphase I due to local cohesion of sister chromatids in the remaining SC fragments. Owing to chiasmata, homologous chromosomes participate in meiosis I in pairs rather than individually, which, along with unipolarity of kinetochores (only in meiosis 1), ensures segregation of homologous chromosomes. The appearance of SC and chiasmata played a key role in the evolution of unicellular organisms since it promoted the development of a progressive type of meiosis. Some lower eukaryotes retain primitive meiosis types. These primitive modes of meiosis also occur in the sex of some insects that is heterozygous for sex chromosomes. I suggest an explanation for these cases. Mutations at meiotic genes impair meiosis; however, due to the preservation of archaic meiotic genes in the genotype, bypass metabolic pathways arise, which provide partial rescue of the traits damaged by mutations. Individual blocks of genetic program of meiotic regulation have probably evolved independently.     

Variation and Evolution of Meiosis

Meiosis arose in the evolution of primitive unicellular organisms as a part of sexual process. One type of meiosis, the so-called classical type, predominates in all kingdoms of eukaryotes. Meiosis is controlled by hundreds of genes, both shared with mitosis and specifically meiotic ones. In a wide range of taxa, which in some cases include kingdoms, meiotic genes and features obey Vavilov's law of homologous variation series. Synaptonemal complexes (SCs) temporarily binding homologous chromosomes at prophase I, ensure precise and equal crossing over and interference. SC proteins have 60–80% homology within the class of mammals but differ from the corresponding proteins in fungi and insects. Thus, nonhomologous SC proteins perform similar functions in different taxa. Some recombination enzymes in fungi and plants have common epitopes. The molecular mechanism of recombination is inherited by eukaryotes from prokaryotes and operates in special compartments: SC recombination nodules. Chiasmata, i.e., physical crossovers of nonsister chromatids, are preserved in bivalents until metaphase I due to local cohesion of sister chromatids in the remaining SC fragments. Owing to chiasmata, homologous chromosomes participate in meiosis I in pairs rather than individually, which, along with unipolarity of kinetochores (only in meiosis 1), ensures segregation of homologous chromosomes. The appearance of SC and chiasmata played a key role in the evolution of unicellular organisms since it promoted the development of a progressive type of meiosis. Some lower eukaryotes retain primitive meiosis types. These primitive modes of meiosis also occur in the sex of some insects that is heterozygous for sex chromosomes. I suggest an explanation for these cases. Mutations at meiotic genes impair meiosis; however, due to the preservation of archaic meiotic genes in the genotype, bypass metabolic pathways arise, which provide partial rescue of the traits damaged by mutations. Individual blocks of genetic program of meiotic regulation have probably evolved independently.     

Conserved Meiotic Genes Point to Sex in the Choanoflagellates

ABSTRACT. The choanoflagellates are a widespread group of heterotrophic aquatic nanoflagellates, which have recently been confirmed as the sister-group to Metazoa. Asexual reproduction is the only mode of cell division that has been observed within the group; at present the range of reproductive modes, as well as the ploidy level, within choanoflagellates are unknown. The recent discovery of long terminal repeat retrotransposons within the genome of Monosiga brevicollis suggests that this species also has sexual stages in its life cycle because asexual organisms cannot tolerate retrotransposons due to the rapid accumulation of deleterious mutations caused by their transposition. We screened the M. brevicollis genome for known eukaryotic meiotic genes, using a recently established "meiosis detection toolkit" of 19 genes. Eighteen of these genes were identified, none of which appears to be a pseudogene. Four of the genes were also identified in expressed sequence tag data from the distantly related Monosiga ovata . The presence of these meiosis-specific genes provides evidence for meiosis, and by implication sex, within this important group of protists.     

New‐age ideas about age‐old sex: separating meiosis from mating could solve a century‐old conundrum

Ever since Darwin first addressed it, sexual reproduction reigns as the ‘queen’ of evolutionary questions. Multiple theories tried to explain how this apparently costly and cumbersome method has become the universal mode of eukaryote reproduction. Most theories stress the adaptive advantages of sex by generating variation, they fail however to explain the ubiquitous persistence of sexual reproduction also where adaptation is not an issue. I argue that the obstacle for comprehending the role of sex stems from the conceptual entanglement of two distinct processes – gamete production by meiosis and gamete fusion by mating (mixis). Meiosis is an ancient, highly rigid and evolutionary conserved process identical and ubiquitous in all eukaryotes. Mating, by contrast, shows tremendous evolutionary variability even in closely related clades and exhibits wonderful ecological adaptability. To appreciate the respective roles of these two processes, which are normally linked and alternating, we require cases where one takes place without the other. Such cases are rather common. The heteromorphic sex chromosomes Y and W, that do not undergo meiotic recombination are an evolutionary test case for demonstrating the role of meiosis. Substantial recent genomic evidence highlights the accelerated rates of change and attrition these chromosomes undergo in comparison to those of recombining autosomes. I thus propose that the most basic role of meiosis is conserving integrity of the genome. A reciprocal case of meiosis without bi‐parental mating, is presented by self‐fertilization, which is fairly common in flowering plants, as well as most types of apomixis. I argue that deconstructing sex into these two distinct processes – meiosis and mating – will greatly facilitate their analysis and promote our understanding of sexual reproduction.     

Cryptic sex in fungi

It is generally accepted that genetic recombination in eukaryotes is mostly driven by meiotic divisions as part of the sexual cycle. The maintenance of the sexual cycle that combines beneficial genes in sexual offspring from two parents provides an advantage for a species in novel or changing environments. Sex thus preserves beneficial and removes deleterious mutations. However, some eukaryotes, including many fungi lack sex entirely, and thus, it was assumed that recombination occurring during mitotic (somatic) divisions is the main force to shape the genome of these asexually propagating microbes. However, several recent reports of a sexual cycle in asexually propagating fungi put this concept in question. Here, we summarize the accumulating evidence for the general occurrence of cryptic sex in filamentous fungi in which sexual reproduction has not been previously reported.     

Regulation of meiotic recombination and prophase I progression in mammals.

Meiosis is the process by which diploid germ cells divide to produce haploid gametes for sexual reproduction. The process is highly conserved in eukaryotes, however the recent availability of mouse models for meiotic recombination has revealed surprising regulatory differences between simple unicellular organisms and those with increasingly complex genomes. Moreover, in these higher eukaryotes, the intervention of physiological and sex-specific factors may also influence how meiotic recombination and progression are monitored and regulated. This review will focus on the recent studies involving mouse mutants for meiosis, and will highlight important differences between traditional model systems for meiosis (such as yeast) and those involving more complex cellular, physiological and genetic criteria.     

八种纤毛虫减数分裂基因的分子进化研究

减数分裂是真核生物适应性进化的重要机制,以8种纤毛虫作为实验对象,通过生物信息学方法对其14个减数分裂基因进行了鉴定及分子进化研究。结果表明:(1)不同的纤毛虫种类存在一些特异性的减数分裂基因的丢失与复制现象;(2)减数分裂相关基因在纤毛虫中很保守;(3)纤毛虫减数分裂重要的同源重组过程是在真核生物中不常见的Ⅱ型。本研究表明,纤毛虫减数分裂可能代表了真核生物较原始的减数分裂方式,在进化的过程中很保守,为研究真核生物减数分裂起源与进化提供了重要线索。     

An expanded inventory of conserved meiotic genes provides evidence for sex in Trichomonas vaginalis

Meiosis is a defining feature of eukaryotes but its phylogenetic distribution has not been broadly determined, especially among eukaryotic microorganisms (i.e. protists)-which represent the majority of eukaryotic 'supergroups'. We surveyed genomes of animals, fungi, plants and protists for meiotic genes, focusing on the evolutionarily divergent parasitic protist Trichomonas vaginalis. We identified homologs of 29 components of the meiotic recombination machinery, as well as the synaptonemal and meiotic sister chromatid cohesion complexes. T. vaginalis has orthologs of 27 of 29 meiotic genes, including eight of nine genes that encode meiosis-specific proteins in model organisms. Although meiosis has not been observed in T. vaginalis, our findings suggest it is either currently sexual or a recent asexual, consistent with observed, albeit unusual, sexual cycles in their distant parabasalid relatives, the hypermastigotes. T. vaginalis may use meiotic gene homologs to mediate homologous recombination and genetic exchange. Overall, this expanded inventory of meiotic genes forms a useful "meiosis detection toolkit". Our analyses indicate that these meiotic genes arose, or were already present, early in eukaryotic evolution; thus, the eukaryotic cenancestor contained most or all components of this set and was likely capable of performing meiotic recombination using near-universal meiotic machinery.     

Pathways to meiotic recombination in Arabidopsis thaliana

Meiosis is a central feature of sexual reproduction. Studies in plants have made and continue to make an important contribution to fundamental research aimed at the understanding of this complex process. Moreover, homologous recombination during meiosis provides the basis for plant breeders to create new varieties of crops. The increasing global demand for food, combined with the challenges from climate change, will require sustained efforts in crop improvement. An understanding of the factors that control meiotic recombination has the potential to make an important contribution to this challenge by providing the breeder with the means to make fuller use of the genetic variability that is available within crop species. Cytogenetic studies in plants have provided considerable insights into chromosome organization and behaviour during meiosis. More recently, studies, predominantly in Arabidopsis thaliana, are providing important insights into the genes and proteins that are required for crossover formation during plant meiosis. As a result, substantial progress in the understanding of the molecular mechanisms that underpin meiosis in plants has begun to emerge. This article summarizes current progress in the understanding of meiotic recombination and its control in Arabidopsis. We also assess the relationship between meiotic recombination in Arabidopsis and other eukaryotes, highlighting areas of close similarity and apparent differences.     

Nuclear architecture and chromosome dynamics in the search of the pairing partner in meiosis in plants

The formation of haploid gametes in organisms with sexual reproduction requires regular bivalent chromosome pairing in meiosis. In many species, homologous chromosomes occupy separate territories at the onset of meiosis. To be paired at metaphase I, they need to be brought into a close proximity for interactions that include homology recognition and the establishment of some form of bonds. How homologues find each other is one of the least understood meiotic events. Plant species with large or medium sized genomes, such as wheat or maize, are excellent materials for the cytological analysis of chromosome dynamics at early meiosis, but genes that control meiosis have been identified mainly in small genome species such as Arabidopsis thaliana. This review is focused on the contribution studies on plants are providing to the knowledge of the initial steps of the meiotic process.     

Adaptive Significance and Long-Term Survival of Asexual Lineages

Important questions remain about the long-term survival and adaptive significance of eukaryotic asexual lineages. Numerous papers dealing with sex advantages still continued to compare parthenogenetic populations versus sexual populations arguing that sex demonstrates a better fitness. Because asexual lineages do not possess any recombination mechanisms favoring rapid changes in the face of severe environmental conditions, they should be considered as an evolutionary dead-end. Nevertheless, reviewing literature dealing with asexual reproduction, it is possible to draw three stimulating conclusions. (1) Asexual reproduction in eukaryotes considerably differs from prokaryotes which experience recombination but neither meiosis nor syngamy. Recombination and meiosis would be a driving force for sexual reproduction. Eukaryotes should therefore be considered as a continuum of sexual organisms that are more or less capable (and sometimes incapable) of sexual reproduction. (2) Rather than revealing ancestral eukaryotic forms, most known lineages of asexual eukaryotes have lost sex due to a genomic conflict affecting their sexual capacity. Thus, it could be argued that hybridization is a major cause of their asexuality. Asexuality may have evolved as a reproductive mechanism reducing conflict within organisms. (3) It could be proposed that, rather than being generalists, parthenogenetic hybrid lineages could be favored when exploiting peculiar restricted ecological niches, following the “frozen niche variation” model. Although hybrid events may result in sex loss, probably caused by genomic conflict, asexual hybrids could display new original adaptive traits, and the rapid colonization of environments through clonal reproduction could favor their long-term survival, leading to evolutionary changes and hybrid speciation. Examination of the evolutionary history of asexual lineages reveals that evolutionary processes act through transitional stages in which even very small temporary benefits may be enough to counter the expected selective disadvantages.     

Genetic tests of ancient asexuality in Root Knot Nematodes reveal recent hybrid origins

Background  

The existence of "ancient asexuals", taxa that have persisted for long periods of evolutionary history without sexual recombination, is both controversial and important for our understanding of the evolution and maintenance of sexual reproduction. A lack of sex has consequences not only for the ecology of the asexual organism but also for its genome. Several genetic signatures are predicted from long-term asexual (apomictic) reproduction including (i) large "allelic" sequence divergence (ii) lack of phylogenetic clustering of "alleles" within morphological species and (iii) decay and loss of genes specific to meiosis and sexual reproduction. These genetic signatures can be hard to assess since it is difficult to demonstrate the allelic nature of very divergent sequences, divergence levels may be complicated by processes such as inter-specific hybridization, and genes may have secondary roles unrelated to sexual reproduction. Apomictic species of Meloidogyne root knot nematodes have been suggested previously to be ancient asexuals. Their relatives reproduce by meiotic parthenogenesis or facultative sexuality, which in combination with the abundance of nematode genomic sequence data, makes them a powerful system in which to study the consequences of reproductive mode on genomic divergence.     

Population genetics provides evidence for recombination in Giardia

Giardia lamblia (syn. Giardia intestinalis, Giardia duodenalis) is an enteric protozoan parasite with two nuclei, and it might be one of the earliest branching eukaryotes. However, the discovery of at least rudimentary forms of certain features, such as Golgi and mitochondria, has refuted the proposal that its emergence from the eukaryotic lineage predated the development of certain eukaryotic features. The recent recognition of many of the genes known to be required for meiosis in the genome has also cast doubt on the idea that Giardia is primitively asexual, but so far there has been no direct evidence of sexual reproduction in Giardia, and population data have suggested clonal reproduction. We did a multilocus sequence evaluation of the genotype A2 reference strain, JH, and five genotype A2 isolates from a highly endemic area in Peru. Loci from different chromosomes yielded significantly different phylogenetic trees, indicating that they do not share the same evolutionary history; within individual loci, tests for recombination yielded significant statistical support for meiotic recombination. These observations provide genetic data supportive of sexual reproduction in Giardia.