Multiple Pathways to Homothallism in Closely Related Yeast Lineages in the Basidiomycota

ABSTRACT Sexual reproduction in fungi relies on proteins with well-known functions encoded by the mating type (MAT) loci. In the Basidiomycota, MAT loci are often bipartite, with the P/R locus encoding pheromone precursors and pheromone receptors and the HD locus encoding heterodimerizing homeodomain transcription factors (Hd1/Hd2). The interplay between different alleles of these genes within a single species usually generates at least two compatible mating types. However, a minority of species are homothallic, reproducing sexually without an obligate need for a compatible partner. Here, we examine the organization and function of the MAT loci of Cystofilobasidium capitatum, a species in the order Cystofilobasidiales, which is unusually rich in homothallic species. We determined MAT gene content and organization in C. capitatum and found that it resembles a mating type of the closely related heterothallic species Cystofilobasidium ferigula. To explain the homothallic sexual reproduction observed in C. capitatum, we examined HD protein interactions in the two Cystofilobasidium species and determined C. capitatum MAT gene expression both in a natural setting and upon heterologous expression in Phaffia rhodozyma, a homothallic species belonging to a clade sister to that of Cystofilobasidium. We conclude that the molecular basis for homothallism in C. capitatum appears to be distinct from that previously established for P. rhodozyma. Unlike in the latter species, homothallism in C. capitatum may involve constitutive activation or dispensability of the pheromone receptor and the functional replacement of the usual Hd1/Hd2 heterodimer by an Hd2 homodimer. Overall, our results suggest that homothallism evolved multiple times within the Cystofilobasidiales. IMPORTANCE Sexual reproduction is important for the biology of eukaryotes because it strongly impacts the dynamics of genetic variation. In fungi, although sexual reproduction is usually associated with the fusion between cells belonging to different individuals (heterothallism), sometimes a single individual is capable of completing the sexual cycle alone (homothallism). Homothallic species are unusually common in a fungal lineage named Cystofilobasidiales. Here, we studied the genetic bases of homothallism in one species in this lineage, Cystofilobasidium capitatum, and found it to be different in several aspects from those of another homothallic species, Phaffia rhodozyma, belonging to the genus most closely related to Cystofilobasidium. Our results strongly suggest that homothallism evolved independently in Phaffia and Cystofilobasidium, lending support to the idea that transitions between heterothallism and homothallism are not as infrequent as previously thought. Our work also helps to establish the Cystofilobasidiales as a model lineage in which to study these transitions.

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Multiple pathways to homothallism in closely related yeast lineages in the Basidiomycota

10.1101/2020.09.30.320192 ◽

2020 ◽

Author(s):

Alexandra Cabrita ◽

Márcia David-Palma ◽

Patrícia H. Brito ◽

Joseph Heitman ◽

Marco A Coelho ◽

...

Keyword(s):

Sexual Reproduction ◽

Mating Type ◽

Protein Interactions ◽

Molecular Mechanisms ◽

Single Species ◽

Natural Setting ◽

Sexual Systems ◽

Heterothallic Species ◽

And Function ◽

Mat Gene

Sexual reproduction in fungi relies on proteins with well-known functions encoded at the mating type (MAT) loci. In the Basidiomycota, MAT loci are often bipartite, the P/R locus encoding pheromone precursors and pheromone receptors and the HD locus encoding heterodimerizing homeodomain transcription factors (Hd1 and Hd2). The interplay between different alleles of these genes within a single species determines a variety of sexual systems and patterns, which may result in the emergence of hundreds of compatible mating types. However, a minority of species are homothallic, reproducing sexually without the need for a compatible partner. Here we examine the organization and function of the MAT loci of Cystofilobasidium capitatum, a species in the order Cystofilobasidiales, which is unusually rich in homothallic species. For this, we determined MAT gene content and organization in C. capitatum and found that it resembled a mating type of the closely related heterothallic species Cystofilobasidium ferigula. To explain the homothallic sexual reproduction observed in C. capitatum we examined HD -protein interactions in the two individual Cystofilobasidium species and determined C. capitatum MAT gene expression both in the natural setting and upon heterologous expression in Phaffia rhodozyma, a homothallic species belonging to a clade sister to the Cystofilobasidium. We conclude that the molecular basis for homothallism in C. capitatum appears to be distinct from that previously established for P. rhodozyma. Unlike the latter species, homothallism in C. capitatum may involve constitutive activation or dispensability of the pheromone receptor and the functional replacement of the usual Hd1/Hd2 heterodimer by an Hd2 homodimer. Overall, our results suggest that homothallism evolved multiple times in the Cystofilobasidiales, underpinned by diverse molecular mechanisms.

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Identification of the Mating-Type (MAT) Locus That Controls Sexual Reproduction of Blastomyces dermatitidis

Eukaryotic Cell ◽

10.1128/ec.00249-12 ◽

2012 ◽

Vol 12 (1) ◽

pp. 109-117 ◽

Cited By ~ 27

Author(s):

Wenjun Li ◽

Thomas D. Sullivan ◽

Eric Walton ◽

Anna Floyd Averette ◽

Sharadha Sakthikumar ◽

...

Keyword(s):

Sexual Reproduction ◽

Mating Type ◽

Genetic Recombination ◽

Sexual Cycle ◽

Blastomyces Dermatitidis ◽

Comparative Genomic ◽

Dimorphic Fungi ◽

Content Type ◽

Long Time ◽

Northern United States

ABSTRACTBlastomyces dermatitidisis a dimorphic fungal pathogen that primarily causes blastomycosis in the midwestern and northern United States and Canada. While the genes controlling sexual development have been known for a long time, the genes controlling sexual reproduction ofB. dermatitidis(teleomorph,Ajellomyces dermatitidis) are unknown. We identified the mating-type (MAT) locus in theB. dermatitidisgenome by comparative genomic approaches. TheB. dermatitidis MATlocus resembles those of other dimorphic fungi, containing either an alpha-box (MAT1-1) or an HMG domain (MAT1-2) gene linked to theAPN2,SLA2, andCOX13genes. However, in some strains ofB. dermatitidis, theMATlocus harbors transposable elements (TEs) that make it unusually large compared to theMATlocus of other dimorphic fungi. Based on theMATlocus sequences ofB. dermatitidis, we designed specific primers for PCR determination of the mating type. TwoB. dermatitidisisolates of opposite mating types were cocultured on mating medium. Immature sexual structures were observed starting at 3 weeks of coculture, with coiled-hyphae-containing cleistothecia developing over the next 3 to 6 weeks. Genetic recombination was detected in potential progeny by mating-type determination, PCR-restriction fragment length polymorphism (PCR-RFLP), and random amplification of polymorphic DNA (RAPD) analyses, suggesting that a meiotic sexual cycle might have been completed. The F1 progeny were sexually fertile when tested with strains of the opposite mating type. Our studies provide a model for the evolution of theMATlocus in the dimorphic and closely related fungi and open the door to classic genetic analysis and studies on the possible roles of mating and mating type in infection and virulence.

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A Surface Glycoprotein Indispensable for Gamete Fusion in the Social Amoeba Dictyostelium discoideum

Eukaryotic Cell ◽

10.1128/ec.00028-12 ◽

2012 ◽

Vol 11 (5) ◽

pp. 638-644 ◽

Cited By ~ 9

Author(s):

Yoshinori Araki ◽

Hideki D. Shimizu ◽

Kentaro Saeki ◽

Marina Okamoto ◽

Lixy Yamada ◽

...

Keyword(s):

Cell Adhesion ◽

Sexual Reproduction ◽

Dictyostelium Discoideum ◽

Mating Type ◽

Surface Glycoprotein ◽

Sexual Cycle ◽

Dependent Manner ◽

Content Type ◽

Social Amoeba ◽

The Social

ABSTRACT Sexual reproduction is essential for the maintenance of species in a wide variety of multicellular organisms, and even unicellular organisms that normally proliferate asexually possess a sexual cycle because of its contribution to increased genetic diversity. Information concerning the molecules involved in fertilization is accumulating for many species of the metazoan, plant, and fungal lineages, and the evolutionary consideration of sexual reproduction systems is now an interesting issue. Macrocyst formation in the social amoeba Dictyostelium discoideum is a sexual process in which cells become sexually mature under dark and submerged conditions and fuse with complementary mating-type cells. In the present study, we isolated D. discoideum insertional mutants defective in sexual cell fusion and identified the relevant gene, macA , which encodes a highly glycosylated, 2,041-amino-acid membrane protein (MacA). Although its overall similarity is restricted to proteins of unknown function within dictyostelids, it contains LamGL and discoidin domains, which are implicated in cell adhesion. The growth and development of macA -null mutants were indistinguishable from those of the parental strain. The overexpression of macA using the V18 promoter in a macA -null mutant completely restored its sexual defects. Although the macA gene encoded exactly the same protein in a complementary mating-type strain, it was expressed at a much lower level. These results suggest that MacA is indispensable for gamete interactions in D. discoideum , probably via cell adhesion. There is a possibility that it is controlled in a mating-type-dependent manner.

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

Genetics ◽

10.1093/genetics/113.3.601 ◽

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.

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Parasexuality and Ploidy Change in Candida tropicalis

Eukaryotic Cell ◽

10.1128/ec.00128-13 ◽

2013 ◽

Vol 12 (12) ◽

pp. 1629-1640 ◽

Cited By ~ 20

Author(s):

Riyad N. H. Seervai ◽

Stephen K. Jones ◽

Matthew P. Hirakawa ◽

Allison M. Porman ◽

Richard J. Bennett

Keyword(s):

Sexual Reproduction ◽

Candida Tropicalis ◽

Culture Conditions ◽

Sexual Cycle ◽

Chromosome Loss ◽

Parasexual Cycle ◽

Content Type ◽

Ploidy Changes ◽

Diploid Cells

ABSTRACTCandidaspecies exhibit a variety of ploidy states and modes of sexual reproduction. Most species possess the requisite genes for sexual reproduction, recombination, and meiosis, yet only a few have been reported to undergo a complete sexual cycle including mating and sporulation.Candida albicans, the most studiedCandidaspecies and a prevalent human fungal pathogen, completes its sexual cycle via a parasexual process of concerted chromosome loss rather than a conventional meiosis. In this study, we examine ploidy changes inCandida tropicalis, a closely related species toC. albicansthat was recently revealed to undergo sexual mating.C. tropicalisdiploid cells mate to form tetraploid cells, and we show that these can be induced to undergo chromosome loss to regenerate diploid forms by growth on sorbose medium. The diploid products are themselves mating competent, thereby establishing a parasexual cycle in this species for the first time. Extended incubation (>120 generations) ofC. tropicalistetraploid cells under rich culture conditions also resulted in instability of the tetraploid form and a gradual reduction in ploidy back to the diploid state. The fitness levels ofC. tropicalisdiploid and tetraploid cells were compared, and diploid cells exhibited increased fitness relative to tetraploid cellsin vitro, despite diploid and tetraploid cells having similar doubling times. Collectively, these experiments demonstrate distinct pathways by which a parasexual cycle can occur inC. tropicalisand indicate that nonmeiotic mechanisms drive ploidy changes in this prevalent human pathogen.

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Comparative Genomics Suggests Primary Homothallism of Pneumocystis Species

mBio ◽

10.1128/mbio.02250-14 ◽

2015 ◽

Vol 6 (1) ◽

Cited By ~ 26

Author(s):

João M. G. C. F. Almeida ◽

Ousmane H. Cissé ◽

Álvaro Fonseca ◽

Marco Pagni ◽

Philippe M. Hauser

Keyword(s):

Comparative Genomics ◽

Sexual Reproduction ◽

Mating Type ◽

Fungal Pathogens ◽

Pneumocystis Carinii ◽

Severe Pneumonia ◽

Genomic Region ◽

Pneumocystis Jirovecii ◽

Content Type

ABSTRACT Pneumocystis species are fungal parasites of mammal lungs showing host specificity. Pneumocystis jirovecii colonizes humans and causes severe pneumonia in immunosuppressed individuals. In the absence of in vitro cultures, the life cycle of these fungi remains poorly known. Sexual reproduction probably occurs, but the system of this process and the mating type (MAT) genes involved are not characterized. In the present study, we used comparative genomics to investigate the issue in P. jirovecii and Pneumocystis carinii, the species infecting rats, as well as in their relative Taphrina deformans. We searched sex-related genes using 103 sequences from the relative Schizosaccharomyces pombe as queries. Genes homologous to several sex-related role categories were identified in all species investigated, further supporting sexuality in these organisms. Extensive in silico searches identified only three putative MAT genes in each species investigated (matMc, matMi, and matPi). In P. jirovecii, these genes clustered on the same contig, proving their contiguity in the genome. This organization seems compatible neither with heterothallism, because two different MAT loci on separate DNA molecules would have been detected, nor with secondary homothallism, because the latter involves generally more MAT genes. Consistently, we did not detect cis-acting sequences for mating type switching in secondary homothallism, and PCR revealed identical MAT genes in P. jirovecii isolates from six patients. A strong synteny of the genomic region surrounding the putative MAT genes exists between the two Pneumocystis species. Our results suggest the hypothesis that primary homothallism is the system of reproduction of Pneumocystis species and T. deformans. IMPORTANCE Sexual reproduction among fungi can involve a single partner (homothallism) or two compatible partners (heterothallism). We investigated the issue in three pathogenic fungal relatives: Pneumocystis jirovecii, which causes severe pneumonia in immunocompromised humans; Pneumocystis carinii, which infects rats; and the plant pathogen Taphrina deformans. The nature, the number, and the organization within the genome of the genes involved in sexual reproduction were determined. The three species appeared to harbor a single genomic region gathering only three genes involved in sexual differentiation, an organization which is compatible with sexual reproduction involving a single partner. These findings illuminate the strategy adopted by fungal pathogens to infect their hosts.

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Role of an Expanded Inositol Transporter Repertoire in Cryptococcus neoformans Sexual Reproduction and Virulence

mBio ◽

10.1128/mbio.00084-10 ◽

2010 ◽

Vol 1 (1) ◽

Cited By ~ 37

Author(s):

Chaoyang Xue ◽

Tongbao Liu ◽

Lydia Chen ◽

Wenjun Li ◽

Iris Liu ◽

...

Keyword(s):

Central Nervous System ◽

Nervous System ◽

Gene Family ◽

Sexual Reproduction ◽

Cryptococcus Neoformans ◽

Yeast Cells ◽

Sexual Cycle ◽

Fungal Virulence ◽

Content Type ◽

Fungal Meningitis

ABSTRACTCryptococcus neoformansandCryptococcus gattiiare globally distributed human fungal pathogens and the leading causes of fungal meningitis. Recent studies reveal thatmyo-inositol is an important factor for fungal sexual reproduction. ThatC. neoformanscan utilizemyo-inositol as a sole carbon source and the existence of abundant inositol in the human central nervous system suggest that inositol is important forCryptococcusdevelopment and virulence. In accord with this central importance of inositol, an expandedmyo-inositol transporter (ITR) gene family has been identified inCryptococcus. This gene family contains two phylogenetically distinct groups, with a total of 10 or more members inC. neoformansand at least six members in the sibling speciesC. gattii. These inositol transporter genes are differentially expressed under inositol-inducing conditions based on quantitative real-time PCR analyses. Expression ofITRgenes in aSaccharomyces cerevisiaeitr1 itr2mutant lacking inositol transport can complement the slow-growth phenotype of this strain, confirming thatITRgenes arebona fideinositol transporters. Gene mutagenesis studies reveal that the Itr1 and Itr1A transporters are important formyo-inositol stimulation of mating and that functional redundancies among themyo-inositol transporters likely exist. Deletion of the inositol 1-phosphate synthase geneINO1in anitr1oritr1amutant background compromised virulence in a murine inhalation model, indicating the importance of inositol sensing and acquisition for fungal infectivity. Our study provides a platform for further understanding the roles of inositol in fungal physiology and virulence.IMPORTANCECryptococcus neoformansis an AIDS-associated human fungal pathogen that causes over 1 million cases of meningitis annually and is the leading cause of fungal meningitis in immunosuppressed patients. The initial cryptococcal infection is caused predominantly via inhalation of sexual spores or desiccated yeast cells from the environment. How this fungus completes its sexual cycle and produces infectious spores in nature and why it frequently infects the central nervous system to cause fatal meningitis are critical questions that remain to be understood. In this study, we demonstrate that inositol acquisition is important not only for fungal sexual reproduction but also for fungal virulence. We identified an expanded inositol transporter gene family that contains over 10 members, important for both fungal sexual reproduction and virulence. Our work contributes to our understanding of how fungi respond to the environmental inositol availability and its impact on sexual reproduction and virulence.

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Unisexual Reproduction Enhances Fungal Competitiveness by Promoting Habitat Exploration via Hyphal Growth and Sporulation

Eukaryotic Cell ◽

10.1128/ec.00147-13 ◽

2013 ◽

Vol 12 (8) ◽

pp. 1155-1159 ◽

Cited By ~ 16

Author(s):

Sujal S. Phadke ◽

Marianna Feretzaki ◽

Joseph Heitman

Keyword(s):

Mating Type ◽

Wild Type Strain ◽

Hyphal Growth ◽

Pathogenic Fungi ◽

Selective Advantage ◽

Sexual Cycle ◽

Developmental Pathway ◽

Content Type ◽

Human Fungal Pathogen ◽

Unisexual Reproduction

ABSTRACT Unisexual reproduction is a novel homothallic sexual cycle recently discovered in both ascomycetous and basidiomycetous pathogenic fungi. It is a form of selfing that induces the yeast-to-hyphal dimorphic transition in isolates of the α mating type of the human fungal pathogen Cryptococcus neoformans . Unisexual reproduction may benefit the pathogen by facilitating sexual reproduction in the absence of the opposite a mating type and by generating infectious propagules called basidiospores. Here, we report an independent potential selective advantage of unisexual reproduction beyond genetic exchange and recombination. We competed a wild-type strain capable of undergoing unisexual reproduction with mutants defective in this developmental pathway and found that unisexual reproduction provides a considerable dispersal advantage through hyphal growth and sporulation. Our results show that unisexual reproduction may serve to facilitate access to both nutrients and potential mating partners and may provide a means to maintain the capacity for dimorphic transitions in the environment.

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Presence and Functionality of Mating Type Genes in the Supposedly Asexual Filamentous Fungus Aspergillus oryzae

Applied and Environmental Microbiology ◽

10.1128/aem.07034-11 ◽

2012 ◽

Vol 78 (8) ◽

pp. 2819-2829 ◽

Cited By ~ 42

Author(s):

Ryuta Wada ◽

Jun-ichi Maruyama ◽

Haruka Yamaguchi ◽

Nanase Yamamoto ◽

Yutaka Wagu ◽

...

Keyword(s):

Gene Expression ◽

Aspergillus Oryzae ◽

Mating Type ◽

Genetic Manipulation ◽

Gene Replacement ◽

Soy Sauce ◽

Sexual Cycle ◽

Dependent Manner ◽

Content Type ◽

Mating Type Genes

ABSTRACTThe potential for sexual reproduction inAspergillus oryzaewas assessed by investigating the presence and functionality ofMATgenes. Previous genome studies had identified aMAT1-1gene in the reference strain RIB40. We now report the existence of a complementaryMAT1-2gene and the sequencing of an idiomorphic region fromA. oryzaestrain AO6. This allowed the development of a PCR diagnostic assay, which detected isolates of theMAT1-1andMAT1-2genotypes among 180 strains assayed, including industrialtane-kojiisolates. Strains used for sake and miso production showed a near-1:1 ratio of the MAT1-1 and MAT1-2 mating types, whereas strains used for soy sauce production showed a significant bias toward the MAT1-2 mating type. MAT1-1 and MAT1-2 isogenic strains were then created by genetic manipulation of the resident idiomorph, and gene expression was compared by DNA microarray and quantitative real-time PCR (qRT-PCR) methodologies under conditions in whichMATgenes were expressed. Thirty-three genes were found to be upregulated more than 10-fold in either the MAT1-1 host strain or the MAT1-2 gene replacement strain relative to each other, showing that both theMAT1-1andMAT1-2genes functionally regulate gene expression inA. oryzaein a mating type-dependent manner, the first such report for a supposedly asexual fungus.MAT1-1expression specifically upregulated an α-pheromone precursor gene, but the functions of most of the genes affected were unknown. The results are consistent with a heterothallic breeding system inA. oryzae, and prospects for the discovery of a sexual cycle are discussed.

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Basidiomycete Mating Type Genes and Pheromone Signaling

Eukaryotic Cell ◽

10.1128/ec.00319-09 ◽

2010 ◽

Vol 9 (6) ◽

pp. 847-859 ◽

Cited By ~ 102

Author(s):

Marjatta Raudaskoski ◽

Erika Kothe

Keyword(s):

Sexual Reproduction ◽

Mating Type ◽

Schizophyllum Commune ◽

Small Gtpases ◽

Mitogen Activated Protein Kinase ◽

Fruiting Body Formation ◽

Receptor System ◽

Content Type ◽

Discrimination Ability ◽

Mating Type Genes

ABSTRACT The genome sequences of the basidiomycete Agaricomycetes species Coprinopsis cinerea, Laccaria bicolor, Schizophyllum commune, Phanerochaete chrysosporium, and Postia placenta, as well as of Cryptococcus neoformans and Ustilago maydis, are now publicly available. Out of these fungi, C. cinerea, S. commune, and U. maydis, together with the budding yeast Saccharomyces cerevisiae, have been investigated for years genetically and molecularly for signaling in sexual reproduction. The comparison of the structure and organization of mating type genes in fungal genomes reveals an amazing conservation of genes regulating the sexual reproduction throughout the fungal kingdom. In agaricomycetes, two mating type loci, A, coding for homeodomain type transcription factors, and B, encoding a pheromone/receptor system, regulate the four typical mating interactions of tetrapolar species. Evidence for both A and B mating type genes can also be identified in basidiomycetes with bipolar systems, where only two mating interactions are seen. In some of these fungi, the B locus has lost its self/nonself discrimination ability and thus its specificity while retaining the other regulatory functions in development. In silico analyses now also permit the identification of putative components of the pheromone-dependent signaling pathways. Induction of these signaling cascades leads to development of dikaryotic mycelia, fruiting body formation, and meiotic spore production. In pheromone-dependent signaling, the role of heterotrimeric G proteins, components of a mitogen-activated protein kinase (MAPK) cascade, and cyclic AMP-dependent pathways can now be defined. Additionally, the pheromone-dependent signaling through monomeric, small GTPases potentially involved in creating the polarized cytoskeleton for reciprocal nuclear exchange and migration during mating is predicted.

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