Evolution and Diversity of a Fungal Self/nonself Recognition Locus

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2010 Dec 3

PMID 21124910

Citations 30

Authors

Charles Hall

Juliet Welch

David J Kowbel

N Louise Glass

Affiliations

Soon will be listed here.

Abstract

Background: Self/nonself discrimination is an essential feature for pathogen recognition and graft rejection and is a ubiquitous phenomenon in many organisms. Filamentous fungi, such as Neurospora crassa, provide a model for analyses of population genetics/evolution of self/nonself recognition loci due to their haploid nature, small genomes and excellent genetic/genomic resources. In N. crassa, nonself discrimination during vegetative growth is determined by 11 heterokaryon incompatibility (het) loci. Cell fusion between strains that differ in allelic specificity at any of these het loci triggers a rapid programmed cell death response.

Methodology/principal Findings: In this study, we evaluated the evolution, population genetics and selective mechanisms operating at a nonself recognition complex consisting of two closely linked loci, het-c (NCU03493) and pin-c (NCU03494). The genomic position of pin-c next to het-c is unique to Neurospora/Sordaria species, and originated by gene duplication after divergence from other species within the Sordariaceae. The het-c pin-c alleles in N. crassa are in severe linkage disequilibrium and consist of three haplotypes, het-c1/pin-c1, het-c2/pin-c2 and het-c3/pin-c3, which are equally frequent in population samples and exhibit trans-species polymorphisms. The absence of recombinant haplotypes is correlated with divergence of the het-c/pin-c intergenic sequence. Tests for positive and balancing selection at het-c and pin-c support the conclusion that both of these loci are under non-neutral balancing selection; other regions of both genes appear to be under positive selection. Our data show that the het-c2/pin-c2 haplotype emerged by a recombination event between the het-c1/pin-c1 and het-c3/pin-c3 approximately 3-12 million years ago.

Conclusions/significance: These results support models by which loci that confer nonself discrimination form by the association of polymorphic genes with genes containing HET domains. Distinct allele classes can emerge by recombination and positive selection and are subsequently maintained by balancing selection and divergence of intergenic sequence resulting in recombination blocks between haplotypes.

Citing Articles

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References

Dishaw L, Litman G . Invertebrate allorecognition: the origins of histocompatibility. Curr Biol. 2009; 19(7):R286-8. PMC: 3699862. DOI: 10.1016/j.cub.2009.02.035. View

Glass N, Dementhon K . Non-self recognition and programmed cell death in filamentous fungi. Curr Opin Microbiol. 2006; 9(6):553-8. DOI: 10.1016/j.mib.2006.09.001. View

Jacobson , Beurkens , Klomparens . Microscopic and Ultrastructural Examination of Vegetative Incompatibility in Partial Diploids Heterozygous at het Loci in Neurospora crassa. Fungal Genet Biol. 1998; 23(1):45-56. DOI: 10.1006/fgbi.1997.1020. View

Bernatchez L, Landry C . MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years?. J Evol Biol. 2003; 16(3):363-77. DOI: 10.1046/j.1420-9101.2003.00531.x. View

Wu J, Saupe S, Glass N . Evidence for balancing selection operating at the het-c heterokaryon incompatibility locus in a group of filamentous fungi. Proc Natl Acad Sci U S A. 1998; 95(21):12398-403. PMC: 22843. DOI: 10.1073/pnas.95.21.12398. View

Ronquist F, Huelsenbeck J . MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003; 19(12):1572-4. DOI: 10.1093/bioinformatics/btg180. View

Jacobson D, Dehghany M, Micali O, Smith M . Molecular and functional analyses of incompatibility genes at het-6 in a population of Neurospora crassa. Fungal Genet Biol. 2000; 30(3):197-205. DOI: 10.1006/fgbi.2000.1218. View

Kamau E, Charlesworth D . Balancing selection and low recombination affect diversity near the self-incompatibility loci of the plant Arabidopsis lyrata. Curr Biol. 2005; 15(19):1773-8. DOI: 10.1016/j.cub.2005.08.062. View

Wang X, Hughes A, Tsukamoto T, Ando T, Kao T . Evidence that intragenic recombination contributes to allelic diversity of the S-RNase gene at the self-incompatibility (S) locus in Petunia inflata. Plant Physiol. 2001; 125(2):1012-22. PMC: 64901. DOI: 10.1104/pp.125.2.1012. View

10.

Galagan J, Selker E . RIP: the evolutionary cost of genome defense. Trends Genet. 2004; 20(9):417-23. DOI: 10.1016/j.tig.2004.07.007. View

11.

Goldman N, Yang Z . A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol Biol Evol. 1994; 11(5):725-36. DOI: 10.1093/oxfordjournals.molbev.a040153. View

12.

Wu J, Glass N . Identification of specificity determinants and generation of alleles with novel specificity at the het-c heterokaryon incompatibility locus of Neurospora crassa. Mol Cell Biol. 2001; 21(4):1045-57. PMC: 99559. DOI: 10.1128/MCB.21.4.1045-1057.2001. View

13.

Menkis A, Jacobson D, Gustafsson T, Johannesson H . The mating-type chromosome in the filamentous ascomycete Neurospora tetrasperma represents a model for early evolution of sex chromosomes. PLoS Genet. 2008; 4(3):e1000030. PMC: 2268244. DOI: 10.1371/journal.pgen.1000030. View

14.

Paoletti M, Saupe S . Fungal incompatibility: evolutionary origin in pathogen defense?. Bioessays. 2009; 31(11):1201-10. DOI: 10.1002/bies.200900085. View

15.

Saupe S, Kuldau G, Smith M, Glass N . The product of the het-C heterokaryon incompatibility gene of Neurospora crassa has characteristics of a glycine-rich cell wall protein. Genetics. 1996; 143(4):1589-600. PMC: 1207423. DOI: 10.1093/genetics/143.4.1589. View

16.

Kosakovsky Pond S, Frost S . Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics. 2005; 21(10):2531-3. DOI: 10.1093/bioinformatics/bti320. View

17.

Nei M, Li W . Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci U S A. 1979; 76(10):5269-73. PMC: 413122. DOI: 10.1073/pnas.76.10.5269. View

18.

Espagne E, Lespinet O, Malagnac F, Da Silva C, Jaillon O, Porcel B . The genome sequence of the model ascomycete fungus Podospora anserina. Genome Biol. 2008; 9(5):R77. PMC: 2441463. DOI: 10.1186/gb-2008-9-5-r77. View

19.

Stern A, Doron-Faigenboim A, Erez E, Martz E, Bacharach E, Pupko T . Selecton 2007: advanced models for detecting positive and purifying selection using a Bayesian inference approach. Nucleic Acids Res. 2007; 35(Web Server issue):W506-11. PMC: 1933148. DOI: 10.1093/nar/gkm382. View

20.

Takuno S, Fujimoto R, Sugimura T, Sato K, Okamoto S, Zhang S . Effects of recombination on hitchhiking diversity in the Brassica self-incompatibility locus complex. Genetics. 2007; 177(2):949-58. PMC: 2034657. DOI: 10.1534/genetics.107.073825. View