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Heterogeneous rates of genome rearrangement contributed to the disparity of species richness in Ascomycota.

ABSTRACT: Chromosomal rearrangements have been shown to facilitate speciation through creating a barrier of gene flow. However, it is not known whether heterogeneous rates of chromosomal rearrangement at the genome scale contributed to the huge disparity of species richness among different groups of organisms, which is one of the most remarkable and pervasive patterns on Earth. The largest fungal phylum Ascomycota is an ideal study system to address this question because it comprises three subphyla (Saccharomycotina, Taphrinomycotina, and Pezizomycotina) whose species numbers differ by two orders of magnitude (59,000, 1000, and 150 respectively).We quantified rates of genome rearrangement for 71 Ascomycota species that have well-assembled genomes. The rates of inter-species genome rearrangement, which were inferred based on the divergence rates of gene order, are positively correlated with species richness at both ranks of subphylum and class in Ascomycota. This finding is further supported by our quantification of intra-species rearrangement rates based on paired-end genome sequencing data of 216 strains from three representative species, suggesting a difference of intrinsic genome instability among Ascomycota lineages. Our data also show that different rates of imbalanced rearrangements, such as deletions, are a major contributor to the heterogenous rearrangement rates.Various lines of evidence in this study support that a higher rate of rearrangement at the genome scale might have accelerated the speciation process and increased species richness during the evolution of Ascomycota species. Our findings provide a plausible explanation for the species disparity among Ascomycota lineages, which will be valuable to unravel the underlying causes for the huge disparity of species richness in various taxonomic groups.

SUBMITTER: Rajeh A

PROVIDER: S-EPMC5937819 | biostudies-other | 2018 Apr

REPOSITORIES: biostudies-other

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Heterogeneous rates of genome rearrangement contributed to the disparity of species richness in Ascomycota.

Rajeh Ahmad A Lv Jie J Lin Zhenguo Z

BMC genomics 20180424 1

<h4>Background</h4>Chromosomal rearrangements have been shown to facilitate speciation through creating a barrier of gene flow. However, it is not known whether heterogeneous rates of chromosomal rearrangement at the genome scale contributed to the huge disparity of species richness among different groups of organisms, which is one of the most remarkable and pervasive patterns on Earth. The largest fungal phylum Ascomycota is an ideal study system to address this question because it comprises th ...[more]

PMID: 29690866

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Project description:BackgroundComparative genomic analysis exhibits dynamic evolution of plastid genome (plastome) in the clusioid clade of Malpighiales, which comprise five families, including multiple inversions and gene losses. Little is known about the plastome evolution in Hypericaceae, a large family in the clade. Only the plastome of one species, Cratoxylum cochinchinense, has been published.ResultsWe generated a complete plastome sequence for Hypericum ascyron, providing the first complete plastome from the tribe Hypericeae (Hypericaceae). The H. ascyron plastome exhibits dynamic changes in gene and intron content, structure, and sequence divergence compared to the C. cochinchinense plastome from the tribe Cratoxyleae (Hypericaceae). Transcriptome data determined the evolutionary fate of the missing plastid genes infA, rps7, rps16, rpl23, and rpl32 in H. ascyron. Putative functional transfers of infA, rps7, and rpl32 were detected to the nucleus, whereas rps16 and rpl23 were substituted by nuclear-encoded homologs. The plastid rpl32 was integrated into the nuclear-encoded SODcp gene. Our findings suggested that the transferred rpl32 had undergone subfunctionalization by duplication rather than alternative splicing. The H. ascyron plastome rearrangements involved seven inversions, at least three inverted repeat (IR) boundary shifts, which generated gene relocations and duplications. Accelerated substitution rates of plastid genes were observed in the H. ascyron plastome compared with that of C. cochinchinense plastid genes. The higher substitution rates in the accD and clpP were correlated with structural change, including a large insertion of amino acids and losses of two introns, respectively. In addition, we found evidence of positive selection of the clpP, matK, and rps3 genes in the three branches related to H. ascyron. In particular, the matK gene was repeatedly under selection within the family Hypericaceae. Selective pressure in the H. ascyron matK gene was associated with the loss of trnK-UUU and relocation into the IR region.ConclusionsThe Hypericum ascyron plastome sequence provides valuable information for improving the understanding of plastome evolution among the clusioid of the Malpighiales. Evidence for intracellular gene transfer from the plastid to the nucleus was detected in the nuclear transcriptome, providing insight into the evolutionary fate of plastid genes in Hypericaceae.

Project description:The positive relationship between habitat heterogeneity and species richness is a cornerstone of ecology. Recently, it was suggested that this relationship should be unimodal rather than linear due to a tradeoff between environmental heterogeneity and population sizes. Increased environmental heterogeneity will decrease effective habitat sizes, which in turn will increase the rate of local species extinctions. The occurrence of the unimodal richness-heterogeneity relationship at the habitat scale was confirmed in both empirical and theoretical studies. However, it is unclear whether it can occur at broader spatial scales, for meta-communities in diverse and patchy landscapes. Here, I used a spatially explicit meta-community model to quantify the roles of two species-level characteristics, niche width and immigration rates, on the type of the richness-heterogeneity relationship at the landscape scale. I found that both positive and unimodal richness-heterogeneity relationships can occur in meta-communities in patchy landscapes. The type of the relationship was affected by the interactions between inter-patch immigration rates and species' niche widths. Unimodal relationships were prominent in meta-communities comprising species with wide niches but low inter-patch immigration rates. In contrast, meta-communities consisting of species with narrow niches and high immigration rates exhibited positive relationships. Meta-communities comprising generalist species are therefore likely to exhibit unimodal richness-heterogeneity relationships as long as low immigration rates prevent rescue effects and patches are small. The richness-heterogeneity relationship at the landscape scale is dictated by species' niche widths and inter-patch immigration rates. These immigration rates, in turn, depend on the interaction between species dispersal capabilities and habitat connectivity, highlighting the roles of both species traits and landscape structure in generating the richness-heterogeneity relationship at the landscape scale.

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Heterogeneous rates of genome rearrangement contributed to the disparity of species richness in Ascomycota.

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Heterogeneous rates of genome rearrangement contributed to the disparity of species richness in Ascomycota.

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