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Genesis of a fungal non-self recognition repertoire.

ABSTRACT: Conspecific allorecognition, the ability for an organism to discriminate its own cells from those of another individual of the same species, has been developed by many organisms. Allorecognition specificities are determined by highly polymorphic genes. The processes by which this extreme polymorphism is generated remain largely unknown. Fungi are able to form heterokaryons by fusion of somatic cells, and somatic non self-recognition is controlled by heterokaryon incompatibility loci (het loci). Herein, we have analyzed the evolutionary features of the het-d and het-e fungal allorecognition genes. In these het genes, allorecognition specificity is determined by a polymorphic WD-repeat domain. We found that het-d and het-e belong to a large gene family with 10 members that all share the WD-repeat domain and show that repeats of all members of the family undergo concerted evolution. It follows that repeat units are constantly exchanged both within and between members of the gene family. As a consequence, high mutation supply in the repeat domain is ensured due to the high total copy number of repeats. We then show that in each repeat four residues located at the protein/protein interaction surface of the WD-repeat domain are under positive diversifying selection. Diversification of het-d and het-e is thus ensured by high mutation supply, followed by reshuffling of the repeats and positive selection for favourable variants. We also propose that RIP, a fungal specific hypermutation process acting specifically on repeated sequences might further enhance mutation supply. The combination of these evolutionary mechanisms constitutes an original process for generating extensive polymorphism at loci that require rapid diversification.

SUBMITTER: Paoletti M

PROVIDER: S-EPMC1805685 | biostudies-literature | 2007

REPOSITORIES: biostudies-literature

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Genesis of a fungal non-self recognition repertoire.

Paoletti Mathieu M Saupe Sven J SJ Clavé Corinne C

PloS one 20070314 3

Conspecific allorecognition, the ability for an organism to discriminate its own cells from those of another individual of the same species, has been developed by many organisms. Allorecognition specificities are determined by highly polymorphic genes. The processes by which this extreme polymorphism is generated remain largely unknown. Fungi are able to form heterokaryons by fusion of somatic cells, and somatic non self-recognition is controlled by heterokaryon incompatibility loci (het loci). ...[more]

PMID: 17356694

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Project description: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.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.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.

Project description:Non-self gametophytic self-incompatibility (GSI) recognition system is characterized by the presence of multiple F-box genes tandemly located in the S-locus, that regulate pollen specificity. This reproductive barrier is present in Solanaceae, Plantaginacea and Maleae (Rosaceae), but only in Petunia functional assays have been performed to get insight on how this recognition mechanism works. In this system, each of the encoded S-pollen proteins (called SLFs in Solanaceae and Plantaginaceae /SFBBs in Maleae) recognizes and interacts with a sub-set of non-self S-pistil proteins, called S-RNases, mediating their ubiquitination and degradation. In Petunia there are 17 SLF genes per S-haplotype, making impossible to determine experimentally each SLF specificity. Moreover, domain -swapping experiments are unlikely to be performed in large scale to determine S-pollen and S-pistil specificities. Phylogenetic analyses of the Petunia SLFs and those from two Solanum genomes, suggest that diversification of SLFs predate the two genera separation. Here we first identify putative SLF genes from nine Solanum and 10 Nicotiana genomes to determine how many gene lineages are present in the three genera, and the rate of origin of new SLF gene lineages. The use of multiple genomes per genera precludes the effect of incompleteness of the genome at the S-locus. The similar number of gene lineages in the three genera implies a comparable effective population size for these species, and number of specificities. The rate of origin of new specificities is one per 10 million years. Moreover, here we determine the amino acids positions under positive selection, those involved in SLF specificity recognition, using 10 Petunia S-haplotypes with more than 11 SLF genes. These 16 amino acid positions account for the differences of self-incompatible (SI) behavior described in the literature. When SLF and S-RNase proteins are divided according to the SI behavior, and the positively selected amino acids classified according to hydrophobicity, charge, polarity and size, we identified fixed differences between SI groups. According to the in silico 3D structure of the two proteins these amino acid positions interact. Therefore, this methodology can be used to infer SLF/S-RNase specificity recognition.

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Genesis of a fungal non-self recognition repertoire.

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Genesis of a fungal non-self recognition repertoire.

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