Evolution of Multispecific Mating-type Alleles for Pheromone Perception in the Homobasidiomycete Fungi

Overview

Journal Curr Genet

Specialty Genetics

Date 2003 Feb 18

PMID 12589466

Citations 11

Authors

Erika Kothe

Susanne Gola

Jurgen Wendland

Affiliations

Soon will be listed here.

Abstract

The evolution of multiple, independent and multispecific mating-type loci is a feature unique to homobasidiomycete fungi. To propose a model of evolution, data assembled for the wood-rotting fungus Schizophyllum commune were analyzed. In one mating-type locus, pheromone receptors and several pheromones are encoded which have been investigated in some detail and can be used to understand the ligand-receptor interactions and activation of signal transduction which are essential to sexual propagation. Previous models for the evolution of new alleles were complicated and involved three subsequent steps (without selectable phenotype) prior to the establishment of a new stable pheromone-receptor pair. This paper presents a model for the evolution of new specificities by recombination and selection that incorporates the multi-state receptor activation recently established for S. commune, explaining differential responses to different pheromones in one receptor molecule. The model takes into account the occurrence of multiple pheromone genes in each locus and unilateral nuclear donor/acceptor strains that may in nature act as steps in the evolution of new specificities. A second homobasidiomycete fungus, Coprinus cinereus, was similarly characterized at the molecular level. Data acquired in this system support the conclusion that the presented model can be generalized.

Citing Articles

Misconception of Schizophyllum commune strain 20R-7-F01 origin from subseafloor sediments over 20 million years old.

Boiko S Sci Rep. 2025; 15(1):6586.

PMID: 39994251 PMC: 11850871. DOI: 10.1038/s41598-024-84457-2.

What Role Might Non-Mating Receptors Play in ?.

Wirth S, Freihorst D, Krause K, Kothe E J Fungi (Basel). 2021; 7(5).

PMID: 34065484 PMC: 8161036. DOI: 10.3390/jof7050399.

A genetic linkage map of Pleurotus tuoliensis integrated with physical mapping of the de novo sequenced genome and the mating type loci.

Gao W, Qu J, Zhang J, Sonnenberg A, Chen Q, Zhang Y BMC Genomics. 2018; 19(1):18.

PMID: 29304732 PMC: 5755439. DOI: 10.1186/s12864-017-4421-z.

A central role for Ras1 in morphogenesis of the basidiomycete Schizophyllum commune.

Knabe N, Jung E, Freihorst D, Hennicke F, Horton J, Kothe E Eukaryot Cell. 2013; 12(6):941-52.

PMID: 23606288 PMC: 3675993. DOI: 10.1128/EC.00355-12.

Interspecific sex in grass smuts and the genetic diversity of their pheromone-receptor system.

Kellner R, Vollmeister E, Feldbrugge M, Begerow D PLoS Genet. 2012; 7(12):e1002436.

PMID: 22242007 PMC: 3248468. DOI: 10.1371/journal.pgen.1002436.

References

Olesnicky N, Brown A, Dowell S, Casselton L . A constitutively active G-protein-coupled receptor causes mating self-compatibility in the mushroom Coprinus. EMBO J. 1999; 18(10):2756-63. PMC: 1171357. DOI: 10.1093/emboj/18.10.2756. View

Casselton L, Olesnicky N . Molecular genetics of mating recognition in basidiomycete fungi. Microbiol Mol Biol Rev. 1998; 62(1):55-70. PMC: 98906. DOI: 10.1128/MMBR.62.1.55-70.1998. View

Banham A, Bohnert H, Mellor E, Casselton L . Heterodimerization between two classes of homeodomain proteins in the mushroom Coprinus cinereus brings together potential DNA-binding and activation domains. Gene. 1996; 172(1):25-31. DOI: 10.1016/0378-1119(96)00177-1. View

Koltin Y, RAPER J, Simchen G . The genetic structure of the incompatibility factors of Schizophyllum commune: the B factor. Proc Natl Acad Sci U S A. 1967; 57(1):55-62. PMC: 335464. DOI: 10.1073/pnas.57.1.55. View

Kothe E . Mating-type genes for basidiomycete strain improvement in mushroom farming. Appl Microbiol Biotechnol. 2001; 56(5-6):602-12. DOI: 10.1007/s002530100763. View

Fowler T, Mitton M, Vaillancourt L, Raper C . Changes in mate recognition through alterations of pheromones and receptors in the multisexual mushroom fungus Schizophyllum commune. Genetics. 2001; 158(4):1491-503. PMC: 1461750. DOI: 10.1093/genetics/158.4.1491. View

Halsall J, Milner M, Casselton L . Three subfamilies of pheromone and receptor genes generate multiple B mating specificities in the mushroom Coprinus cinereus. Genetics. 2000; 154(3):1115-23. PMC: 1460978. DOI: 10.1093/genetics/154.3.1115. View

Badrane H, May G . The divergence-homogenization duality in the evolution of the b1 mating type gene of Coprinus cinereus. Mol Biol Evol. 1999; 16(7):975-86. DOI: 10.1093/oxfordjournals.molbev.a026187. View

Robertson C, McMahon Kende A, Toenjes K, Novotny C, Ullrich R . Evidence for interaction of Schizophyllum commune Y mating-type proteins in vivo. Genetics. 2002; 160(4):1461-7. PMC: 1462057. DOI: 10.1093/genetics/160.4.1461. View

10.

Olesnicky N, Brown A, Honda Y, Dyos S, Dowell S, Casselton L . Self-compatible B mutants in coprinus with altered pheromone-receptor specificities. Genetics. 2000; 156(3):1025-33. PMC: 1461307. DOI: 10.1093/genetics/156.3.1025. View

11.

Gola S, HEGNER J, Kothe E . Chimeric pheromone receptors in the basidiomycete Schizophyllum commune. Fungal Genet Biol. 2000; 30(3):191-6. DOI: 10.1006/fgbi.2000.1222. View

12.

Magae Y, Novotny C, Ullrich R . Interaction of the A alpha Y and Z mating-type homeodomain proteins of Schizophyllum commune detected by the two-hybrid system. Biochem Biophys Res Commun. 1995; 211(3):1071-6. DOI: 10.1006/bbrc.1995.1920. View

13.

Vaillancourt L, Raper C . Pheromones and pheromone receptors as mating-type determinants in basidiomycetes. Genet Eng (N Y). 1996; 18:219-47. DOI: 10.1007/978-1-4899-1766-9_13. View

14.

Koltin Y, Stamberg J, Lemke P . Genetic structure and evolution of the incompatibility factors in higher fungi. Bacteriol Rev. 1972; 36(2):156-71. PMC: 408322. DOI: 10.1128/br.36.2.156-171.1972. View

15.

Raper C, RAPER J . Mutational analysis of a regulatory gene for morphogenesis in Schizophyllum. Proc Natl Acad Sci U S A. 1973; 70(5):1427-31. PMC: 433512. DOI: 10.1073/pnas.70.5.1427. View

16.

Vaillancourt L, Raudaskoski M, Specht C, Raper C . Multiple genes encoding pheromones and a pheromone receptor define the B beta 1 mating-type specificity in Schizophyllum commune. Genetics. 1997; 146(2):541-51. PMC: 1207996. DOI: 10.1093/genetics/146.2.541. View

17.

Hiscock S, Kues U . Cellular and molecular mechanisms of sexual incompatibility in plants and fungi. Int Rev Cytol. 1999; 193:165-295. DOI: 10.1016/s0074-7696(08)61781-7. View

18.

Leff P, Scaramellini C, Law C, McKechnie K . A three-state receptor model of agonist action. Trends Pharmacol Sci. 1997; 18(10):355-62. DOI: 10.1016/s0165-6147(97)01105-x. View

19.

Koltin Y, Stamberg J, Bawnik N, Tamarkin A, Werczberger R . Mutational analysis of natural alleles in and affecting the B incompatibility factor of Schizophyllum. Genetics. 1979; 93(2):383-91. PMC: 1214086. DOI: 10.1093/genetics/93.2.383. View

20.

Specht C . Isolation of the B alpha and B beta mating-type loci of Schizophyllum commune. Curr Genet. 1995; 28(4):374-9. DOI: 10.1007/BF00326436. View