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Fungal Sex: The Basidiomycota

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  • Authors: Marco A. Coelho1, Guus Bakkeren2, Sheng Sun3, Michael E. Hood4, Tatiana Giraud5
  • Editors: Joseph Heitman6, Neil A. R. Gow7
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: UCIBIO-REQUIMTE, Departamento de Ciências da Vida, Faculdade de Ciências e Tecnologia, Universidade NOVA de Lisboa, 2829-516 Caparica, Portugal; 2: Agriculture and Agri-Food Canada, Summerland Research and Development Centre, Summerland, BC, V0H 1Z0, Canada; 3: Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710; 4: Department of Biology, Amherst College, Amherst, MA 01002; 5: Ecologie Systématique Evolution, Univ. Paris-Sud, CNRS, AgroParisTech, Université Paris-Saclay, 91400, Orsay, France; 6: Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710; 7: School of Medical Sciences, University of Aberdeen, Fosterhill, Aberdeen, AB25 2ZD, United Kingdom
    • Source: microbiolspec June 2017 vol. 5 no. 3 doi:10.1128/microbiolspec.FUNK-0046-2016
  • Received 14 February 2016 Accepted 02 March 2017 Published 09 June 2017
  • Marco A. Coelho [email protected]
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  • Abstract:

    Fungi of the Basidiomycota, representing major pathogen lineages and mushroom-forming species, exhibit diverse means to achieve sexual reproduction, with particularly varied mechanisms to determine compatibilities of haploid mating partners. For species that require mating between distinct genotypes, discrimination is usually based on both the reciprocal exchange of diffusible mating pheromones, rather than sexes, and the interactions of homeodomain protein signals after cell fusion. Both compatibility factors must be heterozygous in the product of mating, and genetic linkage relationships of the mating pheromone/receptor and homeodomain genes largely determine the complex patterns of mating-type variation. Independent segregation of the two compatibility factors can create four haploid mating genotypes from meiosis, referred to as tetrapolarity. This condition is thought to be ancestral to the basidiomycetes. Alternatively, cosegregation by linkage of the two mating factors, or in some cases the absence of the pheromone-based discrimination, yields only two mating types from meiosis, referred to as bipolarity. Several species are now known to have large and highly rearranged chromosomal regions linked to mating-type genes. At the population level, polymorphism of the mating-type genes is an exceptional aspect of some basidiomycete fungi, where selection under outcrossing for rare, intercompatible allelic variants is thought to be responsible for numbers of mating types that may reach several thousand. Advances in genome sequencing and assembly are yielding new insights by comparative approaches among and within basidiomycete species, with the promise to resolve the evolutionary origins and dynamics of mating compatibility genetics in this major eukaryotic lineage.

  • Citation: Coelho M, Bakkeren G, Sun S, Hood M, Giraud T. 2017. Fungal Sex: The Basidiomycota. Microbiol Spectrum 5(3):FUNK-0046-2016. doi:10.1128/microbiolspec.FUNK-0046-2016.

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2017-06-09
2019-08-20

Abstract:

Fungi of the Basidiomycota, representing major pathogen lineages and mushroom-forming species, exhibit diverse means to achieve sexual reproduction, with particularly varied mechanisms to determine compatibilities of haploid mating partners. For species that require mating between distinct genotypes, discrimination is usually based on both the reciprocal exchange of diffusible mating pheromones, rather than sexes, and the interactions of homeodomain protein signals after cell fusion. Both compatibility factors must be heterozygous in the product of mating, and genetic linkage relationships of the mating pheromone/receptor and homeodomain genes largely determine the complex patterns of mating-type variation. Independent segregation of the two compatibility factors can create four haploid mating genotypes from meiosis, referred to as tetrapolarity. This condition is thought to be ancestral to the basidiomycetes. Alternatively, cosegregation by linkage of the two mating factors, or in some cases the absence of the pheromone-based discrimination, yields only two mating types from meiosis, referred to as bipolarity. Several species are now known to have large and highly rearranged chromosomal regions linked to mating-type genes. At the population level, polymorphism of the mating-type genes is an exceptional aspect of some basidiomycete fungi, where selection under outcrossing for rare, intercompatible allelic variants is thought to be responsible for numbers of mating types that may reach several thousand. Advances in genome sequencing and assembly are yielding new insights by comparative approaches among and within basidiomycete species, with the promise to resolve the evolutionary origins and dynamics of mating compatibility genetics in this major eukaryotic lineage.

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Fungal Sex: The Basidiomycota
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Citation: Coelho M, Bakkeren G, Sun S, Hood M, Giraud T. 2017. Fungal sex: the basidiomycota. microbiolspec 5(3): doi:10.1128/microbiolspec.FUNK-0046-2016
/content/microbiolspec/10.1128/microbiolspec.FUNK-0046-2016.fig1
FIGURE 1
General life cycles of dimorphic and mushroom-forming basidiomycetes. Three basidiomycetes are pictured where sexual reproduction and a dimorphic switch between a yeast cell and a hyphal form are crucial to infection of plant (A, B) or animal (C) hosts. The haploid yeast forms of the maize smut (A) and the anther smut spp. (B) are nonpathogenic and can undergo asexual mitotic vegetative growth. In , the yeast stage is, however, short-lived because mating occurs mostly between cells within the same tetrad. Upon mating with a compatible partner, both fungi switch to an enduring infection hyphal form (dikaryon; n + n) that can invade the host plant. Proliferation and differentiation of in the plant culminates with the production of masses of wind-dispersing diploid spores (teliospores; 2n) in large tumor-like tissues, whereas in , teliospores are formed in the anthers of infected flowers and transmitted by pollinators onto healthy plants. In the case of , the single-celled yeast form may be free-living or mycoparasitic. A similar dimorphic switch occurs upon mating of yeast cells of opposite mating type ( or α), ultimately resulting in the infectious propagules (basidiospores) that potentially infect an animal host after dispersal. These infectious structures may also be generated by haploid selfing (depicted with gray background), where fusion occurs between homothallic cells carrying identical alleles (α/α diploid is depicted) and form monokaryotic hyphae with unfused clamp connections (see text for details). In mushroom-forming fungi such as , germination of haploid spores yields haploid monokaryons capable of independent growth. When two compatible monokaryons meet, a fertile clamped dikaryon is formed which develops into fruiting bodies (mushrooms) triggered upon suitable environmental cues, where basidia arise. In all these and other basidiomycetes, nuclear fusion (karyogamy) is usually delayed until the formation of basidia (or teliospores). Meiosis ensues, generating four haploid nuclei, which give rise to basidiospores to complete the cycle. Adapted from Morrow and Fraser ( 2 ) and Nieuwenhuis et al. ( 17 ) with permission of the publishers.
microbiolspec/5/3/FUNK-0046-2016-fig1_thmb.gif
microbiolspec/5/3/FUNK-0046-2016-fig1.gif
Image of FIGURE 1
FIGURE 1

General life cycles of dimorphic and mushroom-forming basidiomycetes. Three basidiomycetes are pictured where sexual reproduction and a dimorphic switch between a yeast cell and a hyphal form are crucial to infection of plant (A, B) or animal (C) hosts. The haploid yeast forms of the maize smut (A) and the anther smut spp. (B) are nonpathogenic and can undergo asexual mitotic vegetative growth. In , the yeast stage is, however, short-lived because mating occurs mostly between cells within the same tetrad. Upon mating with a compatible partner, both fungi switch to an enduring infection hyphal form (dikaryon; n + n) that can invade the host plant. Proliferation and differentiation of in the plant culminates with the production of masses of wind-dispersing diploid spores (teliospores; 2n) in large tumor-like tissues, whereas in , teliospores are formed in the anthers of infected flowers and transmitted by pollinators onto healthy plants. In the case of , the single-celled yeast form may be free-living or mycoparasitic. A similar dimorphic switch occurs upon mating of yeast cells of opposite mating type ( or α), ultimately resulting in the infectious propagules (basidiospores) that potentially infect an animal host after dispersal. These infectious structures may also be generated by haploid selfing (depicted with gray background), where fusion occurs between homothallic cells carrying identical alleles (α/α diploid is depicted) and form monokaryotic hyphae with unfused clamp connections (see text for details). In mushroom-forming fungi such as , germination of haploid spores yields haploid monokaryons capable of independent growth. When two compatible monokaryons meet, a fertile clamped dikaryon is formed which develops into fruiting bodies (mushrooms) triggered upon suitable environmental cues, where basidia arise. In all these and other basidiomycetes, nuclear fusion (karyogamy) is usually delayed until the formation of basidia (or teliospores). Meiosis ensues, generating four haploid nuclei, which give rise to basidiospores to complete the cycle. Adapted from Morrow and Fraser ( 2 ) and Nieuwenhuis et al. ( 17 ) with permission of the publishers.

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FIGURE 2
Phylogeny of the Basidiomycota indicating the breeding system and the number of genes across representative species of the three subphyla. The breeding system and the different taxonomic lineages are color-coded as given in the key and are kept consistent in all figures. Gene numbers shown for each species were obtained either from previous reports ( 20 , 41 , 100 ) or from newly surveyed genome data (marked with a hash sign after the species name). In the Agaricomycetes, values shown in parentheses are putative non-mating-type pheromone receptors. A question mark indicates cases where information on the breeding system is not available or is uncertain (e.g., because the sexual stage of a species is unknown). A schematic representation of the and loci is given in Fig. 3 for representative species of each lineage marked with numbers enclosed in white circles. Letters in superscript next to the number of pheromone precursor genes indicate that (a) all genes encode the same mature pheromone peptide or that (b) no CAAX motif was detected in one of the putative pheromone precursors. The species phylogenetic tree was constructed in IQ-TREE ( 193 ) using a previously described approach ( 194 ). Branch support values are shown in the tree nodes as given in the key and were assessed with the ultrafast bootstrap approximation (UFBoot) and the approximate likelihood ratio test (SH-aLRT), each with 1,000 replicates. The basidiomycete clade is rooted with sequences from Ascomycete fungi.
microbiolspec/5/3/FUNK-0046-2016-fig2_thmb.gif
microbiolspec/5/3/FUNK-0046-2016-fig2.gif
Image of FIGURE 2
FIGURE 2

Phylogeny of the Basidiomycota indicating the breeding system and the number of genes across representative species of the three subphyla. The breeding system and the different taxonomic lineages are color-coded as given in the key and are kept consistent in all figures. Gene numbers shown for each species were obtained either from previous reports ( 20 , 41 , 100 ) or from newly surveyed genome data (marked with a hash sign after the species name). In the Agaricomycetes, values shown in parentheses are putative non-mating-type pheromone receptors. A question mark indicates cases where information on the breeding system is not available or is uncertain (e.g., because the sexual stage of a species is unknown). A schematic representation of the and loci is given in Fig. 3 for representative species of each lineage marked with numbers enclosed in white circles. Letters in superscript next to the number of pheromone precursor genes indicate that (a) all genes encode the same mature pheromone peptide or that (b) no CAAX motif was detected in one of the putative pheromone precursors. The species phylogenetic tree was constructed in IQ-TREE ( 193 ) using a previously described approach ( 194 ). Branch support values are shown in the tree nodes as given in the key and were assessed with the ultrafast bootstrap approximation (UFBoot) and the approximate likelihood ratio test (SH-aLRT), each with 1,000 replicates. The basidiomycete clade is rooted with sequences from Ascomycete fungi.

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FIGURE 3a
Schematic showing the genomic structure and diversity of loci in representative basidiomycete lineages. The genomic organization of the homeodomain () and pheromone/receptor () loci is shown for selected species of the Agaricomycotina and the Ustilaginomycotina and Pucciniomycotina. Arrows indicate genes and their direction of transcription. Putative loci are shaded in light brown, and genes are colored as indicated in the key with different color grades representing different alleles (or paralogs). When known, conserved genes flanking loci (colored light yellow or light blue) are shown within each lineage. Genes that encode components of the pheromone response pathway are shown in pink and are in many cases within the locus. Putative homologs of a protein required for posttranslational modification of pheromone precursors (isoprenyl cysteine methyltransferase [ICMT]) are colored purple and appear near the locus in some species. loci no longer determining mating-type specificity in bipolar Agaricomycetes are depicted with a gray background. In , the two mating-type chromosomes are highly rearranged and enriched in transposable elements, so that only a small number of genes is depicted. Of note, whereas in and genes are far apart on the same chromosome, in and the two sets of genes are closer together. Other genes or genomic features are colored or represented as given in the key. For citations and additional details, see text. Gene names or their associated protein accession numbers are shown as they appear in their respective genome databases, except in species of Ustilaginomycotina and Tremellomycetes, where names were given based on sequence identity to the closest homolog in and , respectively.
microbiolspec/5/3/FUNK-0046-2016-fig3a_thmb.gif
microbiolspec/5/3/FUNK-0046-2016-fig3a.gif
Image of FIGURE 3a
FIGURE 3a

Schematic showing the genomic structure and diversity of loci in representative basidiomycete lineages. The genomic organization of the homeodomain () and pheromone/receptor () loci is shown for selected species of the Agaricomycotina and the Ustilaginomycotina and Pucciniomycotina. Arrows indicate genes and their direction of transcription. Putative loci are shaded in light brown, and genes are colored as indicated in the key with different color grades representing different alleles (or paralogs). When known, conserved genes flanking loci (colored light yellow or light blue) are shown within each lineage. Genes that encode components of the pheromone response pathway are shown in pink and are in many cases within the locus. Putative homologs of a protein required for posttranslational modification of pheromone precursors (isoprenyl cysteine methyltransferase [ICMT]) are colored purple and appear near the locus in some species. loci no longer determining mating-type specificity in bipolar Agaricomycetes are depicted with a gray background. In , the two mating-type chromosomes are highly rearranged and enriched in transposable elements, so that only a small number of genes is depicted. Of note, whereas in and genes are far apart on the same chromosome, in and the two sets of genes are closer together. Other genes or genomic features are colored or represented as given in the key. For citations and additional details, see text. Gene names or their associated protein accession numbers are shown as they appear in their respective genome databases, except in species of Ustilaginomycotina and Tremellomycetes, where names were given based on sequence identity to the closest homolog in and , respectively.

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FIGURE 3b
Schematic showing the genomic structure and diversity of loci in representative basidiomycete lineages. The genomic organization of the homeodomain () and pheromone/receptor () loci is shown for selected species of the Agaricomycotina and the Ustilaginomycotina and Pucciniomycotina. Arrows indicate genes and their direction of transcription. Putative loci are shaded in light brown, and genes are colored as indicated in the key with different color grades representing different alleles (or paralogs). When known, conserved genes flanking loci (colored light yellow or light blue) are shown within each lineage. Genes that encode components of the pheromone response pathway are shown in pink and are in many cases within the locus. Putative homologs of a protein required for posttranslational modification of pheromone precursors (isoprenyl cysteine methyltransferase [ICMT]) are colored purple and appear near the locus in some species. loci no longer determining mating-type specificity in bipolar Agaricomycetes are depicted with a gray background. In , the two mating-type chromosomes are highly rearranged and enriched in transposable elements, so that only a small number of genes is depicted. Of note, whereas in and genes are far apart on the same chromosome, in and the two sets of genes are closer together. Other genes or genomic features are colored or represented as given in the key. For citations and additional details, see text. Gene names or their associated protein accession numbers are shown as they appear in their respective genome databases, except in species of Ustilaginomycotina and Tremellomycetes, where names were given based on sequence identity to the closest homolog in and , respectively.
microbiolspec/5/3/FUNK-0046-2016-fig3b_thmb.gif
microbiolspec/5/3/FUNK-0046-2016-fig3b.gif
Image of FIGURE 3b
FIGURE 3b

Schematic showing the genomic structure and diversity of loci in representative basidiomycete lineages. The genomic organization of the homeodomain () and pheromone/receptor () loci is shown for selected species of the Agaricomycotina and the Ustilaginomycotina and Pucciniomycotina. Arrows indicate genes and their direction of transcription. Putative loci are shaded in light brown, and genes are colored as indicated in the key with different color grades representing different alleles (or paralogs). When known, conserved genes flanking loci (colored light yellow or light blue) are shown within each lineage. Genes that encode components of the pheromone response pathway are shown in pink and are in many cases within the locus. Putative homologs of a protein required for posttranslational modification of pheromone precursors (isoprenyl cysteine methyltransferase [ICMT]) are colored purple and appear near the locus in some species. loci no longer determining mating-type specificity in bipolar Agaricomycetes are depicted with a gray background. In , the two mating-type chromosomes are highly rearranged and enriched in transposable elements, so that only a small number of genes is depicted. Of note, whereas in and genes are far apart on the same chromosome, in and the two sets of genes are closer together. Other genes or genomic features are colored or represented as given in the key. For citations and additional details, see text. Gene names or their associated protein accession numbers are shown as they appear in their respective genome databases, except in species of Ustilaginomycotina and Tremellomycetes, where names were given based on sequence identity to the closest homolog in and , respectively.

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FIGURE 4
Phylogeny of Basidiomycota pheromone receptor proteins. Amino acid sequences identified by BLAST from publicly available databases or from genome projects were retrieved for representative species of the tree subphyla of the Basidiomycota. A total of 106 sequences were manually inspected, amended where necessary, and aligned with MAFFT ( 195 ), and poorly aligned regions were trimmed with trimAl ( 196 ). The phylogenetic tree and branch support were obtained as in Fig. 2 , and the tree was rooted with Ste3p. GenBank accession numbers (*), Joint Genome Institute protein identifiers (**), and RIKEN/NBRP identifiers (***) are given after the strain name, with letters in superscript indicating (a) genomes assembled from available raw sequencing data and inspected locally, (b) genomic contigs/scaffolds lacking gene annotation, and (c) genes whose annotation was corrected. Species highlighted in boldface are shown in Fig. 3 , with arrows before their names indicating the allelic version (or paralog) of the pheromone receptor as colored in Fig. 3 . Of note, the and alleles in the Microbotryomycetes (Pucciniomycotina) displayed the deepest allelic divergence and trans-specific polymorphism, with the alleles of the different species branching together rather than each of these alleles clustering with the allele from the same species ( 42 , 45 , 137 ).
microbiolspec/5/3/FUNK-0046-2016-fig4_thmb.gif
microbiolspec/5/3/FUNK-0046-2016-fig4.gif
Image of FIGURE 4
FIGURE 4

Phylogeny of Basidiomycota pheromone receptor proteins. Amino acid sequences identified by BLAST from publicly available databases or from genome projects were retrieved for representative species of the tree subphyla of the Basidiomycota. A total of 106 sequences were manually inspected, amended where necessary, and aligned with MAFFT ( 195 ), and poorly aligned regions were trimmed with trimAl ( 196 ). The phylogenetic tree and branch support were obtained as in Fig. 2 , and the tree was rooted with Ste3p. GenBank accession numbers (*), Joint Genome Institute protein identifiers (**), and RIKEN/NBRP identifiers (***) are given after the strain name, with letters in superscript indicating (a) genomes assembled from available raw sequencing data and inspected locally, (b) genomic contigs/scaffolds lacking gene annotation, and (c) genes whose annotation was corrected. Species highlighted in boldface are shown in Fig. 3 , with arrows before their names indicating the allelic version (or paralog) of the pheromone receptor as colored in Fig. 3 . Of note, the and alleles in the Microbotryomycetes (Pucciniomycotina) displayed the deepest allelic divergence and trans-specific polymorphism, with the alleles of the different species branching together rather than each of these alleles clustering with the allele from the same species ( 42 , 45 , 137 ).

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FIGURE 5
Roles of and genes on the formation and maintenance of the dikaryon in . Pheromone signaling is not required to attract mates, and hyphal fusion is mating-type independent (diagram 1). Upon fusion, nuclei enter the mycelium of the other mate and migrate until they reach a hyphal tip cell (diagram 2). During hyphal tip elongation, the two types of haploid nuclei (depicted in white and black, representing different genotypes) pair at the tip cell (diagram 3), and at the place where mitosis will take place, a hook-like structure (called a clamp connection) is formed (diagram 4). The two nuclei divide synchronously: one of the nuclei divides in the direction of the clamp cell that is growing backward toward the main hyphae, while the other divides along the main hyphal axis (diagram 5). Septa are generated between the dividing nuclei. This way one nucleus stays temporarily entrapped in the clamp cell, one nucleus of the other type is enclosed in the newly formed subapical cell, and a nucleus of each type is maintained in the emerging hyphal tip cell (diagram 6). The clamp cell fuses with the subapical cell and releases the entrapped nucleus from the clamp cell, restoring the dikaryotic state of the subapical cell (diagram 7). In , steps controlled by (diagrams 2 and 7) and (diagrams 3 to 6) genes are colored red and green, respectively. See Casselton et al. ( 18 ) and Kües ( 90 ) for details. The micrograph at the bottom was obtained from Stajich et al. ( 86 ), with permission.
microbiolspec/5/3/FUNK-0046-2016-fig5_thmb.gif
microbiolspec/5/3/FUNK-0046-2016-fig5.gif
Image of FIGURE 5
FIGURE 5

Roles of and genes on the formation and maintenance of the dikaryon in . Pheromone signaling is not required to attract mates, and hyphal fusion is mating-type independent (diagram 1). Upon fusion, nuclei enter the mycelium of the other mate and migrate until they reach a hyphal tip cell (diagram 2). During hyphal tip elongation, the two types of haploid nuclei (depicted in white and black, representing different genotypes) pair at the tip cell (diagram 3), and at the place where mitosis will take place, a hook-like structure (called a clamp connection) is formed (diagram 4). The two nuclei divide synchronously: one of the nuclei divides in the direction of the clamp cell that is growing backward toward the main hyphae, while the other divides along the main hyphal axis (diagram 5). Septa are generated between the dividing nuclei. This way one nucleus stays temporarily entrapped in the clamp cell, one nucleus of the other type is enclosed in the newly formed subapical cell, and a nucleus of each type is maintained in the emerging hyphal tip cell (diagram 6). The clamp cell fuses with the subapical cell and releases the entrapped nucleus from the clamp cell, restoring the dikaryotic state of the subapical cell (diagram 7). In , steps controlled by (diagrams 2 and 7) and (diagrams 3 to 6) genes are colored red and green, respectively. See Casselton et al. ( 18 ) and Kües ( 90 ) for details. The micrograph at the bottom was obtained from Stajich et al. ( 86 ), with permission.

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