Sex, amitosis, and evolvability in the ciliate Tetrahymena thermophila

Understanding the mechanisms that generate genetic variation, and thus contribute to the process of adaptation, is a major goal of evolutionary biology. Mutation and genetic exchange have been well studied as mechanisms to generate genetic variation. However, there are additional processes that may also generate substantial genetic variation in some populations and the extent to which these variation generating mechanisms are themselves shaped by natural selection is still an open question. Tetrahymena thermophila is a ciliate with an unusual mechanism of nuclear division, called amitosis, which can generate genetic variation among the asexual descendants of a newly produced sexual progeny. We hypothesize that amitosis thus increases the evolvability of newly produced sexual progeny relative to species that undergo mitosis. To test this hypothesis, we used experimental evolution and simulations to compare the rate of adaptation in T. thermophila populations founded by a single sexual progeny to parental populations that had not had sex in many generations. The populations founded by a sexual progeny adapted more quickly than parental populations in both laboratory populations and simulated populations. This suggests that the additional genetic variation generated by amitosis of a heterozygote can increase the rate of adaptation following sex and may help explain the evolutionary success of the unusual genetic architecture of Tetrahymena and ciliates more generally.

Genetic diversity among asexual and sexual progenies of Phytophthora capsici detected with ISSR markers

The population structure of Phytophthora capsici among asexual and sexual progenies was analyzed using ISSR. Thirty asexual progenies of one parent and three sexual populations were assayed for genetic diversity using 5 ISSR primers and DNA from 120 offspring of P. capsici was amplified. In total, 71 reproducible ISSR fragments were obtained, of which 100% were polymorphic, revealing high polymorphism among the isolates. Among them, the percentages of polymorphism of sexual and asexual progeny isolates were 100.00 and 77.46%, respectively. Genetic similarity coefficients among all the isolates ranged from 0.54 to 0.73. The sexual offspring population showed much more variability than the asexual offspring population with 76.26% variability attributed to diversity within populations as compared with 23.74% among populations. This research reveals that the sexual progeny population of P. capsici contributes more genetic diversity than that of asexual progeny population.

Unique patterns of mating pheromone presence and absence could result in the ambiguous sexual behaviours of Colletotrichum species

Colletotrichum species are known to engage in unique sexual behaviours that differ significantly from the mating strategies of other filamentous ascomycete species. For example, most ascomycete fungi require the expression of both the MAT1-1-1 and MAT1-2-1 genes to induce sexual reproduction. In contrast, all isolates of Colletotrichum harbour only the MAT1-2-1 gene and yet, are capable of recognizing suitable mating partners and producing sexual progeny. The molecular mechanisms contributing to mating types and behaviours in Colletotrichum are, however, unknown. A comparative genomics approach analysing 35 genomes, representing 31 Colletotrichum species and two Verticillium species, was used to elucidate a putative molecular mechanism underlying the unique sexual behaviours observed in Colletotrichum species. The existence of only the MAT1-2 idiomorph was confirmed across all species included in this study. Comparisons of the loci harbouring the two mating pheromones and their cognate receptors revealed interesting patterns of gene presence and absence. The results showed that these genes have been lost multiple, independent times over the evolutionary history of this genus. These losses indicate that the pheromone pathway no longer plays an active role in mating type determination, suggesting an undiscovered mechanism by which mating partner recognition is controlled in these species. This further suggests that there has been a redirection of the underlying genetic mechanisms that regulate sexual development in Colletotrichum species. This research thus provides a foundation from which further interrogation of this topic can take place.

Unique Patterns of Mating Pheromone Presence and Absence could Result in the Ambiguous Sexual Behaviours of Colletotrichum Species

Background: Colletotrichum species are known to engage in unique sexual behaviours that differ significantly from the mating strategies of other filamentous ascomycete species. Most ascomycete fungi require the expression of both the MAT1-1-1 and MAT1-2-1 genes to regulate mating type and induce sexual reproduction. In contrast, all isolates of Colletotrichum are known to harbour only the MAT1-2-1 gene and yet, are capable of recognizing suitable mating partners and producing sexual progeny. The molecular mechanisms contributing to mating types and behaviours in Colletotrichum are thus unknown. Results: A comparative genomics approach analysing genomes from 47 Colletotrichum isolates was used to elucidate a putative molecular mechanism underlying the unique sexual behaviours observed in Colletotrichum species. The existence of only the MAT1-2 idiomorph was confirmed across all species included in this study. Comparisons at the loci harbouring the two mating pheromones and their cognate receptors revealed interesting patterns of gene presence and absence as well as gene loss. The results also showed that these genes have been lost multiple times over the evolutionary history of this genus. Conclusion: The multiple losses of the pheromone genes in these species suggest strong selection against the typical mating strategies seen in other species. This further suggests that these pheromones no longer play a role in mating type determination and that the species of this genus have undiscovered mechanisms by which to control mating type and mating partner recognition. This research thus provides a base from which further interrogation of this topic can take place.

Triparental inheritance inDictyostelium

Sex promotes the recombination and reassortment of genetic material and is prevalent across eukaryotes, although our knowledge of the molecular details of sexual inheritance is scant in several major lineages. In social amoebae, sex involves a promiscuous mixing of cytoplasm before zygotes consume the majority of cells, but for technical reasons, sexual progeny have been difficult to obtain and study. We report here genome-wide characterization of meiotic progeny inDictyostelium discoideum. We find that recombination occurs at high frequency in pairwise crosses between all three mating types, despite the absence of the Spo11 enzyme that is normally required to initiate crossover formation. Fusions of more than two gametes to form transient syncytia lead to frequent triparental inheritance, with haploid meiotic progeny bearing recombined nuclear haplotypes from two parents and the mitochondrial genome from a third. Cells that do not contribute genetically to theDictyosteliumzygote nucleus thereby have a stake in the next haploid generation.D. discoideummitochondrial genomes are polymorphic, and our findings raise the possibility that some of this variation might be a result of sexual selection on genes that can promote the spread of individual organelle genomes during sex. This kind of self-interested mitochondrial behavior may have had important consequences during eukaryogenesis and the initial evolution of sex.

RNA interference in formation of the somatic genome of ciliates Paramecium and Tetrahymena

Ciliates are the model of choice to study RNA interference, the mechanism playing key role in biology of these protists. The genome scanning processes of two ciliates, Tetrahymena and Paramecium (Oligohymenophorea), leading to formation of the somatic genome from the chromosomes of the generative nucleus are compared in the review. Matching of several simulta neously present in one cell genomes is mediated by small RNAs and results in precise reproduction of maternal somatic genome in the sexual progeny.

Successful asexual lineages of the Irish potato Famine pathogen are triploid

The oomycetePhytophthora infestanswas the causal agent of the Irish Great Famine and is a recurring threat to global food security. The pathogen can reproduce both sexually and asexually and has a potential to adapt both abiotic and biotic environment. Although in many regions the A1 and A2 mating types coexist, the far majority of isolates belong to few clonal, asexual lineages. As other oomycetes,P. infestansis thought to be diploid during the vegetative phase of its life cycle, but it was observed that trisomy correlated with virulence and mating type locus and that polyploidy can occur in some isolates. It remains unknown about the frequency of polyploidy occurrence in nature and the relationship between ploidy level and sexuality. Here we discovered that the sexuality ofP. infestansisolates correlates with ploidy by comparison of microsatellite fingerprinting, genome-wide polymorphism, DNA quantity, and chromosome numbers. The sexual progeny ofP. infestansin nature are diploid, whereas the asexual lineages are mostly triploids, including successful clonal lineages US-1 and 13_A2. This study reveals polyploidization as an extra evolutionary risk to this notorious plant destroyer.

Genome Sequencing and Mapping Reveal Loss of Heterozygosity as a Mechanism for Rapid Adaptation in the Vegetable Pathogen Phytophthora capsici

The oomycete vegetable pathogen Phytophthora capsici has shown remarkable adaptation to fungicides and new hosts. Like other members of this destructive genus, P. capsici has an explosive epidemiology, rapidly producing massive numbers of asexual spores on infected hosts. In addition, P. capsici can remain dormant for years as sexually recombined oospores, making it difficult to produce crops at infested sites, and allowing outcrossing populations to maintain significant genetic variation. Genome sequencing, development of a high-density genetic map, and integrative genomic or genetic characterization of P. capsici field isolates and intercross progeny revealed significant mitotic loss of heterozygosity (LOH) in diverse isolates. LOH was detected in clonally propagated field isolates and sexual progeny, cumulatively affecting >30% of the genome. LOH altered genotypes for more than 11,000 single-nucleotide variant sites and showed a strong association with changes in mating type and pathogenicity. Overall, it appears that LOH may provide a rapid mechanism for fixing alleles and may be an important component of adaptability for P. capsici.