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Schematics of life cycles of algae and plants (1n = haploid chromosome number; 2n = diploid chromosome number). A: The simplest life cycles consists of an alternation between a unicellular haploid phase and a unicellular diploid phase (Chlamydomonas). B: The expression of multicellularity in the haploid phase (Chara) or C: in the diploid phase (Fucus) results in a haplobiontic life cycle. D: The expression of multicellularity in both phases results in a diplobiontic life cycle characteristic of the embryophytes (Marsilia). E: The diploid phase can have two phenotypes, for example, the life cycle of late-divergent red algae (Polysiphonia) (see B) (original drawings).
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Biologists have long theorized about the evolution of life cycles, meiosis, and sexual reproduction. We revisit these topics and propose that the fundamental difference between life cycles is where and when multicellularity is expressed. We develop a scenario to explain the evolutionary transition from the life cycle of a unicellular organism to on...
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... brown alga Laminaria), and still others are trimorphic (e.g. the red alga Polysiphonia). Yet, all of these variations are fundamentally the same. In addition to the capacity for asexual reproduction, each life cycle involves fusion of gametes (syngamy), meiosis, and an alternation between a haploid and a diploid unicellular or multicellular phase (Fig. 2), or their equivalent euploid levels in life cycles that normally involve endoduplication or that evolved as a result of auto-polyploidy. The primary difference among them lies in the duration of the haploid and diploid phase and in whether multicellularity is expressed in one or both of these ...
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... is generally held that the ancestral life cycle in each algal clade involved an alternation between a unicellular haploid cell and a diploid cell ( Fig. 2A), much like the life cycle of Chlamydomonas (Fig. 3A), and that either or both unicellular phases had the ability to replicate asexually by mitotic division [9-11, 14, 20-23]. This "default" life cycle presumably The diploid phase can have two phenotypes, for example, the life cycle of late-divergent red algae (Polysiphonia) (see Fig. ...
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... phenotypes (the carposporophyte and the tetrasporophyte). The carposporophyte develops from the zygote and resides on the female gametophyte. It produces diploid carpospores that develop into the free-living diploid multicellular tetrasporophyte that subsequently produces haploid spores that grow into free-living, isomorphic gametophytes (see Fig. 2E). A and B adapted from Raven et al. [24] (Figs. 15-41 and 15-35, ...
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... during the Precambrian and was subsequently evolutionarily modified by the intercalation of mitotic divisions in one or both phases. For example, the appearance of multicellularity in the haploid phase resulting from mitotic divisions after zygotic meiosis yielded the life cycle of the freshwater charophycean algae Chara and Coleochaete (Fig. 2B), whereas the evolution of multicellularity in the diploid phase resulting from mitotic divisions before gametic meiosis produced the life cycle of the marine alga Fucus (Fig. 2C), and, by convergent evolution, typical metazoans such as mammals (Fig. 1A). Finally, the appearance of multicellularity in both the haploid and the diploid ...
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... in the haploid phase resulting from mitotic divisions after zygotic meiosis yielded the life cycle of the freshwater charophycean algae Chara and Coleochaete (Fig. 2B), whereas the evolution of multicellularity in the diploid phase resulting from mitotic divisions before gametic meiosis produced the life cycle of the marine alga Fucus (Fig. 2C), and, by convergent evolution, typical metazoans such as mammals (Fig. 1A). Finally, the appearance of multicellularity in both the haploid and the diploid phase by means of delayed zygotic meiosis and sporic meiosis independently resulted in the life cycle of the green marine alga Ulva and the land plants (Fig. 2D). Variants of these ...
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... cycle of the marine alga Fucus (Fig. 2C), and, by convergent evolution, typical metazoans such as mammals (Fig. 1A). Finally, the appearance of multicellularity in both the haploid and the diploid phase by means of delayed zygotic meiosis and sporic meiosis independently resulted in the life cycle of the green marine alga Ulva and the land plants (Fig. 2D). Variants of these three basic life cycles certainly exist. For example, the life cycles of some red algae, such as Polysiphonia, contain more than one diploid multicellular organism ( Fig. 3B) and can involve curious and striking intra- organismic differences in the number of nuclei per cell and ploidy levels [25,26]. The ...
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... [27]. Inspection of the presumably ancestral eukaryotic life cycle ( Fig. 2A) shows that two unicellular "adults" must take on the function of gametes, and thus are consumed in each cycle of sexual reproduction via syngamy, i.e. each cycle results in a net gain of only two individuals. In contrast, a haploid multicellular organism consisting of only two cells, one of which functions as a gamete, will quickly ...
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... to the diversity of life cycles in the algae and land plants, we see that meiosis and syngamy occur in every variant (see Fig. 2). Yet, no model for the evolution of meiosis has been proposed without being criticized, sometimes even by its creators. For example, Maynard Smith [4] proposed perhaps the best known scenario for the evolution of meiosis and sexual reproduction in which two haploid cells fuse to produce a diploid heterokaryon with separate spindles ...
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... cycles that have an alternation between a multicellular haploid and a multicellular diploid generation (see Fig. 2D) occur in the brown algae, the green algae, and the land plants. In each case, these life cycles are posited to have evolved from a life cycle similar to that of Chlamydomonas (see Figs. 2A and 3A). Comparative phenotypic and molecular studies also indicate that multicellularity most likely appeared first in the haploid generation (see ...
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... cycles that have an alternation between a multicellular haploid and a multicellular diploid generation (see Fig. 2D) occur in the brown algae, the green algae, and the land plants. In each case, these life cycles are posited to have evolved from a life cycle similar to that of Chlamydomonas (see Figs. 2A and 3A). Comparative phenotypic and molecular studies also indicate that multicellularity most likely appeared first in the haploid generation (see Fig. 2B) and subsequently in the diploid generation within each of these three lineages [3,12,14,22,35,[55][56][57][58]. This parallel sequence of events raises a simple question: why did ...
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... Fig. 2D) occur in the brown algae, the green algae, and the land plants. In each case, these life cycles are posited to have evolved from a life cycle similar to that of Chlamydomonas (see Figs. 2A and 3A). Comparative phenotypic and molecular studies also indicate that multicellularity most likely appeared first in the haploid generation (see Fig. 2B) and subsequently in the diploid generation within each of these three lineages [3,12,14,22,35,[55][56][57][58]. This parallel sequence of events raises a simple question: why did multicellularity evolve in the haploid phase first and in the diploid phase ...
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The doubled haploid lines (DHL) of maize in their top crosses are expected to include genotypes that accumulated favorable genes for both high-yielding and drought tolerance. The objectives of this study were: (i) to screen 254 DHL's x tester crosses for tolerance to water stress at flowering (WSF) and grain filling (WSG), (ii) to estimate the supe...
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... Les organismes multicellulaires sont apparus à de multiples reprises au cours de l'évolution des eucaryotes (Niklas and Newman 2013; et l'association avec la reproduction sexuée a permis de faire des organismes multicellulaires à reproduction sexuée les plus diversifiés (Niklas et al. 2014;Speijer et al. 2015;Chen and Wiens 2021). La reproduction sexuée nécessite un cycle cellulaire spécialisé, qui peut être associé à une différenciation extrême de la cellule lors de la méiose. ...
La régulation fine de la traduction pour la dynamique du cycle cellulaire est un sujet important dans la recherche cellulaire. Au cours de ma thèse, j'ai analysé les relations entre l’activité traductionnelle des ARNm et les divisions embryonnaires mitotiques d'oursins. La fécondation de l'œuf déclenche l'activation de la machinerie traductionnelle nécessaire à la reprise des divisions mitotiques. Un réseau de régulation traductionnelle (TlRN), indépendant de la transcription, reste à identifier et à caractériser en amont des acteurs du cycle cellulaire. A la recherche d'activités mitotiques pour visualiser la dynamique spatiale à l'intérieur d'œufs, j'ai obtenu des données originales montrant l'activité dynamique et spatiale du complexe mitotique CyclinB/CDK1 et la phosphorylation de l'histone H3 sur la thréonine 3 (pH3T3) pendant la mitose embryonnaire. Ensuite, j'ai analysé le rôle in vivo de 5'UTR spécifiques pour contrôler le recrutement d'ARNm dans les polysomes actifs après la fécondation. Enfin, j'ai montré que la traduction de l'ARNm codant pour eIF4B (facteur d'initiation eucaryote 4B) contrôle l'activité traductionnelle et la dynamique des deux premières divisions mitotiques induites par la fécondation. Je propose qu'eIF4B agisse comme un régulateur positif au sein du TlRN. Ces données permettront d'étudier l'effet potentiel d'eIF4B sur les activités CDK1 et pH3T3.
... In contrast, asymmetric CHH methylation is deposited by Domains Rearranged Methyltransferase 2 (DRM2) through RNA-directed DNA methylation (RdDM) and by CMT2 (Matzke et al. 2009;Zemach et al. 2013). A feedback loop mechanism is required where CMT2 and CMT3 recognize H3K9me2 to methylate neighboring CHH and CHG sites while the H3K9 methyltransferase KRYP-TONITE (KYP) recognizes methylated cytosines, further reinforcing the transcriptional silencing of heterochromatin (Wilkins and Holliday 2009;Du et al. 2014;Niklas et al. 2014;Lenormand et al. 2016). In the yeast Cryptococcus neoformans, CG methylation is propagated by the maintenance methyltransferase DNMT5 in the absence of a de novo methyltransferase and also involves an H3K9 methylation loop (Catania et al. 2020). ...
Plants and algae have a complex life history that transitions between distinct life forms called the sporophyte and the gametophyte. This phenomenon-called the alternation of generations-has fascinated botanists and phycologists for over 170 years. Despite the mesmerizing array of life histories described in plants and algae, we are only now beginning to learn about the molecular mechanisms controlling them and how they evolved. Epigenetic silencing plays an essential role in regulating gene expression during multicellular development in eukaryotes, raising questions about its impact on the life history strategy of plants and algae. Here, we trace the origin and function of epigenetic mechanisms across the plant kingdom, from unicellular green algae through to angiosperms, and attempt to reconstruct the evolutionary steps that influenced life history transitions during plant evolution. Central to this evolutionary scenario is the adaption of epigenetic silencing from a mechanism of genome defense to the repression and control of alternating generations. We extend our discussion beyond the green lineage and highlight the peculiar case of the brown algae. Unlike their unicellular diatom relatives, brown algae lack epigenetic silencing pathways common to animals and plants yet display complex life histories, hinting at the emergence of novel life history controls during stramenopile evolution.
... The discovery that land plant species have an alternation of generations life cycle profoundly changed how we view these plant species, as pointed out by Niklas et al. (2014) and by Friedman (2015). Before this discovery was made, the assumption was that land plant species had a life cycle with just one stage in it with adults (i.e., haplobiontic), suggesting that the study of the adults at that one stage might tell us all about any reproductive or sexual features found in a given land plant species. ...
The two-sex model makes the assumption that there are only two sexual reproductive states: male and female. However, in land plants (embryophytes) the application of this model to the alternation of generations life cycle requires the subtle redefinition of several common terms related to sexual reproduction, which seems to obscure aspects of one or the other plant generation: For instance, the homosporous sporophytic plant is treated as being asexual, and the gametophytes of angiosperms treated like mere gametes. In contrast, the proposal is made that the sporophytes of homosporous plants are indeed sexual reproductive organisms, as are the gametophytes of heterosporous plants. This view requires the expansion of the number of sexual reproductive states we accept for these plant species; therefore, a three-sex model for homosporous plants and a four-sex model for heterosporous plants are described and then contrasted with the current two-sex model. These new models allow the use of sexual reproductive terms in a manner largely similar to that seen in animals, and may better accommodate the plant alternation of generations life cycle than does the current plant two-sex model. These new models may also help stimulate new lines of research, and examples of how they might alter our view of events in the flower, and may lead to new questions about sexual determination and differentiation, are presented. Thus it is suggested that land plant species have more than merely two sexual reproductive states and that recognition of this may promote our study and understanding of them.
... A more in-depth treatment of the evolutionary conservation of gamete cell fate commitment and mating is available in previous publications [37,44,[49][50][51][52][53]. Using these sources, a list of broadly conserved protein families known to be involved in sexual reproduction were compiled (S4 Data) to be used as HOG queries to the LSH Forest to retrieve the top 10 closest coevolving HOGs. ...
Phylogenetic profiling is a computational method to predict genes involved in the same biological process by identifying protein families which tend to be jointly lost or retained across the tree of life. Phylogenetic profiling has customarily been more widely used with prokaryotes than eukaryotes, because the method is thought to require many diverse genomes. There are now many eukaryotic genomes available, but these are considerably larger, and typical phylogenetic profiling methods require at least quadratic time as a function of the number of genes. We introduce a fast, scalable phylogenetic profiling approach entitled HogProf, which leverages hierarchical orthologous groups for the construction of large profiles and locality-sensitive hashing for efficient retrieval of similar profiles. We show that the approach outperforms Enhanced Phylogenetic Tree, a phylogeny-based method, and use the tool to reconstruct networks and query for interactors of the kinetochore complex as well as conserved proteins involved in sexual reproduction: Hap2, Spo11 and Gex1. HogProf enables large-scale phylogenetic profiling across the three domains of life, and will be useful to predict biological pathways among the hundreds of thousands of eukaryotic species that will become available in the coming few years. HogProf is available at https://github.com/DessimozLab/HogProf.
... Unlike Arabidopsis and Oryza sativa, our understanding of algal meiosis is still limited [62], making difficult to interpret the conservation and divergence of PHD domain between algae and higher plants. One possibility is that, algal meiosis is mechanistically more similar to the processes in ancestral species in which meiosis first evolved and may not need the replacement of mitosis-specific cohesin by a meiosis-specific one [63]. We also cannot exclude the possibility that SCC2-PHD domain functions diverge among plant taxa. ...
Cohesin, a multisubunit protein complex, is required for holding sister chromatids together during mitosis and meiosis. The recruitment of cohesin by the sister chromatid cohesion 2/4 (SCC2/4) complex has been extensively studied in Saccharomyces cerevisiae mitosis, but its role in mitosis and meiosis remains poorly understood in multicellular organisms, because complete loss-of-function of either gene causes embryonic lethality. Here, we identified a weak allele of Atscc2 (Atscc2-5) that has only minor defects in vegetative development but exhibits a significant reduction in fertility. Cytological analyses of Atscc2-5 reveal multiple meiotic phenotypes including defects in chromosomal axis formation, meiosis-specific cohesin loading, homolog pairing and synapsis, and AtSPO11-1-dependent double strand break repair. Surprisingly, even though AtSCC2 interacts with AtSCC4 in vitro and in vivo, meiosis-specific knockdown of AtSCC4 expression does not cause any meiotic defect, suggesting that the SCC2-SCC4 complex has divergent roles in mitosis and meiosis. SCC2 homologs from land plants have a unique plant homeodomain (PHD) motif not found in other species. We show that the AtSCC2 PHD domain can bind to the N terminus of histones and is required for meiosis but not mitosis. Taken together, our results provide evidence that unlike SCC2 in other organisms, SCC2 requires a functional PHD domain during meiosis in land plants.
... A more indepth treatment of the evolutionary conservation of gamete cell fate commitment and mating is available in previous publications [32,41,[46][47][48][49][50] . Using these sources, a list of broadly conserved protein families known to be involved in sexual reproduction were compiled to be used as HOG queries to the LSH Forest to ret rieve the top 10 closest coevolving HOGs . ...
Phylogenetic profiling is a computational method to predict genes involved in the same biological process by identifying protein families which tend to be jointly lost or retained across the tree of life. Phylogenetic profiling has customarily been more widely used with prokaryotes than eukaryotes, because the method is thought to require many diverse genomes. There are now many eukaryotic genomes available, but these are considerably larger, and typical phylogenetic profiling methods require quadratic time or worse in the number of genes. We introduce a fast, scalable phylogenetic profiling approach entitled HogProf, which leverages hierarchical orthologous groups for the construction of large profiles and locality-sensitive hashing for efficient retrieval of similar profiles. We show that the approach outperforms Enhanced Phylogenetic Tree, a phylogeny-based method, and use the tool to reconstruct networks and query for interactors of the kinetochore complex as well as conserved proteins involved in sexual reproduction: Hap2, Spo11 and Gex1. HogProf enables large-scale phylogenetic profiling across the three domains of life, and will be useful to predict biological pathways among the hundreds of thousands of eukaryotic species that will become available in the coming few years. HogProf is available at https://github.com/DessimozLab/HogProf .
... Interestingly, a hypothesis posited by Niklas and colleagues [68] argues that meiosis evolved before sexual reproduction as a method for rectifying spontaneous whole genome duplication (aneuploidy). If still in effect, this mechanism could also explain the presence of genes for recombination and repair. ...
Background: Chrysochromulina (Haptophyta) species are recognized as seminal contributors to marine and freshwater ecosystem function. Historically, scale vestiture is used to augment taxonomic identification of these algae, and a large literature exists concerning the morphology of many scale-covered representatives. Scale-less freshwater isolates present a new challenge. Details concerning the microanatomy of naked cells remain essentially unreported. Insight into morphological similarities/differences between scaled and naked cells provides information on the evolution of the taxon, especially as discussions defining cryptic species complexes become more germane. Using light, scanning, and transmission microscopy, we present an analysis of the cellular structure for three Chrysochromulina freshwater isolates. Results: Chrysochromulina tobinii Cattolico, Chrysochromulina parva Lackey and Chrysochromulina AND cells are approximately 5 μm wide, saddle-shaped to globose, and devoid of scales. A lipid body is nestled close to each of two chloroplasts and numerous mitochondria. Plastoglobuli are frequently associated with thylakoidal membranes that encircle an internal pyrenoid. The Golgi apparatus has large, club-shaped cisternae. The haptonema consists of 9 microtubules within the cytoplasm, but 6 or 7 microtubules in the external portion. A rootlet system anchors the two flagella that are sub-apically inserted adjacent to the haptonema. The flagellar complex is anchored in the cytoplasm by a flat ribbon of microtubules and microtubular rootlets associated with each basal body. Fibrous rootlets, several of which are cross-banded, interconnect the two flagellar basal bodies and haptonema. Conclusion: Three freshwater, scale-less Chrysochromulina isolates are almost indistinguishable in ultrastructure, even though extensive genome sequencing studies verify their distinctiveness. These freshwater representatives certainly comprise members of a cryptic species complex. Extensive morphological similarity also occurs between freshwater and scaled marine isolates. Importantly, this report addresses the misidentification of Chrysochromulina tobinii Cattolico as Chrysochromulina parva Lackey and clarifies a complex literature regarding the morphological description of the type species for this algal clade.
... As a result, the topic of "sex-research in algae and plants" evolved over subsequent decades. 12,14 Today it is well established that only ca. 5% of all angiosperms are dioecious and their reproductive roles are completely separated, whereas ca. 95% are monoecious ("hermaphrodites"). ...
One hundred and fifty years ago, Julius von Sachs’ (1832–1897) monumental Lehrbuch der Botanik (Textbook of Botany) was published, which signified the origin of physiological botany and its integration with evolutionary biology. Sachs regarded the physiology of photoautotrophic organisms as a sub-discipline of botany, and introduced a Darwinian perspective into the emerging plant sciences. Here, we summarize Sachs’ achievements and his description of sexuality with respect to the cellular basis of plant and animal biparental reproduction. We reproduce and analyze a forgotten paper (Gutachten) of Sachs dealing with Die Akademische Frau (The Academic Woman), published during the year of his death on the question concerning gender equality in humans. Finally, we summarize his endorsement of woman’s rights to pursue academic studies in the natural sciences at the University level, and conclude that Sachs was a humanist as well as a great scientist.
... Taken at face value, this bottleneck in metazoan embryological patterning provides evidence for the evolution of an early and successful strategy for achieving the basic metazoan body plan. However, as we have shown recently, this principle cannot be extended to land plants, a monophyletic lineage characterized by taxon-specific alterations in gametophyte/ sporophyte-generations (Niklas et al. 2014. ...
... Currently, plant Evo-Devo is at a similar stage as classical genetics was before the Modern Synthesis was achieved by Theodosius Dobzhansky , Ernst Mayr (1904Mayr ( -2005, and others. During the 1940s, it was difficult to reconcile Mendelian quantitative genetics with the Darwinian supposition that evolution involves gradualistic genomic changes (Mayr 1982;Niklas 1997Niklas , 2016Niklas 2004, 2005). The rapidly expanding information gained from genomics and proteomics has not been fully integrated with that provided by the more traditional physiological, developmental, or evolutionary disciplines. ...
In 1790, the German poet Johann W. v. Goethe (1749–1832) proposed the concept of a hypothetical sessile organism known as the ‘Plant Archetype,’ which was subsequently reconstructed and depicted by 19th-century botanists, such as Franz Unger (1800–1870) and Julius Sachs (1832–1897), and can be considered one of the first expressions of Evo-Devo thinking. Here, we present the history of this concept in the context of Ernst Haeckel’s (1834–1919) biogenetic law espoused in his Generelle Morphologie der Organismen of 1866. We show that Haeckel’s idea of biological recapitulation may help to explain why various phenomena, such as the ontogenetic transformations in the stellar anatomy of lycopods and ferns, the transition from primary to secondary anatomy of seed plants, the presence of unfused juvenile cone scale segments in the Japanese cedar (Cryptomeria japonica), and the transition of C3- to C4-photosynthesis in the ontogeny of maize (Zea mays), appear to support his theories. In addition, we outline the current status of plant evolutionary developmental biology (Evo-Devo), which can be traced back to Haeckel's (1866) biogenetic law, with a focus on the model plant thale cress (Arabidopsis thaliana).
... However, unlike bisexual reproduction, unisexual reproduction can proceed either through cell-cell fusion or endoreplication, and the latter is likely the major route for ploidy increase [3,9,16]. Increase in ploidy by endoduplication often occurs as a response to stress in eukaryotes [64][65][66], and sexual reproduction in many fungi, including Cryptococcus, takes place under stressful conditions. After increased ploidy through endoduplication, Cryptococcus could complete sexual reproduction by meiosis to return to the haploid state. ...
The fungus Cryptococcus neoformans can undergo a-α bisexual and unisexual reproduction. Completion of both sexual reproduction modes requires similar cellular differentiation processes and meiosis. Although bisexual reproduction generates equal number of a and α progeny and is far more efficient than unisexual reproduction under mating-inducing laboratory conditions, the α mating type dominates in nature. Population genetic studies suggest that unisexual reproduction by α isolates might have contributed to this sharply skewed distribution of the mating types. However, the predominance of the α mating type and the seemingly inefficient unisexual reproduction observed under laboratory conditions present a conundrum. Here, we discovered a previously unrecognized condition that promotes unisexual reproduction while suppressing bisexual reproduction. Pheromone is the principal stimulus for bisexual development in Cryptococcus. Interestingly, pheromone and other components of the pheromone pathway, including the key transcription factor Mat2, are not necessary but rather inhibitory for Cryptococcus to complete its unisexual cycle under this condition. The inactivation of the pheromone pathway promotes unisexual reproduction despite the essential role of this pathway in non-self-recognition during bisexual reproduction. Nonetheless, the requirement for the known filamentation regulator Znf2 and the expression of hyphal or basidium specific proteins remain the same for pheromone-dependent or independent sexual reproduction. Transcriptome analyses and an insertional mutagenesis screen in mat2Δ identified calcineurin being essential for this process. We further found that Znf2 and calcineurin work cooperatively in controlling unisexual development in this fungus. These findings indicate that Mat2 acts as a repressor of pheromone-independent unisexual development while serving as an activator for a-α bisexual development. The bi-functionality of Mat2 might have allowed it to act as a toggle switch for the mode of sexual development in this ubiquitous eukaryotic microbe.
