Gildor T et al. (2019), Developmental transcriptomes of the sea star, P...

ECB-ART-48291

Sci Rep 2019 Nov 07;91:16201. doi: 10.1038/s41598-019-52577-9.

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Developmental transcriptomes of the sea star, Patiria miniata, illuminate how gene expression changes with evolutionary distance.

Gildor T , Cary GA , Lalzar M , Hinman VF , Ben-Tabou de-Leon S .

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Understanding how changes in developmental gene expression alter morphogenesis is a fundamental problem in development and evolution. A promising approach to address this problem is to compare the developmental transcriptomes between related species. The echinoderm phylum consists of several model species that have significantly contributed to the understanding of gene regulation and evolution. Particularly, the regulatory networks of the sea star, Patiria miniata (P. miniata), have been extensively studied, however developmental transcriptomes for this species were lacking. Here we generated developmental transcriptomes of P. miniata and compared these with those of two sea urchins species. We demonstrate that the conservation of gene expression depends on gene function, cell type and evolutionary distance. With increasing evolutionary distance the interspecies correlations in gene expression decreases. The reduction is more severe in the correlations between morphologically equivalent stages (diagonal elements) than in the correlation between morphologically distinct stages (off-diagonal elements). This could reflect a decrease in the morphological constraints compared to other constraints that shape gene expression at large evolutionary divergence. Within this trend, the interspecies correlations of developmental control genes maintain their diagonality at large evolutionary distance, and peak at the onset of gastrulation, supporting the hourglass model of phylotypic stage conservation.

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Genes referenced: LOC100887844 LOC115919910 LOC115925415 LOC583082 srpl

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	Figure 1. Developmental time points studied and examples for gene expression profiles on the three species. (A) Images of adult and larval stage of P. miniata, P. lividus and S. purpuratus. Arrows point to the sea urchin skeletogenic rods and arrow heads point to the sea urchin pigments. (B) Images of P. miniata, P. lividus and S. purpuratus embryos at the developmental stages that were studied in this work. Time point 6 hpf in S. purpuratus does not have RNA-seq data. (C) Relative gene expression in the three species measured in the current paper by RNA-seq for P. miniata (orange curves), by RNA-seq for P. lividus19 (purple curves) and by nanostring for S. purpuratus28 (black curves). Error bars indicate standard deviation. To obtain relative expression levels for each species we divide the level at each time point in the maximal mRNA level measured for this species in this time interval; so 1 is the maximal expression in this time interval.
	Figure 2. Venn diagram and NMDS analysis of 1:1:1 homologous genes. (A) Venn diagram showing the number of 1:1:1 homologous genes expressed in all three species, in two of the species or only in one species. (B) First two principal components of expression variation (NMDS) between different developmental time points in P. miniata (orange), P. lividus (purple) and S. purpuratus (black).
	Figure 3. Interspecies Pearson correlations for different GO terms, ordered by the level of matrix diagonality (MD) of Pl-Sp matrices. In each panel, from (A–J) we present the Pearson correlation of the expression levels of genes with specific GO term between different developmental stages in two species. Upper matrix in each panel shows the Pearson correlation between the two sea urchins (P. lividus and S. purpuratus) and the bottom matrix is the Pearson correlation between the sea star, P. miniata and the sea urchin P. lividus. These matrices include the seven developmental points that have RNA-seq data in all species (Fig. 1B, excluding 9 hpf in P. miniata and 4 hpf in P. lividus). In each panel we indicate the GO term tested, the number of genes in each set, the average correlation strength in the diagonal (AC) and the matrix diagonality (MD), see text for explanation. Linear color scale of Pearson correlations 0–1 is identical for all graphs and given at the middle of the figure. (F) Shows the Pearson interspecies correlation for all 1:1:1 genes.
	Figure 4. The average correlation strength and the matrix diagonality are independent parameters that reflect different properties of expression conservation. (A) The average correlation strength (AC) between Pl-Sp (black bars) and Pl-Pm (red bars) in receding order of Pl-Pm correlation strength. Error bars indicate standard deviation of the correlation strength along the matrix diagonal. (B) Matrix diagonality (MD) of the interspecies correlations between Pl-Sp (black bars) and Pl-Pm (cyan bars) in receding order of Pl-Pm matrix diagonality. In (A,B) the different gene sets are colored by the following key: developmental GO terms in green, housekeeping GO terms in blue, lineage specific genes in red and all the other sets in black. (C) The matrix diagonality changes independently of the average correlation for both Pl-Sp (black dots) and Pl-Pm (orange dots). (D) The interspecies average correlation between S. purpuratus and P. lividus corresponds to the interspecies average correlation between P. lividus and P. miniata (R pearson = 0.68). (E) The matrix diagonality of the interspecies correlations between S. purpuratus and P. lividus relates to the matrix diagonality between P. lividus and P. miniata (R Pearson = 0.78). In (D,E) we didn’t include the skeletogenic lineage data point as it is an outlier.
	Figure 5. The correlation matrix diagonality, MD, reflects how the dominance between cellular and developmental constraints changes with evolutionary distance. Illustration of typical interspecies correlation matrices of developmental control genes and housekeeping genes between closely related and further diverged species (upper and lower panels, respectively). With increasing evolutionary distance, that is, between the sea urchin and the sea star, the average correlation and the diagonality decrease for all gene sets but the diagonality of developmental control genes is least affected and they still maintain the hourglass pattern (left panels). On the other hand, the interspecies correlation matrices of housekeeping genes are strong and non-diagonal even between the two sea urchins and remain non-diagonal between the sea urchin and the sea star (right panels).

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Anders, HTSeq--a Python framework to work with high-throughput sequencing data. 2015, Pubmed