scholarly journals Evolution of Mating Types Driven by Purifying Selection against Mitochondrial Mutations

2016 ◽  
Author(s):  
Arunas L Radzvilavicius
Keyword(s):  
Cell Fusion ◽  
Mating Type ◽  
Genetic Material ◽  
Purifying Selection ◽  
Uniparental Inheritance ◽  
Mating Types ◽  
Mitochondrial Mutations ◽  
Mating Partner ◽  
Asymmetric Transmission ◽  
Mitochondrial Mutation

AbstractSexual cell fusion combines genetic material of two gametes, but why the two reproductive cells have to belong to distinct self-incompatible gamete classes is not known. In a vast majority of sexual eukaryotes, mitochondria are inherited uniparentally from only one of the two mating types, which is thought to facilitate purifying selection against deleterious mitochondrial mutations and limit the inter-genomic conflicts. Here I argue that two mating types in eukaryotes represent a mechanism of mitochondrial quality control through the highly asymmetric transmission of mitochondrial genes at cell fusion. I develop a mathematical model to explicitly study the evolution of two self-incompatible mating type alleles linked to the nuclear locus controlling the pattern of organelle inheritance. The invasion of mating-type alleles is opposed by the short-term fitness benefit of mitochondrial mixing under negative epistasis and the lower chance of encountering a compatible mating partner. Nevertheless, under high mitochondrial mutation rates purifying selection against defective mitochondria can drive two mating types with uniparental inheritance to fixation. The invasion is further facilitated by the paternal leakage of mitochondria under paternal control of cytoplasmic inheritance. In contrast to previous studies, the model does not rely on the presence of selfish cytoplasmic elements, providing a more universal solution to the longstanding evolutionary puzzle of two sexes.

The origin of multiple mating types in mushrooms

1993 ◽  
Vol 104 (2) ◽  
pp. 227-230
Author(s):  
U. Kues ◽  
L.A. Casselton
Keyword(s):  
Mating Type ◽  
Multiple Mating ◽  
Mating Types ◽  
Mating Partner ◽  
Binucleate Cells ◽  
Large Numbers ◽  
Mating Type Genes ◽  
And Function ◽  
Developmental Switch ◽  
Sterile Mycelium

Having multiple mating types greatly improves the chances of meeting a compatible mating partner, particularly in an organism like the mushroom that has no sexual differentiation and no mechanism for signalling to a likely mate. Having several thousands of mating types, as some mushrooms do, is, however, remarkable - and even more remarkable is the fact that individuals only recognise that they have met a compatible mate after their cells have fused. How are such large numbers of mating types generated and what is the nature of the intracellular interaction that distinguishes self from non- self? Answers to these fascinating questions come from cloning some of the mating type genes of the ink cap mushroom Coprinus cinereus. A successful mating in Coprinus triggers a major switch in cell type, the conversion of a sterile mycelium with uninucleate cells (monokaryon) to a fertile mycelium with binucleate cells (dikaryon) which differentiates the characteristic fruit bodies. The mating type genes that regulate this developmental switch map to two multiallelic loci designated A and B and these must both carry different alleles for full mating compatibility. A and B independently regulate different steps in the developmental switch, making it possible to study just one component of the system and work in our laboratory has concentrated on understanding the structure and function of the A genes. It is estimated that some 160 different A mating types exist in nature, any two of which can together trigger the A-regulated part of sexual development. The first clue to how such large numbers are generated came from classical genetic analysis, which identified two functionally redundant A loci, (alpha) and beta. Functional redundancy is, indeed, the key to multiple A mating types and, as seen in Fig.1, molecular cloning has identified many more genes than was possible by recombination analysis.

scholarly journals Dynamics of mitochondrial inheritance in the evolution of binary mating types and two sexes

2013 ◽  
Vol 280 (1769) ◽  
pp. 20131920 ◽  
Author(s):  
Zena Hadjivasiliou ◽  
Nick Lane ◽  
Robert M. Seymour ◽  
Andrew Pomiankowski
Keyword(s):  
Relative Fitness ◽  
Uniparental Inheritance ◽  
Dependent Manner ◽  
Mating Types ◽  
Mitochondrial Mutation ◽  
Unicellular Eukaryotes ◽  
Fitness Advantage ◽  
Mitochondrial Population ◽  
Fitness Benefits

The uniparental inheritance (UPI) of mitochondria is thought to explain the evolution of two mating types or even true sexes with anisogametes. However, the exact role of UPI is not clearly understood. Here, we develop a new model, which considers the spread of UPI mutants within a biparental inheritance (BPI) population. Our model explicitly considers mitochondrial mutation and selection in parallel with the spread of UPI mutants and self-incompatible mating types. In line with earlier work, we find that UPI improves fitness under mitochondrial mutation accumulation, selfish conflict and mitonuclear coadaptation. However, we find that as UPI increases in the population its relative fitness advantage diminishes in a frequency-dependent manner. The fitness benefits of UPI ‘leak’ into the biparentally reproducing part of the population through successive matings, limiting the spread of UPI. Critically, while this process favours some degree of UPI, it neither leads to the establishment of linked mating types nor the collapse of multiple mating types to two. Only when two mating types exist beforehand can associated UPI mutants spread to fixation under the pressure of high mitochondrial mutation rate, large mitochondrial population size and selfish mutants. Variation in these parameters could account for the range of UPI actually observed in nature, from strict UPI in some Chlamydomonas species to BPI in yeast. We conclude that UPI of mitochondria alone is unlikely to have driven the evolution of two mating types in unicellular eukaryotes.

scholarly journals Uniparental sexual reproduction following cell-cell fusion of opposite mating-type partners

2020 ◽  
Author(s):  
Vikas Yadav ◽  
Sheng Sun ◽  
Joseph Heitman
Keyword(s):  
Mating Type ◽  
Genetic Material ◽  
Nuclear Genome ◽  
Sexual Cycle ◽  
Uniparental Inheritance ◽  
Opposite Mating Type ◽  
Fluorescent Reporter ◽  
Unisexual Reproduction ◽  
F1 Progeny ◽  
Opposite Sex

AbstractSome animal species require an opposite-sex partner for their sexual development but discard the partner’s genome before gamete formation, generating hemi-clonal progeny in a process called hybridogenesis. In this study, we discovered hybridogenesis-like reproduction in a basidiomycete fungus, Cryptococcus neoformans. C. neoformans has two mating types, MATa and MATα, which fuse to produce a dikaryotic zygote that completes a sexual cycle producing recombinant meiotic progeny. Here, we discovered exclusive uniparental inheritance of nuclear genetic material in a fraction of the F1 progeny produced during bisexual reproduction of two opposite mating-type partners. By analyzing strains expressing fluorescent reporter proteins, we observed that dikaryotic hyphae were produced, but only one parental nuclei was found in the terminal basidium where sporulation occurs. Whole-genome sequencing revealed the nuclear genome of the progeny was identical with one or the other parental genome, whereas the mitochondrial genome was always inherited from the MATa parent. Uniparental sporulation was also observed in natural isolate crosses occurring in concert with biparental sporulation. The meiotic recombinase Dmc1 was found to be critical for uniparental reproduction. These findings reveal an unusual mode of eukaryotic microbial unisexual reproduction that shares features with hybridogenesis in animals.

scholarly journals Differential Gene Expression between Fungal Mating Types Is Associated with Sequence Degeneration

2020 ◽  
Vol 12 (4) ◽  
pp. 243-258 ◽  
Author(s):  
Wen-Juan Ma ◽  
Fantin Carpentier ◽  
Tatiana Giraud ◽  
Michael E Hood
Keyword(s):  
Differential Expression ◽  
Differentially Expressed Genes ◽  
Mating Type ◽  
Sex Chromosomes ◽  
Sex Chromosome ◽  
Gc Content ◽  
Differentially Expressed ◽  
Mating Types ◽  
Sexual Antagonism ◽  
Recombination Suppression

Abstract Degenerative mutations in non-recombining regions, such as in sex chromosomes, may lead to differential expression between alleles if mutations occur stochastically in one or the other allele. Reduced allelic expression due to degeneration has indeed been suggested to occur in various sex-chromosome systems. However, whether an association occurs between specific signatures of degeneration and differential expression between alleles has not been extensively tested, and sexual antagonism can also cause differential expression on sex chromosomes. The anther-smut fungus Microbotryum lychnidis-dioicae is ideal for testing associations between specific degenerative signatures and differential expression because 1) there are multiple evolutionary strata on the mating-type chromosomes, reflecting successive recombination suppression linked to mating-type loci; 2) separate haploid cultures of opposite mating types help identify differential expression between alleles; and 3) there is no sexual antagonism as a confounding factor accounting for differential expression. We found that differentially expressed genes were enriched in the four oldest evolutionary strata compared with other genomic compartments, and that, within compartments, several signatures of sequence degeneration were greater for differentially expressed than non-differentially expressed genes. Two particular degenerative signatures were significantly associated with lower expression levels within differentially expressed allele pairs: upstream insertion of transposable elements and mutations truncating the protein length. Other degenerative mutations associated with differential expression included nonsynonymous substitutions and altered intron or GC content. The association between differential expression and allele degeneration is relevant for a broad range of taxa where mating compatibility or sex is determined by genes located in large regions where recombination is suppressed.

scholarly journals THE SEARCH FOR MATING-TYPE-LIMITED GENES IN THE HOMOTHALLIC ALGA CHLAMYDOMONAS MONOICA

Genetics ◽  
1986 ◽  
Vol 113 (3) ◽  
pp. 601-619
Author(s):  
Karen P VanWinkle-Swift ◽  
Jang-Hee Hahn
Keyword(s):  
Mating Type ◽  
Resistance Mutation ◽  
Mendelian Inheritance ◽  
Sexual Cycle ◽  
Uniparental Inheritance ◽  
Cell Type ◽  
Erythromycin Resistance ◽  
Type Locus ◽  
Heterothallic Species ◽  
Chlamydomonas Monoica

ABSTRACT The non-Mendelian erythromycin resistance mutation ery-u1 shows bidirectional uniparental inheritance in crosses between homothallic ery-u1 and ery-u1  + strains of Chlamydomonas monoica. This inheritance pattern supports a general model for homothallism invoking intrastrain differentiation into opposite compatible mating types and, further, suggests that non-Mendelian inheritance is under mating-type (mt) control in C. monoica as in heterothallic species. However, the identification of genes expressed or required by one gametic cell type, but not the other, is essential to verify the existence of a regulatory mating-type locus in C. monoica and to understand its role in cell differentiation and sexual development. By screening for a shift from bidirectional to unidirectional transmission of the non-Mendelian ery-u1 marker, a mutant with an apparent mating-type-limited sexual cycle defect was obtained. The responsible mutation, mtl-1, causes a 1000-fold reduction in zygospore germination in populations homozygous for the mutant allele and, approximately, a 50% reduction in germination for heterozygous (mtl-1/mtl-1  +) zygospores. By next screening for strains unable to yield any viable zygospores in a cross to mtl-1, a second putative mating-type-limited mutant, mtl-2, was obtained. The mtl-2 strain, although self-sterile, mates efficiently with mtl-2  + strains and shows a unidirectional uniparental pattern of inheritance for the ery-u1 cytoplasmic marker, similar to that observed for crosses involving mtl-1. Genetic analysis indicates that mtl-1 and mtl-2 define unique unlinked Mendelian loci and that the sexual cycle defects of reduced germination (mtl-1) or self-sterility (mtl-2) cosegregate with the effect on ery-u1 cytoplasmic gene transmission. By analogy to C. reinhardtii, the mtl-1 and mtl-2 phenotypes can be explained if the expression of these gene loci is limited to the mt  + gametic cell type, or if the wild-type alleles at these loci are required for the normal formation and/or functioning of mt  + gametes only.

scholarly journals Deletion of the Schizophyllum commune Aα Locus: The Roles of Aα Y and Z Mating-Type Genes

Genetics ◽  
1996 ◽  
Vol 144 (4) ◽  
pp. 1437-1444
Author(s):  
C Ian Robertson ◽  
Kirk A Bartholomew ◽  
Charles P Novotny ◽  
Robert C Ullrich
Keyword(s):  
Mating Type ◽  
Sexual Development ◽  
Schizophyllum Commune ◽  
Mating Types ◽  
Developmental Pathway ◽  
Mating Type Gene ◽  
Mating Type Genes ◽  
Regulatory Loci ◽  
Type Gene

The Aα locus is one of four master regulatory loci that determine mating type and regulate sexual development in Schizophyllum commune. We have made a plasmid containing a URA1 gene disruption of the Aα Y1 gene. Y1 is the sole Aα gene in Aα1 strains. We used the plasmid construction to produce an Aα null (i.e., AαΔ) strain by replacing the genomic Y1 gene with URA1 in an Aα1 strain. To characterize the role of the Aα genes in the regulation of sexual development, we transformed various Aα Y and Z alleles into AαΔ strains and examined the acquired mating types and mating abilities of the transformants. These experiments demonstrate that the Aα Y gene is not essential for fungal viability and growth, that a solitary Z Aα mating-type gene does not itself activate development, that Aβ proteins are sufficient to activate the A developmental pathway in the absence of Aα proteins and confirm that Y and Z genes are the sole determinants of Aα mating type. The data from these experiments support and refine our model of the regulation of A-pathway events by Y and Z proteins.

scholarly journals A PCR-based Assay for Distinguishing between A1 and A2 Mating Types of Phytophthora capsici

2017 ◽  
Vol 142 (4) ◽  
pp. 260-264
Author(s):  
Ping Li ◽  
Dong Liu ◽  
Min Guo ◽  
Yuemin Pan ◽  
Fangxin Chen ◽  
...  
Keyword(s):  
Genetic Diversity ◽  
Mating Type ◽  
Phytophthora Capsici ◽  
Mating Types ◽  
Sequence Repeat ◽  
Chain Reaction ◽  
Plant Parasite ◽  
Dna Fragment ◽  
Polymerase Chain ◽  
Microsatellite Diversity

Sexual reproduction in the plant parasite Phytophthora capsici Leonian requires the interaction of two distinct mating types, A1 and A2. Co-occurrence of these mating types can enhance the genetic diversity of P. capsici and alter its virulence or resistance characteristics. Using an intersimple sequence repeat (ISSR) screen of microsatellite diversity, we identified, cloned, and sequenced a novel 1121-base pair (bp) fragment specific to the A1 mating type of P. capsici. Primers Pcap-1 and Pcap-2 were designed from this DNA fragment to specifically detect the A1 mating type. Polymerase chain reaction (PCR) using these primers amplified an expected 997-bp fragment from known A1 mating types, but yielded a 508-bp fragment from known A2 mating types. This PCR-based assay could be adapted to accurately and rapidly detect the co-occurrence of A1 and A2 P. capsici mating types from field material.

scholarly journals The Chlamydomonas Mating Type Plus Fertilization Tubule, a Prototypic Cell Fusion Organelle: Isolation, Characterization, and In Vitro Adhesion to Mating Type Minus Gametes

1997 ◽  
Vol 137 (7) ◽  
pp. 1537-1553 ◽  
Author(s):  
Nedra F. Wilson ◽  
Mary J. Foglesong ◽  
William J. Snell
Keyword(s):  
Cell Fusion ◽  
Mating Type ◽  
Plasma Membranes ◽  
Surface Proteins ◽  
Filamentous Actin ◽  
Mating Structure ◽  
Cell Protrusion ◽  
Isolation And Characterization ◽  
In Vitro Adhesion

In the biflagellated alga Chlamydomonas, adhesion and fusion of the plasma membranes of gametes during fertilization occurs via an actin-filled, microvillus-like cell protrusion. Formation of this ∼3-μm-long fusion organelle, the Chlamydomonas fertilization tubule, is induced in mating type plus (mt+) gametes during flagellar adhesion with mating type minus (mt−) gametes. Subsequent adhesion between the tip of the mt+ fertilization tubule and the apex of a mating structure on mt− gametes is followed rapidly by fusion of the plasma membranes and zygote formation. In this report, we describe the isolation and characterization of fertilization tubules from mt+ gametes activated for cell fusion. Fertilization tubules were detached by homogenization of activated mt+ gametes in an EGTA-containing buffer and purified by differential centrifugation followed by fractionation on sucrose and Percoll gradients. As determined by fluorescence microscopy of samples stained with a fluorescent probe for filamentous actin, the method yielded 2–3 × 106 fertilization tubules/μg protein, representing up to a 360-fold enrichment of these organelles. Examination by negative stain electron microscopy demonstrated that the purified fertilization tubules were morphologically indistinguishable from fertilization tubules on intact, activated mt+ gametes, retaining both the extracellular fringe and the internal array of actin filaments. Several proteins, including actin as well as two surface proteins identified by biotinylation studies, copurified with the fertilization tubules. Most importantly, the isolated mt+ fertilization tubules bound to the apical ends of activated mt− gametes between the two flagella, the site of the mt− mating structure; a single fertilization tubule bound per cell, binding was specific for gametes, and fertilization tubules isolated from trypsin-treated, activated mt+ gametes did not bind to activated mt− gametes.

The alpha-mating type locus of Cryptococcus neoformans contains a peptide pheromone gene

1993 ◽  
Vol 13 (3) ◽  
pp. 1962-1970
Author(s):  
T D Moore ◽  
J C Edman
Keyword(s):  
Cryptococcus Neoformans ◽  
Mating Type ◽  
Cell Types ◽  
Yeast Cells ◽  
Mating Types ◽  
Type Locus ◽  
Reading Frame ◽  
Cloning Method ◽  
Opportunistic Fungal Pathogen ◽  
Specific Fragment

The opportunistic fungal pathogen Cryptococcus neoformans has two mating types, MATa and MAT alpha. The MAT alpha strains are more virulent. Mating of opposite mating type haploid yeast cells results in the production of a filamentous hyphal phase. The MAT alpha locus has been isolated in this study in order to identify the genetic differences between mating types and their contribution to virulence. A 138-bp fragment of MAT alpha-specific DNA which cosegregates with alpha-mating type was isolated by using a difference cloning method. Overlapping phage and cosmid clones spanning the entire MAT alpha locus were isolated by using this MAT alpha-specific fragment as a probe. Mapping of these clones physically defined the MAT alpha locus to a 35- to 45-kb region which is present only in MAT alpha strains. Transformation studies with fragments of the MAT alpha locus identified a 2.1-kb XbaI-HindIII fragment that directs starvation-induced filament formation in MATa cells but not in MAT alpha cells. This 2.1-kb fragment contains a gene, MF alpha, with a small open reading frame encoding a pheromone precursor similar to the lipoprotein mating factors found in Saccharomyces cerevisiae, Ustilago maydis, and Schizosaccharomyces pombe. The ability of the MATa cells to express, process, and secrete the MAT alpha pheromone in response to starvation suggests similar mechanisms for these processes in both cell types. These results also suggest that the production of pheromone is under a type of nutritional control shared by the two cell types.

Transformation of protoplasted yeast cells is directly associated with cell fusion

1984 ◽  
Vol 4 (4) ◽  
pp. 771-778
Author(s):  
S Harashima ◽  
A Takagi ◽  
Y Oshima
Keyword(s):  
Cell Fusion ◽  
Mating Type ◽  
Nuclear Fusion ◽  
Yeast Cells ◽  
Nuclear Markers ◽  
Type Locus ◽  
Mating Type Locus ◽  
Yeast Protoplasts ◽  
Yeast Plasmids ◽  
Binominal Distribution

The frequency of cell fusion during transformation of yeast protoplasts with various yeast plasmids with a chromosome replicon (YRp or YCp) or 2 mu DNA (YEp) was estimated by two methods. In one method, a mixture of protoplasts of two haploid strains with identical mating type and complementary auxotrophic nuclear markers with or without cytoplasmic markers was transformed. When the number of various phenotypic classes of transformants for the nuclear markers was analyzed by equations derived from binominal distribution theory, the frequency of nuclear fusion among the transformants was 42 to 100% in transformations with the YRp or YCp plasmids and 28 to 39% with the YEp plasmids. In another method, a haploid bearing the sir mutation, which allows a diploid (or polyploid) homozygous for the MAT (mating type) locus to sporulate by the expression of the silent mating-type loci HML and HMR, was transformed with the plasmids. Sporulation ability was found in 43 to 95% of the transformants with the YRp or YCp plasmids, and 26 to 31% of the YEp transformants. When cytoplasmic mixing was included with the nuclear fusion, 96 to 100% of the transformants were found to be cell fusants. Based upon these observations, we concluded that transformation of yeast protoplasts is directly associated with cell fusion.

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