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. 2015 Feb 14;16(1):80.
doi: 10.1186/s12864-015-1278-x.

Comparative Genome and Transcriptome Analyses of the Social Amoeba Acytostelium Subglobosum That Accomplishes Multicellular Development Without Germ-Soma Differentiation

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Comparative Genome and Transcriptome Analyses of the Social Amoeba Acytostelium Subglobosum That Accomplishes Multicellular Development Without Germ-Soma Differentiation

Hideko Urushihara et al. BMC Genomics. .
Free PMC article

Abstract

Background: Social amoebae are lower eukaryotes that inhabit the soil. They are characterized by the construction of a starvation-induced multicellular fruiting body with a spore ball and supportive stalk. In most species, the stalk is filled with motile stalk cells, as represented by the model organism Dictyostelium discoideum, whose developmental mechanisms have been well characterized. However, in the genus Acytostelium, the stalk is acellular and all aggregated cells become spores. Phylogenetic analyses have shown that it is not an ancestral genus but has lost the ability to undergo cell differentiation.

Results: We performed genome and transcriptome analyses of Acytostelium subglobosum and compared our findings to other available dictyostelid genome data. Although A. subglobosum adopts a qualitatively different developmental program from other dictyostelids, its gene repertoire was largely conserved. Yet, families of polyketide synthase and extracellular matrix proteins have not expanded and a serine protease and ABC transporter B family gene, tagA, and a few other developmental genes are missing in the A. subglobosum lineage. Temporal gene expression patterns are astonishingly dissimilar from those of D. discoideum, and only a limited fraction of the ortholog pairs shared the same expression patterns, so that some signaling cascades for development seem to be disabled in A. subglobosum.

Conclusions: The absence of the ability to undergo cell differentiation in Acytostelium is accompanied by a small change in coding potential and extensive alterations in gene expression patterns.

Figures

Figure 1
Figure 1
Properties of A. subglobosum in comparison with D. discoideum. A: Morphologies of fruiting bodies of A. subglobosum (left) and D. discoideum (right). Note the differences in magnification. B: Higher magnification photographs of A. subglobosum (left) and D. discoideum stalk (right). C: Developmental time courses for both species. D: Phylogenetic relationships shown schematically for the species described in the text. Numerals in the triangles indicate the group number of each clade. E: Results of flow cytometry analysis of nuclear DNA content. Arrows indicate the peak positions of the haploid nuclei. F: DAPI staining of the nuclei. Two independent nuclei (left pictures) and sum of 35 nuclei (right) are shown.
Figure 2
Figure 2
Gene orthology analysis of 4 social amoeba species. A: Results of the bidirectional best hit approach are shown schematically. Numbers represent species-specific genes. Colors orange, red, blue, and green represent D. discoideum, A. subglobosum, P. pallidum, and D. fasciculatum, respectively. Genes in area G are absent in the A. subglobosum lineage but present in D. discoideum, P. pallidum, and D. fasciculatum. B: Gene numbers of each species contained in the areas A–K of the Venn diagram.
Figure 3
Figure 3
A phylogenetic tree of the PKS family (OG5_126633) showing the A. subglobosum -specific lack of expansion. Color designations are shown at the bottom right. Black stars indicate the positions of stlA and stlB.
Figure 4
Figure 4
Comparison of temporal gene expression patterns between D. discoideum and A. subglobosum . A: Results of collective clustering are shown as heat maps with the scale shown below. Cluster distances are shown on the left. Clusters 1–3 represent down-regulated genes, while clusters 4–8 contain up-regulated genes during development. B: Fractions of genes in each cluster for A. subglobosum (right) and D. discoideum (left). Numbers indicate the genes in each cluster. C: Differential expression patterns of orthologous gene pairs for total (top), prestalk-specific (middle), and prespore-specific genes (bottom). Match: in the same cluster; similar: different cluster but in the same group; precocious: A. subglobosum genes were in the up-regulated group, while D. discoideum orthologs were in the down-regulated group; retarded: opposite of precocious.
Figure 5
Figure 5
Comparison of the overall process of fruiting formation between A. subglobosum and D. discoideum . A: Overall process of fruiting body formation in D. discoideum shown schematically as gene-expression relays. Extracellular signaling molecules are shown in red. Gray, orange, blue, and green ovules represent the expression of aggregation, spore-lineage, stalk-lineage, and terminal differentiation genes, respectively. UC: Upper cup; LC: lower cup; BD: basal disk. B: Possible gene-expression relays in A. subglobosum shown in correspondence with (A).
Figure 6
Figure 6
Developmental signaling in D. discoideum overlaid with genomic and transcriptomics data of A. subglobosum . A: Signaling cascades for cell-fate determination and prestalk differentiation in D. discoideum. B: Signaling cascades for spore encapsulation (PSV exocytosis) in D. discoideum. The cascades are overlaid with A. subglobosum genome and transcriptome information. Extracellular and intracellular signaling molecules are indicated by blue and red rectangles, respectively. Components of intracellular cascades are mostly shown by gene names but some in (A) are by protein names. Faint colors indicate that operation in A. subglobosum is unlikely. Solid arrows indicate induction or inhibition, while dotted lines indicate processing and/or transport. Genes in red designate the absence of orthologs, while those in green, blue, orange, and gray designate the same, similar, precocious, and trace expression in A. subglobosum, respectively. PSV: prespore vesicle.

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