scholarly journals The Pheromone and Pheromone Receptor Mating-Type Locus Is Involved in Controlling Uniparental Mitochondrial Inheritance in Cryptococcus

Genetics ◽  
2019 ◽  
Vol 214 (3) ◽  
pp. 703-717 ◽  
Author(s):  
Sheng Sun ◽  
Ci Fu ◽  
Giuseppe Ianiri ◽  
Joseph Heitman
Keyword(s):  
Sexual Reproduction ◽  
Mendelian Inheritance ◽  
Fungal Species ◽  
Uniparental Inheritance ◽  
Ancestral State ◽  
Type Locus ◽  
Pheromone Receptor ◽  
Selfish Genetic Elements ◽  
Restrict Movement ◽  
Underlying Mechanisms

Mitochondria are inherited uniparentally during sexual reproduction in the majority of eukaryotic species studied, including humans, mice, and nematodes, as well as many fungal species. Mitochondrial uniparental inheritance (mito-UPI) could be beneficial in that it avoids possible genetic conflicts between organelles with different genetic backgrounds, as recently shown in mice, and it could prevent the spread of selfish genetic elements in the mitochondrial genome. Despite the prevalence of observed mito-UPI, the underlying mechanisms and the genes involved in controlling this non-Mendelian inheritance are poorly understood in many species. In Cryptococcus neoformans, a human pathogenic basidiomyceteous fungus, mating types (MATα and MATa) are defined by alternate alleles at the single MAT locus that evolved from fusion of the two MAT loci (P/R encoding pheromones and pheromone receptors, and HD encoding homeodomain transcription factors) that are the ancestral state in the basidiomycota. Mitochondria are inherited uniparentally from the MATa parent in C. neoformans, and this requires the SXI1α and SXI2a HD factors encoded by MAT. However, there is evidence that additional genes contribute to the control of mito-UPI in Cryptococcus. Here, we show that in C. amylolentus, a sibling species of C. neoformans with unlinked P/R and HD MAT loci, mito-UPI is controlled by the P/R locus and is independent of the HD locus. Consistently, by replacing the MATα alleles of the pheromones (MF) and pheromone receptor (STE3) with the MATa alleles, we show that these P/R locus-defining genes indeed affect mito-UPI in C. neoformans during sexual reproduction. Additionally, we show that during early stages of C. neoformans sexual reproduction, conjugation tubes are always produced by the MATα cells, resulting in unidirectional migration of the MATα nucleus into the MATa cell during zygote formation. This process is controlled by the P/R locus and could serve to physically restrict movement of MATα mitochondria in the zygotes, and thereby contribute to mito-UPI. We propose a model in which both physical and genetic mechanisms function in concert to prevent the coexistence of mitochondria from the two parents in the zygote, and subsequently in the meiotic progeny, thus ensuring mito-UPI in pathogenic Cryptococcus, as well as in closely related nonpathogenic species. The implications of these findings are discussed in the context of the evolution of mito-UPI in fungi and other more diverse eukaryotes.

scholarly journals The pheromone and pheromone receptor mating-type locus is involved in controlling uniparental mitochondrial inheritance in Cryptococcus

2019 ◽  
Author(s):  
Sheng Sun ◽  
Ci Fu ◽  
Giuseppe Ianiri ◽  
Joseph Heitman
Keyword(s):  
Sexual Reproduction ◽  
Mendelian Inheritance ◽  
Fungal Species ◽  
Uniparental Inheritance ◽  
Ancestral State ◽  
Type Locus ◽  
Pheromone Receptor ◽  
Selfish Genetic Elements ◽  
Restrict Movement ◽  
Underlying Mechanisms

ABSTRACTMitochondria are inherited uniparentally during sexual reproduction in the majority of eukaryotic species studied, including humans, mice, nematodes, as well as many fungal species. Mitochondrial uniparental inheritance (mito-UPI) could be beneficial in that it avoids possible genetic conflicts between organelles with different genetic backgrounds, as recently shown in mice; and it could prevent the spread of selfish genetic elements in the mitochondrial genome. Despite the prevalence of observed mito-UPI, the underlying mechanisms and the genes involved in controlling this non-mendelian inheritance are poorly understood in many species. In Cryptococcus neoformans, a human pathogenic basidiomyceteous fungus, mating types (MATα and MATa) are defined by alternate alleles at the single MAT locus that evolved from fusion of the two MAT loci (P/R encoding pheromones and pheromone receptors, HD encoding homeodomain transcription factors) that are the ancestral state in the basidiomycota. Mitochondria are inherited uniparentally from the MATa parent in C. neoformans and this requires the SXI1α and SXI2a HD factors encoded by MAT. However, there is evidence additional genes contribute to control of mito-UPI in Cryptococcus. Here we show that in Cryptococcus amylolentus, a sibling species of C. neoformans with unlinked P/R and HD MAT loci, mitochondrial uniparental inheritance is controlled by the P/R locus, and is independent of the HD locus. Consistently, by replacing the MATα alleles of the pheromones (MF) and pheromone receptor (STE3) with the MATa alleles, we show that these P/R locus defining genes indeed affect mito-UPI in C. neoformans during sexual reproduction. Additionally, we show that during early stages of C. neoformans sexual reproduction, conjugation tubes are always produced by the MATα cells, resulting in unidirectional migration of the MATα nucleus into the MATa cell during zygote formation. This process is controlled by the P/R locus and could serve to physically restrict movement of MATα mitochondria in the zygotes, and thereby contribute to mito-UPI. We propose a model in which both physical and genetic mechanisms function in concert to prevent the coexistence of mitochondria from the two parents in the zygote and subsequently in the meiotic progeny, thus ensuring mito-UPI in pathogenic Cryptococcus, as well as in closely related non-pathogenic species. The implications of these findings are discussed in the context of the evolution of mito-UPI in fungi and other more diverse eukaryotes.

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 Expression and Immunostaining Analyses Suggest thatPneumocystisPrimary Homothallism Involves Trophic Cells Displaying Both Plus and Minus Pheromone Receptors

mBio ◽  
2019 ◽  
Vol 10 (4) ◽  
Author(s):  
A. Luraschi ◽  
S. Richard ◽  
J. M. G. C. F. Almeida ◽  
M. Pagni ◽  
M. T. Cushion ◽  
...  
Keyword(s):  
Fungal Infections ◽  
Severe Pneumonia ◽  
Mate Recognition ◽  
Fungal Species ◽  
Sexual Cycle ◽  
Host Immune System ◽  
Type Locus ◽  
Pheromone Receptor ◽  
Human Lungs

ABSTRACTThe genusPneumocystisencompasses fungal species that colonize mammals’ lungs with host specificity. Should the host immune system weaken, the fungal species can cause severe pneumonia. The life cycle of these pathogens is poorly known, mainly because anin vitroculture method has not been established. Both asexual and sexual cycles would occur. Trophic cells, the predominant forms during infection, could multiply asexually but also enter into a sexual cycle. Comparative genomics revealed a single mating type locus, including plus and minus genes, suggesting that primary homothallism involving self-fertility of each strain is the mode of reproduction ofPneumocystisspecies. We identified and analyzed the expression of themam2andmap3genes encoding the receptors for plus and minus pheromones using reverse transcriptase PCR, in both infected mice and bronchoalveolar lavage fluid samples from patients withPneumocystispneumonia. Both receptors were most often concomitantly expressed during infection, revealing that both pheromone-receptor systems are involved in the sexual cycle. Themap3transcripts were subject to alternative splicing. Using immunostaining, we investigated the presence of the pheromone receptors at the surfaces ofPneumocystiscells from a patient. The staining tools were first assessed inSaccharomyces cerevisiaedisplaying thePneumocystisreceptors at their cellular surface. Both receptors were present at the surfaces of the vast majority of the cells that were likely trophic forms. The receptors might have a role in mate recognition and/or postfertilization events. Their presence at the cell surface might facilitate outbreeding versus inbreeding of self-fertile strains.IMPORTANCEThe fungi belonging to the genusPneumocystismay cause severe pneumonia in immunocompromised humans, a disease that can be fatal if not treated. This disease is nowadays one of the most frequent invasive fungal infections worldwide. Whole-genome sequencing revealed that the sexuality of these fungi involves a single partner that can self-fertilize. Here, we report that two receptors recognizing specifically excreted pheromones are involved in this self-fertility within infected human lungs. Using fluorescent antibodies binding specifically to these receptors, we observed that most often, the fungal cells display both receptors at their surface. These pheromone-receptor systems might play a role in mate recognition and/or postfertilization events. They constitute an integral part of thePneumocystisobligate sexuality within human lungs, a cycle that is necessary for the dissemination of the fungus to new individuals.

Selfish genetic elements and their role in evolution: the evolution of sex and some of what that entails

1995 ◽  
Vol 349 (1329) ◽  
pp. 321-332 ◽  
Keyword(s):  
Sexual Reproduction ◽  
Empirical Support ◽  
Nuclear Genes ◽  
Uniparental Inheritance ◽  
Mating Types ◽  
Evolution Of Sex ◽  
Conflict Of Interests ◽  
Genetic Elements ◽  
Selfish Genetic Elements ◽  
To Receive

An individual is often considered (sometimes implicitly) to be the product of a well functioning mutualism between its constituent genes. This however need not be so. One consequence of sexual reproduction is that costly competition within an individual between genes that are effectively allelic can provide the conditions for the spread of suppressors of such competition. The spread of both these ultracompetitive alleles (alias selfish genetic elements) and their suppressors is evidence of a ‘conflict of interests’ within the genome. That this conflict is a potentially important force in the evolution of genetic systems is illustrated by consideration of the problem of the evolution of sexes (alias mating types). One hypothesis holds that sexes are the result of selection on nuclear genes to coordinate the inheritance of cytoplasmic genomes (usually this means the enforcement of uniparental inheritance) so as to prevent competition between unrelated cytoplasmic genomes. This hypothesis is tested against five comparative predictions and shown to receive considerable empirical support.

scholarly journals Mating-type locus rearrangement leads to shift from homothallism to heterothallism in Citrus-associated Phyllosticta species

2020 ◽  
Author(s):  
Desirrê Alexia Lourenço Petters-Vandresen ◽  
Bruno Janoski Rossi ◽  
Johannes Z. Groenewald ◽  
Pedro W. Crous ◽  
Marcos Antonio Machado ◽  
...  
Keyword(s):  
Disease Management ◽  
Sexual Reproduction ◽  
Mating Type ◽  
Management Practices ◽  
Black Spot ◽  
Tan Spot ◽  
Ancestral State ◽  
Type Locus ◽  
Mating Type Locus ◽  
Host Interaction

AbstractCurrently, eight Phyllosticta species are known to be associated with Citrus hosts, incorporating endophytic and pathogenic lifestyles. As sexual reproduction is a key factor involved in host-interaction, it could be related to the differences in lifestyle. To evaluate this hypothesis, we characterized the mating-type loci of six Citrus-associated Phyllosticta species from whole genome assemblies. Mating-type genes are highly variable in their sequence content, but the genomic locations and organization of the mating-type loci are conserved. Phyllosticta citriasiana, P. citribraziliensis and P. paracitricarpa are heterothallic, and P. citrichinaensis was confirmed to be homothallic. In addition, the P. citrichinaensis MAT1-2 idiomorph occurs in a separate location from the mating-type locus. Ancestral state reconstruction suggests that homothallism is the ancestral thallism state in Phyllosticta, with a shift to heterothallism in Phyllosticta species that are pathogenic to Citrus. Moreover, the homothallic strategies of P. capitalensis and P. citrichinaensis result from independent evolutionary events. As the pathogenic species P. citriasiana, P. citricarpa and P. paracitricarpa are heterothallic and incapable of selfing, disease management practices focused in preventing the occurrence of sexual reproduction could assist in the control of Citrus Black Spot and Citrus Tan Spot diseases. This study emphasizes the importance of studying Citrus-Phyllosticta interactions under evolutionary and genomic perspectives, as these approaches can provide valuable information about the association between Phyllosticta species and their hosts, and also serve as guidance for the improvement of disease management practices.

scholarly journals Investigation of Mating Pheromone–Pheromone Receptor Specificity in Lentinula edodes

Genes ◽  
2020 ◽  
Vol 11 (5) ◽  
pp. 506
Author(s):  
Sinil Kim ◽  
Byeongsuk Ha ◽  
Minseek Kim ◽  
Hyeon-Su Ro
Keyword(s):  
Mating Type ◽  
Lentinula Edodes ◽  
Signal Pathway ◽  
Recombinant Yeast ◽  
Mating Pheromone ◽  
Type Locus ◽  
Pheromone Receptor ◽  
Mating Type Locus ◽  
Yeast Mating ◽  
Mating Signal

The B mating-type locus of Lentinula edodes, a representative edible mushroom, is highly complex because of allelic variations in the mating pheromone receptors (RCBs) and the mating pheromones (PHBs) in both the Bα and Bβ subloci. The complexity of the B mating-type locus, five Bα subloci with five alleles of RCB1 and nine PHBs and three Bβ subloci with 3 alleles of RCB2 and five PHBs, has led us to investigate the specificity of the PHB–RCB interaction because the interaction plays a key role in non-self-recognition. In this study, the specificities of PHBs to RCB1-2 and RCB1-4 from the Bα sublocus and RCB2-1 from the Bb sublocus were investigated using recombinant yeast strains generated by replacing STE2, an endogenous yeast mating pheromone receptor, with the L. edodes RCBs. Fourteen synthetic PHBs with C-terminal carboxymethylation but without farnesylation were added to the recombinant yeast cells and the PHB–RCB interaction was monitored by the expression of the FUS1 gene—a downstream gene of the yeast mating signal pathway. RCB1-2 (Bα2) was activated by PHB1 (4.3-fold) and PHB2 (2.1-fold) from the Bα1 sublocus and RCB1-4 (Bα4) was activated by PHB5 (3.0-fold) and PHB6 (2.7-fold) from the Bα2 sublocus and PHB13 (3.0-fold) from the Bα5 sublocus. In particular, PHB3 from Bβ2 and PHB9 from Bβ3 showed strong activation of RCB2-1 of the Bβ1 sublocus by 59-fold. The RCB–PHB interactions were confirmed in the monokaryotic S1–10 strain of L. edodes by showing increased expression of clp1, a downstream gene of the mating signal pathway and the occurrence of clamp connections after the treatment of PHBs. These results indicate that a single PHB can interact with a non-self RCB in a sublocus-specific manner for the activation of the mating pheromone signal pathways in L. edodes.

scholarly journals ‘Meiotic genes’ are constitutively expressed in an asexual amoeba and are not necessarily involved in sexual reproduction

2019 ◽  
Vol 15 (3) ◽  
pp. 20180871 ◽  
Author(s):  
Sutherland K. Maciver ◽  
Zisis Koutsogiannis ◽  
Alvaro de Obeso Fernández del Valle
Keyword(s):  
Homologous Recombination ◽  
Sexual Reproduction ◽  
Asexual Reproduction ◽  
Shotgun Sequencing ◽  
Ancestral State ◽  
Rna Seq ◽  
Next Generation ◽  
Related Process

The amoebae (and many other protists) have traditionally been considered as asexual organisms, but suspicion has been growing that these organisms are cryptically sexual or are at least related to sexual lineages. This contention is mainly based on genome studies in which the presence of ‘meiotic genes’ has been discovered. Using RNA-seq (next-generation shotgun sequencing, identifying and quantifying the RNA species in a sample), we have found that the entire repertoire of meiotic genes is expressed in exponentially growing Acanthamoeba and we argue that these so-called meiotic genes are involved in the related process of homologous recombination in this amoeba. We contend that they are only involved in meiosis in other organisms that indulge in sexual reproduction and that homologous recombination is important in asexual protists as a guard against the accumulation of mutations. We also suggest that asexual reproduction is the ancestral state.

Selfish DNA as a method of pest control

1994 ◽  
Vol 344 (1309) ◽  
pp. 313-324 ◽  
Keyword(s):  
Genetic Load ◽  
Single Copy ◽  
Mendelian Inheritance ◽  
Host Population ◽  
Molecular Techniques ◽  
Uniparental Inheritance ◽  
Pest Species ◽  
Agricultural Pests ◽  
Selfish Dna ◽  
Host Fitness

The inheritance of most genes is tightly controlled, governed by the rules of mendelian inheritance if nuclear or uniparental inheritance if cytoplasmic. A few notable genes and cytoplasmic genomes have escaped this regulation. Such genes may spread by increasing their own rate of transmission despite reducing host fitness and may be regarded as ‘selfish’. Their population genetics are described and it appears they may impose a significant genetic load on the host population. Modern molecular techniques may enable similar loads to be imposed on pest species either by transferring selfish genes between species, or by linking deleterious genes to a selfish locus. Alternatively, ‘modifier’ genes that eliminate the virulent, or disease vectorial capacity, of the pest population may be introduced by linkage to a selfish locus. Selfish elements present in multiple copies may be preferable to single-copy elements as the former are capable of a larger reduction in host fitness. The practical application of these agents depends on five factors: (i) the rate of ‘reversion’ to a non-selfish form; (ii) the evolution of host repressor systems; (iii) their effect on host fitness, which determines their rate of invasion; (iv) the mechanism regulating host population size in the field; and (v) their ease of manipulation in the laboratory. The first two factors are the most uncertain in most systems, but should be amenable to experimental analysis. It is proposed that the development of such techniques may result in powerful new methods of population control which may be applied to both agricultural pests and disease vectors.

scholarly journals Comparative Mitogenomics of Fungal Species in Stachybotryaceae Provides Evolutionary Insights into Hypocreales

2021 ◽  
Vol 22 (24) ◽  
pp. 13341
Author(s):  
Li-Yuan Ren ◽  
Shu Zhang ◽  
Yong-Jie Zhang
Keyword(s):  
State Estimation ◽  
Early Cretaceous ◽  
Gene Order ◽  
Phylogenetic Analyses ◽  
Fungal Species ◽  
Stachybotrys Chartarum ◽  
Ancestral State ◽  
Intron Insertion ◽  
Dominant Pattern ◽  
The Family

Stachybotrys chartarum is one of the world’s ten most feared fungi within the family Stachybotryaceae, although to date, not a single mitogenome has been documented for Stachybotryaceae. Herein, six mitogenomes of four different species in Stachybotryaceae are newly reported. The S. chartarum mitogenome was 30.7 kb in length and contained two introns (one each in rnl and cox1). A comparison of the mitogenomes of three different individuals of S. chartarum showed few nucleotide variations and conservation of gene content/order and intron insertion. A comparison of the mitogenomes of four different Stachybotryaceae species (Memnoniella echinata, Myrothecium inundatum, S. chartarum, and S. chlorohalonata), however, revealed variations in intron insertion, gene order/content, and nad2/nad3 joining pattern. Further investigations on all Hypocreales species with available mitogenomes showed greater variabilities in gene order (six patterns) and nad2/nad3 joining pattern (five patterns) although a dominant pattern always existed in each case. Ancestral state estimation showed that in each case the dominant pattern was always more ancestral than those rare patterns. Phylogenetic analyses based on mitochondrion-encoded genes supported the placement of Stachybotryaceae in Hypocreales. The crown age of Stachybotryaceae was estimated to be approximately the Early Cretaceous (141–142 Mya). This study greatly promotes our understanding of the evolution of fungal species in Hypocreales.

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