Genetic Dissection of Sexual Reproduction in a Primary Homothallic Basidiomycete

Research output: Contribution to journalArticle

5 Citations (Scopus)

Abstract

In fungi belonging to the phylum Basidiomycota, sexual compatibility is usually determined by two genetically unlinked MAT loci, one of which encodes one or more pheromone receptors (P/R) and pheromone precursors, and the other comprehends at least one pair of divergently transcribed genes encoding homeodomain (HD) transcription factors. Most species are heterothallic, meaning that sexual reproduction requires mating between two sexually compatible individuals harboring different alleles at both MAT loci. However, some species are known to be homothallic, one individual being capable of completing the sexual cycle without mating with a genetically distinct partner. While the molecular underpinnings of the heterothallic life cycles of several basidiomycete model species have been dissected in great detail, much less is known concerning the molecular basis for homothallism. Following the discovery in available draft genomes of the homothallic basidiomycetous yeast Phaffia rhodozyma of P/R and HD genes, we employed available genetic tools to determine their role in sexual development. Two P/R clusters, each harboring one pheromone receptor and one pheromone precursor gene were found in close vicinity of each other and were shown to form two redundant P/R pairs, each receptor being activated by the pheromone encoded by the most distal pheromone precursor gene. The HD locus is apparently genetically unlinked to the P/R locus and encodes a single pair of divergently transcribed HD1 and HD2 transcription factors, both required for normal completion of the sexual cycle. Given the genetic makeup of P. rhodozyma MAT loci, we postulate that it is a primarily homothallic organism and we propose a model for the interplay of molecular interactions required for sexual development in this species. Phaffia rhodozyma is considered one of the most promising microbial source of the carotenoid astaxanthin. Further development of this yeast as an industrial organism will benefit from new insights regarding its sexual reproduction system.

Original languageEnglish
Article numbere1006110
JournalPLoS Genetics
Volume12
Issue number6
DOIs
Publication statusPublished - 1 Jun 2016

Fingerprint

Pheromone Receptors
Basidiomycota
chemoreceptors
dissection
sexual reproduction
pheromone
Reproduction
Dissection
Pheromones
pheromones
loci
Sexual Development
sexual development
Genes
Transcription Factors
genes
transcription factors
Yeasts
gene
yeasts

Keywords

  • fungal protein
  • MATING-TYPE LOCUS
  • DENDRORHOUS PHAFFIA-RHODOZYMA
  • CRYPTOCOCCUS-NEOFORMANS
  • HOMEODOMAIN PROTEINS
  • USTILAGO-MAYDIS
  • SACCHAROMYCES-CEREVISIAE
  • UNISEXUAL REPRODUCTION
  • ASPERGILLUS-NIDULANS
  • MOLECULAR EVOLUTION
  • COPRINUS-CINEREUS

Cite this

@article{6fe50ffd062f47ee820f76cd2000d63b,
title = "Genetic Dissection of Sexual Reproduction in a Primary Homothallic Basidiomycete",
abstract = "In fungi belonging to the phylum Basidiomycota, sexual compatibility is usually determined by two genetically unlinked MAT loci, one of which encodes one or more pheromone receptors (P/R) and pheromone precursors, and the other comprehends at least one pair of divergently transcribed genes encoding homeodomain (HD) transcription factors. Most species are heterothallic, meaning that sexual reproduction requires mating between two sexually compatible individuals harboring different alleles at both MAT loci. However, some species are known to be homothallic, one individual being capable of completing the sexual cycle without mating with a genetically distinct partner. While the molecular underpinnings of the heterothallic life cycles of several basidiomycete model species have been dissected in great detail, much less is known concerning the molecular basis for homothallism. Following the discovery in available draft genomes of the homothallic basidiomycetous yeast Phaffia rhodozyma of P/R and HD genes, we employed available genetic tools to determine their role in sexual development. Two P/R clusters, each harboring one pheromone receptor and one pheromone precursor gene were found in close vicinity of each other and were shown to form two redundant P/R pairs, each receptor being activated by the pheromone encoded by the most distal pheromone precursor gene. The HD locus is apparently genetically unlinked to the P/R locus and encodes a single pair of divergently transcribed HD1 and HD2 transcription factors, both required for normal completion of the sexual cycle. Given the genetic makeup of P. rhodozyma MAT loci, we postulate that it is a primarily homothallic organism and we propose a model for the interplay of molecular interactions required for sexual development in this species. Phaffia rhodozyma is considered one of the most promising microbial source of the carotenoid astaxanthin. Further development of this yeast as an industrial organism will benefit from new insights regarding its sexual reproduction system.",
keywords = "fungal protein, MATING-TYPE LOCUS, DENDRORHOUS PHAFFIA-RHODOZYMA, CRYPTOCOCCUS-NEOFORMANS, HOMEODOMAIN PROTEINS, USTILAGO-MAYDIS, SACCHAROMYCES-CEREVISIAE, UNISEXUAL REPRODUCTION, ASPERGILLUS-NIDULANS, MOLECULAR EVOLUTION, COPRINUS-CINEREUS",
author = "M{\'a}rcia David-Palma and Sampaio, {Jos{\'e} Paulo} and Paula Gon{\cc}alves",
note = "Unidade de Ciencias Biomoleculares Aplicadas-UCIBIO from FCT/MEC (UID/Multi/04378/2013); ERDF under the PT2020 Partnership Agreement (POCI-01-0145-FEDER-007728); Fundacao para a Ciencia e a Tecnologia (UID/Multi/04378/2013 ; PTDC/BIA-GEN/112799/2009 ; SFRH/BD/81895/2011).",
year = "2016",
month = "6",
day = "1",
doi = "10.1371/journal.pgen.1006110",
language = "English",
volume = "12",
journal = "PLoS Genetics",
issn = "1553-7390",
publisher = "PUBLIC LIBRARY SCIENCE",
number = "6",

}

Genetic Dissection of Sexual Reproduction in a Primary Homothallic Basidiomycete. / David-Palma, Márcia; Sampaio, José Paulo; Gonçalves, Paula.

In: PLoS Genetics, Vol. 12, No. 6, e1006110, 01.06.2016.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Genetic Dissection of Sexual Reproduction in a Primary Homothallic Basidiomycete

AU - David-Palma, Márcia

AU - Sampaio, José Paulo

AU - Gonçalves, Paula

N1 - Unidade de Ciencias Biomoleculares Aplicadas-UCIBIO from FCT/MEC (UID/Multi/04378/2013); ERDF under the PT2020 Partnership Agreement (POCI-01-0145-FEDER-007728); Fundacao para a Ciencia e a Tecnologia (UID/Multi/04378/2013 ; PTDC/BIA-GEN/112799/2009 ; SFRH/BD/81895/2011).

PY - 2016/6/1

Y1 - 2016/6/1

N2 - In fungi belonging to the phylum Basidiomycota, sexual compatibility is usually determined by two genetically unlinked MAT loci, one of which encodes one or more pheromone receptors (P/R) and pheromone precursors, and the other comprehends at least one pair of divergently transcribed genes encoding homeodomain (HD) transcription factors. Most species are heterothallic, meaning that sexual reproduction requires mating between two sexually compatible individuals harboring different alleles at both MAT loci. However, some species are known to be homothallic, one individual being capable of completing the sexual cycle without mating with a genetically distinct partner. While the molecular underpinnings of the heterothallic life cycles of several basidiomycete model species have been dissected in great detail, much less is known concerning the molecular basis for homothallism. Following the discovery in available draft genomes of the homothallic basidiomycetous yeast Phaffia rhodozyma of P/R and HD genes, we employed available genetic tools to determine their role in sexual development. Two P/R clusters, each harboring one pheromone receptor and one pheromone precursor gene were found in close vicinity of each other and were shown to form two redundant P/R pairs, each receptor being activated by the pheromone encoded by the most distal pheromone precursor gene. The HD locus is apparently genetically unlinked to the P/R locus and encodes a single pair of divergently transcribed HD1 and HD2 transcription factors, both required for normal completion of the sexual cycle. Given the genetic makeup of P. rhodozyma MAT loci, we postulate that it is a primarily homothallic organism and we propose a model for the interplay of molecular interactions required for sexual development in this species. Phaffia rhodozyma is considered one of the most promising microbial source of the carotenoid astaxanthin. Further development of this yeast as an industrial organism will benefit from new insights regarding its sexual reproduction system.

AB - In fungi belonging to the phylum Basidiomycota, sexual compatibility is usually determined by two genetically unlinked MAT loci, one of which encodes one or more pheromone receptors (P/R) and pheromone precursors, and the other comprehends at least one pair of divergently transcribed genes encoding homeodomain (HD) transcription factors. Most species are heterothallic, meaning that sexual reproduction requires mating between two sexually compatible individuals harboring different alleles at both MAT loci. However, some species are known to be homothallic, one individual being capable of completing the sexual cycle without mating with a genetically distinct partner. While the molecular underpinnings of the heterothallic life cycles of several basidiomycete model species have been dissected in great detail, much less is known concerning the molecular basis for homothallism. Following the discovery in available draft genomes of the homothallic basidiomycetous yeast Phaffia rhodozyma of P/R and HD genes, we employed available genetic tools to determine their role in sexual development. Two P/R clusters, each harboring one pheromone receptor and one pheromone precursor gene were found in close vicinity of each other and were shown to form two redundant P/R pairs, each receptor being activated by the pheromone encoded by the most distal pheromone precursor gene. The HD locus is apparently genetically unlinked to the P/R locus and encodes a single pair of divergently transcribed HD1 and HD2 transcription factors, both required for normal completion of the sexual cycle. Given the genetic makeup of P. rhodozyma MAT loci, we postulate that it is a primarily homothallic organism and we propose a model for the interplay of molecular interactions required for sexual development in this species. Phaffia rhodozyma is considered one of the most promising microbial source of the carotenoid astaxanthin. Further development of this yeast as an industrial organism will benefit from new insights regarding its sexual reproduction system.

KW - fungal protein

KW - MATING-TYPE LOCUS

KW - DENDRORHOUS PHAFFIA-RHODOZYMA

KW - CRYPTOCOCCUS-NEOFORMANS

KW - HOMEODOMAIN PROTEINS

KW - USTILAGO-MAYDIS

KW - SACCHAROMYCES-CEREVISIAE

KW - UNISEXUAL REPRODUCTION

KW - ASPERGILLUS-NIDULANS

KW - MOLECULAR EVOLUTION

KW - COPRINUS-CINEREUS

UR - http://www.scopus.com/inward/record.url?scp=84977551125&partnerID=8YFLogxK

U2 - 10.1371/journal.pgen.1006110

DO - 10.1371/journal.pgen.1006110

M3 - Article

VL - 12

JO - PLoS Genetics

JF - PLoS Genetics

SN - 1553-7390

IS - 6

M1 - e1006110

ER -