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      Interspecific Sex in Grass Smuts and the Genetic Diversity of Their Pheromone-Receptor System

        1 , 2 , 2 , 1 , *

      PLoS Genetics

      Public Library of Science

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          Abstract

          The grass smuts comprise a speciose group of biotrophic plant parasites, so-called Ustilaginaceae, which are specifically adapted to hosts of sweet grasses, the Poaceae family. Mating takes a central role in their life cycle, as it initiates parasitism by a morphological and physiological transition from saprobic yeast cells to pathogenic filaments. As in other fungi, sexual identity is determined by specific genomic regions encoding allelic variants of a pheromone-receptor (PR) system and heterodimerising transcription factors. Both operate in a biphasic mating process that starts with PR–triggered recognition, directed growth of conjugation hyphae, and plasmogamy of compatible mating partners. So far, studies on the PR system of grass smuts revealed diverse interspecific compatibility and mating type determination. However, many questions concerning the specificity and evolutionary origin of the PR system remain unanswered. Combining comparative genetics and biological approaches, we report on the specificity of the PR system and its genetic diversity in 10 species spanning about 100 million years of mating type evolution. We show that three highly syntenic PR alleles are prevalent among members of the Ustilaginaceae, favouring a triallelic determination as the plesiomorphic characteristic of this group. Furthermore, the analysis of PR loci revealed increased genetic diversity of single PR locus genes compared to genes of flanking regions. Performing interspecies sex tests, we detected a high potential for hybridisation that is directly linked to pheromone signalling as known from intraspecies sex. Although the PR system seems to be optimised for intraspecific compatibility, the observed functional plasticity of the PR system increases the potential for interspecific sex, which might allow the hybrid-based genesis of newly combined host specificities.

          Author Summary

          Sexual reproduction is prevalent among eukaryotes and involves the maintenance of different sexes within reproducing populations. Due to similarities to higher eukaryotes like animals and plants, fungi serve as adequate model systems to study sex determination, mate recognition, and mating type evolution. In fungi, sexual identity is determined by a few genes that reside at specific genomic regions. Those so-called mating type loci encode a pheromone-receptor system and heterodimerising transcription factors. Intensive studies of various model organisms uncovered important aspects of sex in fungi. However, comparative surveys that cover distinct phylogenetic groups within the fungal kingdom are still rare, leaving many questions unanswered about the diversity, specificity, and evolutionary transitions of fungal mating types. Here, we report on mating genetics and the specificity of mate recognition in the plant biotrophic basidiomycete family Ustilaginaceae. In our Ustilaginaceae-wide study, we unravel a conserved triallelic pheromone-receptor system that preserved interspecific sexual compatibility for more than 100 million years and most likely gave rise to the convergent evolution of biallelic mating type determinations. Moreover, our results demonstrate that grass smuts represent a valuable model group to study the hybrid-based genesis of novel genotypes and their evolutionary impact on speciation.

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          Most cited references 136

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          Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.

           S Altschul (1997)
          The BLAST programs are widely used tools for searching protein and DNA databases for sequence similarities. For protein comparisons, a variety of definitional, algorithmic and statistical refinements described here permits the execution time of the BLAST programs to be decreased substantially while enhancing their sensitivity to weak similarities. A new criterion for triggering the extension of word hits, combined with a new heuristic for generating gapped alignments, yields a gapped BLAST program that runs at approximately three times the speed of the original. In addition, a method is introduced for automatically combining statistically significant alignments produced by BLAST into a position-specific score matrix, and searching the database using this matrix. The resulting Position-Specific Iterated BLAST (PSI-BLAST) program runs at approximately the same speed per iteration as gapped BLAST, but in many cases is much more sensitive to weak but biologically relevant sequence similarities. PSI-BLAST is used to uncover several new and interesting members of the BRCT superfamily.
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            MrBayes 3: Bayesian phylogenetic inference under mixed models.

            MrBayes 3 performs Bayesian phylogenetic analysis combining information from different data partitions or subsets evolving under different stochastic evolutionary models. This allows the user to analyze heterogeneous data sets consisting of different data types-e.g. morphological, nucleotide, and protein-and to explore a wide variety of structured models mixing partition-unique and shared parameters. The program employs MPI to parallelize Metropolis coupling on Macintosh or UNIX clusters.
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              CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.

              The sensitivity of the commonly used progressive multiple sequence alignment method has been greatly improved for the alignment of divergent protein sequences. Firstly, individual weights are assigned to each sequence in a partial alignment in order to down-weight near-duplicate sequences and up-weight the most divergent ones. Secondly, amino acid substitution matrices are varied at different alignment stages according to the divergence of the sequences to be aligned. Thirdly, residue-specific gap penalties and locally reduced gap penalties in hydrophilic regions encourage new gaps in potential loop regions rather than regular secondary structure. Fourthly, positions in early alignments where gaps have been opened receive locally reduced gap penalties to encourage the opening up of new gaps at these positions. These modifications are incorporated into a new program, CLUSTAL W which is freely available.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Genet
                plos
                plosgen
                PLoS Genetics
                Public Library of Science (San Francisco, USA )
                1553-7390
                1553-7404
                December 2011
                December 2011
                29 December 2011
                : 7
                : 12
                Affiliations
                [1 ]Ruhr-Universität Bochum, Geobotany Laboratory, Bochum, Germany
                [2 ]Heinrich-Heine University Düsseldorf, Institute for Microbiology, Düsseldorf, Germany
                Duke University Medical Center, United States of America
                Author notes

                Conceived and designed the experiments: RK EV DB. Performed the experiments: RK EV. Analyzed the data: RK. Contributed reagents/materials/analysis tools: RK EV MF DB. Wrote the paper: RK EV DB MF.

                Article
                PGENETICS-D-11-01919
                10.1371/journal.pgen.1002436
                3248468
                22242007
                Kellner et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                Page count
                Pages: 17
                Categories
                Research Article
                Biology
                Ecology
                Biodiversity
                Evolutionary Biology
                Evolutionary Processes
                Coevolution
                Hybridization
                Introgression
                Mutation
                Speciation
                Evolutionary Systematics
                Phylogenetics
                Forms of Evolution
                Coevolution
                Convergent Evolution
                Organismal Evolution
                Microbial Evolution
                Evolutionary Genetics
                Genetics
                Molecular Genetics
                Gene Identification and Analysis
                Microbiology
                Mycology
                Fungal Evolution
                Fungal Physiology
                Fungal Reproduction
                Fungal Structure
                Fungi
                Microbial Pathogens
                Molecular Cell Biology
                Signal Transduction
                Signaling Cascades
                MAPK signaling cascades
                Signaling in Cellular Processes
                G-Protein Signaling

                Genetics

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