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URL: https://pubmed.ncbi.nlm.nih.gov/18725939/

⇱ Elusive origins of the extra genes in Aspergillus oryzae - PubMed

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Abstract

The genome sequence of Aspergillus oryzae revealed unexpectedly that this species has approximately 20% more genes than its congeneric species A. nidulans and A. fumigatus. Where did these extra genes come from? Here, we evaluate several possible causes of the elevated gene number. Many gene families are expanded in A. oryzae relative to A. nidulans and A. fumigatus, but we find no evidence of ancient whole-genome duplication or other segmental duplications, either in A. oryzae or in the common ancestor of the genus Aspergillus. We show that the presence of divergent pairs of paralogs is a feature peculiar to A. oryzae and is not shared with A. nidulans or A. fumigatus. In phylogenetic trees that include paralog pairs from A. oryzae, we frequently find that one of the genes in a pair from A. oryzae has the expected orthologous relationship with A. nidulans, A. fumigatus and other species in the subphylum Eurotiomycetes, whereas the other A. oryzae gene falls outside this clade but still within the Ascomycota. We identified 456 such gene pairs in A. oryzae. Further phylogenetic analysis did not however indicate a single consistent evolutionary origin for the divergent members of these pairs. Approximately one-third of them showed phylogenies that are suggestive of horizontal gene transfer (HGT) from Sordariomycete species, and these genes are closer together in the A. oryzae genome than expected by chance, but no unique Sordariomycete donor species was identifiable. The postulated HGTs from Sordariomycetes still leave the majority of extra A. oryzae genes unaccounted for. One possible explanation for our observations is that A. oryzae might have been the recipient of many separate HGT events from diverse donors.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

👁 Figure 1
Figure 1. Definition of Topology S loci in (a) A. oryzae, (b) A. fumigatus, and (c) A. nidulans.
Yellow boxes indicate the genes that are orthologous in the three species. The red box contains the extra paralog (labeled AO2, AFU2 or AN2). Loci having Topology S were identified in each species by an automated process without the use of an outgroup, but the root of the tree is likely to lie on the upper (longest) branch.
👁 Figure 2
Figure 2. Boxplots of the distributions of synonymous nucleotide divergence (K S) values between A. nidulans genes (AN) and A. oryzae gene copies AO1 and AO2, for all genes in Set SAO.
The boxes show the median and interquartile values, with 95% of the data falling within the whiskers. K S values were calculated using yn00 from the PAML package . K S values for the AO1 genes are significantly lower than for the corresponding AO2 genes (P<10−4; Wilcoxon test).
👁 Figure 3
Figure 3. Model of a WGD hypothesis for the origin of extra genes in A. oryzae.
A WGD in the common ancestor of the three Aspergillus species, followed by extensive gene losses in both A. nidulans and A. fumigatus could potentially account for the large number of genes in Set SAO. In this schematic diagram black squares represent genes, double vertical lines represent chromosome breaks, and dashed horizontal lines represent gene deletions or intrachromosomal rearrangements. Our method of testing for WGD involves sliding a window (blue box) through the A. oryzae genome to find clusters of nearby genes that are enriched in genes from Set SAO (red box). If a WGD occurred, the paralogs of the genes in the blue window are expected to be closer together on the sister A. oryzae genomic region than expected by chance.
👁 Figure 4
Figure 4. Testing for whole genome duplication in A. oryzae and S. cerevisiae.
Black histograms show the distribution of distance scores (d) obtained in 10,000 simulations where paralog locations were randomized. Blue and green lines show the cutoff points for the most-clustered 1% and 5% of these data, respectively. Red lines show the observed d values for S. cerevisiae or A. oryzae. All the graphs are for windows of size j = 200. Panels A-C consider only windows where the paralogous genes are all on the same chromosome. (A) Results for S. cerevisiae for windows with i = 10 paralogs. (B) Results for S. cerevisiae for windows with i = 12 paralogs. (C) Results for A. oryzae for windows with i = 6 paralogs. (D) Results for A. oryzae for windows with i = 3 paralogs, including a penalty of 3000 for each interchromosomal rearrangement event.
👁 Figure 5
Figure 5. Topologies A, B and C for rooted trees.
Left: The three topologies correspond to the three possible points for placement of a root (arrows labeled A, B, C) onto an unrooted tree consisting of a gene pair from A. oryzae and their homolog from a Sordariomycete such as Fusarium graminearum. Center: Rooted representations of the topologies. Right: real examples of A. oryzae genes classified in each of the three topologies. Numbers in parentheses are NCBI protein identifiers. Trees were constructed using PHYML with bootstrap percentages (form 500 replicates) shown. The main groups differentiating the topologies from each other are colored.
👁 Figure 6
Figure 6. A case of family expansion due to apparent HGT.
The gene family is a member of the metal dependent hydrolytic enzyme superfamily (amidases, aminoacyclases, and carboxypeptidases). The A. oryzae genes AO1 and AO2 originally identified in our automated search are labeled. Four of the six A. oryzae genes (83775625, 83765251, 83766521, 83770136) in this family lack orthologs in A. nidulans and A. fumigatus, and for the first two of these there is strong bootstrap support for HGT from Sordariomycete. Of these four genes, three show Topology A and one (83766521) shows Topology C relative to their nearest Sordariomycete homologs.

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