Conserved developmental transcriptomes in evolutionarily divergent species

Abstract

Background: Evolutionarily divergent organisms often share developmental anatomies despite vast differences between their genome sequences. The social amoebae Dictyostelium discoideum and Dictyostelium purpureum have similar developmental morphologies although their genomes are as divergent as those of man and jawed fish.

Results: Here we show that the anatomical similarities are accompanied by extensive transcriptome conservation. Using RNA sequencing we compared the abundance and developmental regulation of all the transcripts in the two species. In both species, most genes are developmentally regulated and the greatest expression changes occur during the transition from unicellularity to multicellularity. The developmental regulation of transcription is highly conserved between orthologs in the two species. In addition to timing of expression, the level of mRNA production is also conserved between orthologs and is consistent with the intuitive notion that transcript abundance correlates with the amount of protein required. Furthermore, the conservation of transcriptomes extends to cell-type specific expression.

Conclusions: These findings suggest that developmental programs are remarkably conserved at the transcriptome level, considering the great evolutionary distance between the genomes. Moreover, this transcriptional conservation may be responsible for the similar developmental anatomies of Dictyostelium discoideum and Dictyostelium purpureum.

Figure 1

Conservation of morphology and gene expression patterns in the developmental programs of D. discoideum and D. purpureum. (a) An illustration of the developmental programs. Both species begin the developmental program by aggregation of starving cells into centers that contain approximately 50,000 cells. The aggregates undergo morphological transformations from loose aggregates to tight aggregates to tipped aggregates while the cells differentiate into prespore and prestalk cells (not shown). Later in development, D. purpureum slugs (right) migrate while leaving a cellular stalk behind them whereas D. discoideum slugs do not. After culmination, the fruiting bodies are similar in size and shape and both consist of a ball of spores (sorus) carried on top of a cellular stalk as indicated. They differ in that D. purpureum fruiting bodies lack a basal disc at the bottom of the stalk and their sori are purple rather than yellow. (b) Developmental morphologies. A top view with light microscopy of cells developing on dark nitrocellulose filters is shown. Species names and developmental times are indicated. Scale bar: 0.5 mm. (c) The heat maps represent the patterns of change in standardized mRNA abundance for all the genes in the D. discoideum and the D. purpureum genomes. Each row represents an average of 85 genes and each column represents a developmental time point (hours). The colors represent relative mRNA abundances (see scale). The genes are ordered according to their regulation pattern in each species. The black lines divide the transcripts, from top to bottom, into: down-regulated, intermediate regulation and up-regulated. The dendrograms represent the differences between the transcriptomes at each time point. (d) The maximal similarity between each D. purpureum developmental time point (x-axis) to each D. discoideum time point (y-axis) across the 7,560 orthologs. The dashed line represents a hypothetical comparison between perfectly synchronous developmental programs.

Figure 2

Conservation of regulation and function between D. discoideum and D. purpureum transcriptional profiles. We compared the similarity between the transcriptional profiles of orthologs from the two species. (a) The three-dimensional density plot represents the distribution of expression levels (x-axis, average read count) and of the similarities between the transcription profiles of the orthologs (y-axis, Pearson's correlation). The z-axis (gene count) represents the number of genes in each bin (defined by the black gridlines). The histogram behind the density plot summarizes the gene counts in four sections (separated by the yellow lines). The number of genes (top) and their fraction of the total (%) are indicated. (b) The bars represent the number of transcripts with various highly conserved expression patterns (gene counts indicated inside bars). (c) Prominent Gene Ontology terms enriched within each group. (d) Representative expression patterns in D. discoideum (yellow) and D. purpureum (purple). The time (hours; x-axis), relative mRNA abundance (y-axis), and gene names are indicated.

Figure 3

Conservation of transcript abundance between various species. (a) Scatter plot representing the abundance of the D. discoideum transcripts (x-axis, log₁₀ scale) compared to their D. purpureum orthologs (y-axis, log₁₀ scale). Each point represents the sum of read counts over the seven developmental time points. We divided the genes into three groups and indicated enriched Gene Ontology terms. Low abundance, <1,000 reads (green); intermediate abundance, 1,000 to 10,000 reads (blue); and high abundance, >10,000 reads (red). (b) We calculated the median gene abundance rank (y-axis, percentile) within five functional categories (indicated by the color code) in amoebae (D. discoideum and D. purpureum), mice (M. musculus), and yeast (S. cerevisiae), as indicated (x-axis). The asterisk indicates that only 21 genes represent this category in D. purpureum whereas the other species have >100 genes.

Figure 4

Conservation of cell-type specificity between D. discoideum and D. purpureum transcripts. Similarity between cell-type enriched orthologs. The yellow circle represents D. discoideum transcripts, the purple circle represents D. purpureum, and the overlap represents the conservation of cell-type-enriched genes. The differentially expressed genes within each set are divided into prespore enriched (green), prestalk enriched (red) and known markers (in parentheses).