Molecular and Genetic Evidence for a Tetrapolar Mating System in the Basidiomycetous Yeast Kwoniella mangrovensis and Two Novel Sibling Species

Guerreiro, Marco Alexandre; Springer, Deborah J.; Rodrigues, Joana A.; Rusché, Laura N.; Findley, Keisha; Heitman, Joseph; Fonseca, Álvaro

doi:10.1128/ec.00065-13

Cited by 23 publications

(33 citation statements)

References 39 publications

(86 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Moreover, we identified a gene encoding a p21-activated kinase ( STE20 ) in the vicinity of the STE3-2 gene, which is consistent with observations in other basidiomycetes, viz. species of the pathogenic Cryptococcus neoformans complex [50] and of the sensu lato Kwoniella clade [51] in Tremellales (Agaricomycotina), as well as in yeast species in the Pucciniomycotina [52, 53]. A final set of orthologs encoding transcription factors that have key roles in mating in S. cerevisiae (Ste12) [54], C. neoformans (Mat2 and Znf2) [55], and U. maydis (Prf1) [56] were also found and are listed in Additional file 4: Table S4.…”

Section: Resultsmentioning

confidence: 99%

Comparative genomics provides new insights into the diversity, physiology, and sexuality of the only industrially exploited tremellomycete: Phaffia rhodozyma

et al. 2016

View full text Add to dashboard Cite

BackgroundThe class Tremellomycete (Agaricomycotina) encompasses more than 380 fungi. Although there are a few edible Tremella spp., the only species with current biotechnological use is the astaxanthin-producing yeast Phaffia rhodozyma (Cystofilobasidiales). Besides astaxanthin, a carotenoid pigment with potent antioxidant activity and great value for aquaculture and pharmaceutical industries, P. rhodozyma possesses multiple exceptional traits of fundamental and applied interest. The aim of this study was to obtain, and analyze two new genome sequences of representative strains from the northern (CBS 7918T, the type strain) and southern hemispheres (CRUB 1149) and compre them to a previously published genome sequence (strain CBS 6938). Photoprotection and antioxidant related genes, as well as genes involved in sexual reproduction were analyzed.ResultsBoth genomes had ca. 19 Mb and 6000 protein coding genes, similar to CBS 6938. Compared to other fungal genomes P. rhodozyma strains and other Cystofilobasidiales have the highest number of intron-containing genes and highest number of introns per gene. The Patagonian strain showed 4.4 % of nucleotide sequence divergence compared to the European strains which differed from each other by only 0.073 %. All known genes related to the synthesis of astaxanthin were annotated. A hitherto unknown gene cluster potentially responsible for photoprotection (mycosporines) was found in the newly sequenced P. rhodozyma strains but was absent in the non-mycosporinogenic strain CBS 6938. A broad battery of enzymes that act as scavengers of free radical oxygen species were detected, including catalases and superoxide dismutases (SODs). Additionally, genes involved in sexual reproduction were found and annotated.ConclusionsA draft genome sequence of the type strain of P. rhodozyma is now available, and comparison with that of the Patagonian population suggests the latter deserves to be assigned to a distinct variety. An unexpected genetic trait regarding high occurrence of introns in P. rhodozyma and other Cystofilobasidiales was revealed. New genomic insights into fungal homothallism were also provided. The genetic basis of several additional photoprotective and antioxidant strategies were described, indicating that P. rhodozyma is one of the fungi most well-equipped to cope with environmental oxidative stress, a factor that has probably contributed to shaping its genome.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-3244-7) contains supplementary material, which is available to authorized users.

show abstract

Section: Resultsmentioning

confidence: 99%

Comparative genomics provides new insights into the diversity, physiology, and sexuality of the only industrially exploited tremellomycete: Phaffia rhodozyma

et al. 2016

View full text Add to dashboard Cite

show abstract

“…Of the three genes, only STE12 is expected to have a mating-related role in L. scottii since homologs of this gene were shown to function as master regulators of the pheromone/receptor-signaling pathway in other fungal species (Sprague and Thorner 1992;Zarnack et al 2008;Jones and Bennett 2011). In C. neoformans, C. amylolentus, and K. mangrovensis, STE12 alleles are matingtype-specific (Findley et al 2009;Guerreiro et al 2013) and, in the former species, this gene is involved in morphogenesis, virulence, and ecological fitness (Chang et al 2001). The presence of STE12 in only one mating type in L. scottii could suggest that it may specifically function during postmating development, but this finding is also consistent with previous observations in the red yeast R. toruloides that the initiation of the conjugation tube formation occurs earlier and to a greater extent in cells of one of the mating types (Abe et al 1975).…”

Section: Resultsmentioning

confidence: 99%

“…Studies with a similar scope on other tetrapolar species (viz. K. mangrovensis, K. heveanensis, Cryptococcus flavescens, and C. terrestris (Tremellales, Agaricomycotina) (Metin et al 2010;Guerreiro et al 2013;Yurkov et al 2015) readily detected arbitrary assortment of MAT alleles, even within a more restricted number of isolates. Although we cannot rule out that other mechanisms may cause the apparent nonrandom association between P/R (A) and HD (B) loci in L. scottii, we highlight two possibilities in particular.…”

Section: Mat Allele Diversity In the L Scottii Species Complexmentioning

confidence: 99%

“…Interestingly, most of the known tetrapolar yeast species exhibit a biallelic P/R locus and a multiallelic HD locus (viz. Ustilago maydis, Kwoniella heveanensis, Kwoniella mangrovensis, Cryptococcus amylolentus) (Bölker et al 1992;Kämper et al 1995;Metin et al 2010;Findley et al 2012;Guerreiro et al 2013), a configuration originally designated as "modified tetrapolar" by Robert J. Bandoni to denote that outcrossing in such a system cannot exceed 50% (Bandoni 1963;Kües et al 2011). Indeed, only by evolving multiple alleles at both MAT loci can a tetrapolar system maximize the outcrossing efficiency to .50%, as observed in mushroomforming species (viz.…”

mentioning

confidence: 99%

See 1 more Smart Citation

Evolution of Mating Systems in Basidiomycetes and the Genetic Architecture Underlying Mating-Type Determination in the YeastLeucosporidium scottii

et al. 2015

View full text Add to dashboard Cite

In most fungi, sexual reproduction is bipolar; that is, two alternate sets of genes at a single mating-type (MAT) locus determine two mating types. However, in the Basidiomycota, a unique (tetrapolar) reproductive system emerged in which sexual identity is governed by two unlinked MAT loci, each of which controls independent mechanisms of self/nonself recognition. Tetrapolar-to-bipolar transitions have occurred on multiple occasions in the Basidiomycota, resulting, for example, from linkage of the two MAT loci into a single inheritable unit. Nevertheless, owing to the scarcity of molecular data regarding tetrapolar systems in the earliest-branching lineage of the Basidiomycota (subphylum Pucciniomycotina), it is presently unclear if the last common ancestor was tetrapolar or bipolar. Here, we address this question, by investigating the mating system of the Pucciniomycotina yeast Leucosporidium scottii. Using whole-genome sequencing and chromoblot analysis, we discovered that sexual reproduction is governed by two physically unlinked gene clusters: a multiallelic homeodomain (HD) locus and a pheromone/receptor (P/R) locus that is biallelic, thereby dismissing the existence of a third P/R allele as proposed earlier. Allele distribution of both MAT genes in natural populations showed that the two loci were in strong linkage disequilibrium, but independent assortment of MAT alleles was observed in the meiotic progeny of a test cross. The sexual cycle produces fertile progeny with similar proportions of the four mating types, but approximately 2/3 of the progeny was found to be nonhaploid. Our study adds to others in reinforcing tetrapolarity as the ancestral state of all basidiomycetes.KEYWORDS sexual reproduction; mating type; mating-type determination; fungi; Basidiomycota S EXUAL reproduction has a pivotal role in the biology of many eukaryotes and is likely a defining evolutionary innovation of this lineage (Dacks and Roger 1999;Goodenough and Heitman 2014). In addition to promoting genetic variation, required for adaptation to fluctuating environments and longterm survival, sexual reproduction in many fungal species, in particular, has a central role in pathogenic development (Bakkeren et al. 2008;Nadal et al. 2008;Heitman 2010;Heitman et al. 2014). It is thus not surprising that recent advances in genome sequencing have revealed that most fungal species have retained the machinery for sexual reproduction and meiosis (Halary et al. 2011;Dyer and O'Gorman 2012;Gioti et al. 2013;Heitman et al. 2014). However, this resilience to keep sexual competence intact comes with an extremely dynamic evolution of sexual behaviors and mating type-determining mechanisms, which may influence important evolutionary and ecological processes, such as adaptation and speciation (Billiard et al. 2011;Heitman et al. 2013;Nieuwenhuis et al. 2013).In the phylum Basidiomycota, sexual reproduction is often dictated by two independent sets of mating-type (MAT)-specific genes that control different stages of the sexual cycle. These...

show abstract

“…From an evolutionary standpoint, it is noteworthy that extant tetrapolar dimorphic basidiomycetes have more commonly a biallelic P/R locus (26, 70–72, 74, 78). For these, the proportion of compatible mates in the population cannot exceed 50%, irrespective of the number of alleles at the HD locus.…”

Section: Breeding Systems In the Basidiomycotamentioning

confidence: 99%

Fungal Sex: The Basidiomycota

et al. 2017

View full text Add to dashboard Cite

SUMMARY 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, co-segregation 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 mating types that may number 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.

show abstract

Molecular and Genetic Evidence for a Tetrapolar Mating System in the Basidiomycetous Yeast Kwoniella mangrovensis and Two Novel Sibling Species

Cited by 23 publications

References 39 publications

Comparative genomics provides new insights into the diversity, physiology, and sexuality of the only industrially exploited tremellomycete: Phaffia rhodozyma

Comparative genomics provides new insights into the diversity, physiology, and sexuality of the only industrially exploited tremellomycete: Phaffia rhodozyma

Evolution of Mating Systems in Basidiomycetes and the Genetic Architecture Underlying Mating-Type Determination in the YeastLeucosporidium scottii

Fungal Sex: The Basidiomycota

Contact Info

Product

Resources

About