Causes and Consequences of Genome Expansion in Fungi

Department of Ecology and Evolutionary Biology, Yale University, USA.
Genome Biology and Evolution (Impact Factor: 4.23). 11/2011; 4(1):13-23. DOI: 10.1093/gbe/evr124
Source: PubMed


Fungi display a large diversity in genome size and complexity, variation that is often considered to be adaptive. But because nonadaptive processes can also have important consequences on the features of genomes, we investigated the relationship of genetic drift and genome size in the phylum Ascomycota using multiple indicators of genetic drift. We detected a complex relationship between genetic drift and genome size in fungi: genetic drift is associated with genome expansion on broad evolutionary timescales, as hypothesized for other eukaryotes; but within subphyla over smaller timescales, the opposite trend is observed. Moreover, fungi and bacteria display similar patterns of genome degradation that are associated with initial effects of genetic drift. We conclude that changes in genome size within Ascomycota have occurred using two different routes: large-scale genome expansions are catalyzed by increasing drift as predicted by the mutation-hazard model of genome evolution and small-scale modifications in genome size are independent of drift.

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Available from: Yogeshwar D Kelkar, Nov 04, 2014
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    • "In a recent analysis of the underlying processes associated with genome size expansion within the Ascomycota, Kelkar and Ochman (2012) suggest that genetic drift, reflected through a decrease in gene density and a proliferation of introns, has played a significant role across many lineages on broad evolutionary time scales. The large genome size of C. geophilum might therefore result from ancestral genome size expansion driven by genetic drift, which would lead to a repeat-rich and relatively gene-poor genome. "
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    ABSTRACT: Estimations of genome size and its variation can provide valuable information regarding the genetic diversity of organisms and their adaptation potential to heterogeneous environments. We used flow cytometry to characterize the variation in genome size among 40 isolates of Cenococcum geophilum, an ectomycorrhizal fungus with a wide ecological and geographical distribution, obtained from two serpentine and two non-serpentine sites in Portugal. Besides determining the genome size and its intraspecies variation, we wanted to assess whether a relationship exists between genome size and the edaphic background of the C. geophilum isolates. Our results reveal C. geophilum to have one of the largest genome sizes so far measured in the Ascomycota, with a mean haploid genome size estimate of 0.208 pg (203 Mbp). However, no relationship was found between genome size and the edaphic background of the sampled isolates, indicating genetic and demographic processes to be more important for shaping the genome size variation in this species than environmental selection. The detection of variation in ploidy level among our isolates, including a single individual with both presumed haploid and diploid nuclei, provides supportive evidence for a possible cryptic sexual or parasexual cycle in C. geophilum (although other mechanisms may have caused this variation). The existence of such a cycle would have wide significance, explaining the high levels of genetic diversity and likelihood of recombination previously reported in this species, and adds to the increasing number of studies suggesting sexual cycles in previously assumed asexual fungi.
    Mycorrhiza 01/2014; 24:13-20. DOI:10.1007/s00572-013-0501-3 · 3.46 Impact Factor
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    • "For W. sebi 5284 proteins were predicted, and 4285 for M. globosa, while >10000 proteins are not uncommon in other basidomycetes). Despite the reduction in genome size and gene number the number of introns is not unusually small as is seen in some other fungi with small genomes [22]: on average, the predicted genes contain 2.41 introns that are 61 bp long (Table 1). In other fungi the average intron densities range from just over 1.0 intron/ kb coding sequence (cds) in Schizosaccharomyces pombe to approximately 5.0 introns/ kb cds in Cryptococcus neoformans[23]. "
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    ABSTRACT: The basidomycete Wallemia ichthyophaga from the phylogenetically distinct class Wallemiomycetes is the most halophilic fungus known to date. It requires at least 10% NaCl and thrives in saturated salt solution. To investigate the genomic basis of this exceptional phenotype, we obtained a de-novo genome sequence of the species type-strain and analysed its transcriptomic response to conditions close to the limits of its lower and upper salinity range. The unusually compact genome is 9.6 Mb large and contains 1.67% repetitive sequences. Only 4884 predicted protein coding genes cover almost three quarters of the sequence. Of 639 differentially expressed genes, two thirds are more expressed at lower salinity. Phylogenomic analysis based on the largest dataset used to date (whole proteomes) positions Wallemiomycetes as a 250-million-year-old sister group of Agaricomycotina. Contrary to the closely related species Wallemia sebi, W. ichthyophaga appears to have lost the ability for sexual reproduction. Several protein families are significantly expanded or contracted in the genome. Among these, there are the P-type ATPase cation transporters, but not the sodium/ hydrogen exchanger family. Transcription of all but three cation transporters is not salt dependent. The analysis also reveals a significant enrichment in hydrophobins, which are cell-wall proteins with multiple cellular functions. Half of these are differentially expressed, and most contain an unusually large number of acidic amino acids. This discovery is of particular interest due to the numerous applications of hydrophobines from other fungi in industry, pharmaceutics and medicine. W. ichthyophaga is an extremophilic specialist that shows only low levels of adaptability and genetic recombination. This is reflected in the characteristics of its genome and its transcriptomic response to salt. No unusual traits were observed in common salt-tolerance mechanisms, such as transport of inorganic ions or synthesis of compatible solutes. Instead, various data indicate a role of the cell wall of W. ichthyophaga in its response to salt. Availability of the genomic sequence is expected to facilitate further research into this unique species, and shed more light on adaptations that allow it to thrive in conditions lethal to most other eukaryotes.
    BMC Genomics 09/2013; 14(1):617. DOI:10.1186/1471-2164-14-617 · 3.99 Impact Factor
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    • "Fungi are a diverse group of osmotrophs, ranging from obligate, single-celled pathogens to large, multicellular heterotrophs, with intimate associations across the spectrum of life. Most fungal genomes sequenced to date are streamlined by eukaryotic standards (20–60 Mb, 30–70% coding sequence, low-to-moderate levels of transposable elements, 2–3 introns per gene, and low levels of alternative transcription), though current extremes range from just 2.3 Mb for the microsporidian Encephalitozoon intestinalis to 160 Mb for the Ascomycete Golovinomyces orontii, both obligate pathogens (Kelkar and Ochman 2012). The most familiar and first sequenced fungi, the model “yeasts” Saccharomyces cerevisiae and Schizosaccharomyces pombe, have proven to be atypical relative to the majority of Ascomycetes with a reduced genome size and gene count, few introns and a greater proportion of coding sequence. "
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    ABSTRACT: Gene context determines gene expression, with local chromosomal environment most influential. Comparative genomic analysis is often limited in scope to conserved or divergent gene and protein families, and fungi are well suited to this approach with low functional redundancy and relatively streamlined genomes. We show here that one aspect of gene context, the amount of potential upstream regulatory sequence maintained through evolution, is highly predictive of both molecular function and biological process in diverse fungi. Orthologues with large upstream intergenic regions are strongly enriched in information processing functions, such as signal transduction and sequence specific DNA binding, and, in the genus Aspergillus, include the majority of experimentally studied, high-level developmental and metabolic transcriptional regulators. Many uncharacterised genes are also present in this class and, by implication, may be of similar importance. Large intergenic regions also share two novel sequence characteristics, currently of unknown significance: they are enriched for plus-strand polypyrimidine tracts and an information-rich, putative regulatory motif that was present in the last common ancestor of the Pezizomycotina. Systematic consideration of gene UIR in comparative genomics, particularly for poorly characterised species, could help reveal organisms' regulatory priorities.
    Genome Biology and Evolution 05/2013; 5(7). DOI:10.1093/gbe/evt077 · 4.23 Impact Factor
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