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. 2018 Apr 24;115(17):4459-4464.
doi: 10.1073/pnas.1720817115. Epub 2018 Apr 6.

The gene regulatory program of Acrobeloides nanus reveals conservation of phylum-specific expression

Philipp H Schiffer  1 , Avital L Polsky  2 , Alison G Cole  3 , Julia I R Camps  4 , Michael Kroiher  5 , David H Silver  2 , Vladislav Grishkevich  2 , Leon Anavy  2 , Georgios Koutsovoulos  6 , Tamar Hashimshony  2 , Itai Yanai  7
Affiliations

The gene regulatory program of Acrobeloides nanus reveals conservation of phylum-specific expression

Philipp H Schiffer et al. Proc Natl Acad Sci U S A. .

Abstract

The evolution of development has been studied through the lens of gene regulation by examining either closely related species or extremely distant animals of different phyla. In nematodes, detailed cell- and stage-specific expression analyses are focused on the model Caenorhabditis elegans, in part leading to the view that the developmental expression of gene cascades in this species is archetypic for the phylum. Here, we compared two species of an intermediate evolutionary distance: the nematodes C. elegans (clade V) and Acrobeloides nanus (clade IV). To examine A. nanus molecularly, we sequenced its genome and identified the expression profiles of all genes throughout embryogenesis. In comparison with C. elegans, A. nanus exhibits a much slower embryonic development and has a capacity for regulative compensation of missing early cells. We detected conserved stages between these species at the transcriptome level, as well as a prominent middevelopmental transition, at which point the two species converge in terms of their gene expression. Interestingly, we found that genes originating at the dawn of the Ecdysozoa supergroup show the least expression divergence between these two species. This led us to detect a correlation between the time of expression of a gene and its phylogenetic age: evolutionarily ancient and young genes are enriched for expression in early and late embryogenesis, respectively, whereas Ecdysozoa-specific genes are enriched for expression during the middevelopmental transition. Our results characterize the developmental constraints operating on each individual embryo in terms of developmental stages and genetic evolutionary history.

Keywords: Nematoda; development; developmental constraints; evolution; gene expression.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
The genome of the nematode A. nanus in comparison with that of other nematodes. (A) Phylogenetic tree of the indicated species. Roman numerals indicate clades according to ref. . Genome sizes, N50 of the assembly, repeats (23, 50), protein count, and number of orthologs with A. nanus are indicated in the table (see SI Experimental Procedures, #except for S. carpocapsae data, where 1–1 orthologs from ref. are given). (B) Scatter plot of gene family sizes between A. nanus and C. elegans. Differentially enriched families are indicated by color. Larger circles indicate specific families: PF00001, Rhodopsin-like receptors; PF00001, ABC transporters; PF00011, Hsp20/alpha crystallin family; PF00012, Hsp70 protein; PF00096, zinc finger; C2H2 type; PF000232, glycosyl hydrolase family 1, transcription factors; PF00651, overrepresented Pfam domains between A. nanus and C. elegans.
Fig. 2.
Fig. 2.
Single-cell A. nanus blastomere analysis. (A) The two-cell stage in A. nanus and C. elegans, indicating also the AB and P1 blastomeres. Embryos are 50 µm in length. (B) Heat map showing correlation coefficients among the A. nanus transcriptomes of five AB blastomeres and three P1 blastomeres. (C) Comparison of the A. nanus gene expression levels between the AB and P1 blastomeres. Expression levels are computed as transcripts per million (tpm; SI Experimental Procedures). Genes of the indicated functional groups are highlighted. (D) Ratios of expression between AB and P1 in C. elegans and A. nanus, respectively. The red box indicates genes with high P1 expression only in A. nanus.
Fig. 3.
Fig. 3.
A gene expression developmental time-course for A. nanus embryogenesis. (A) Micrographs of A. nanus embryos at the indicated stages. (B) RNA-Seq of 81 randomly collected A. nanus embryos. The embryos were sorted according to BLIND. (C) A correlation matrix of the BLIND-sorted A. nanus transcriptomes. Note the sharp transitions after the one- to eight-cell stages and then again at morphogenesis.
Fig. 4.
Fig. 4.
Expression of homeodomain genes between A. nanus and C. elegans. (A) Comparison of temporal expression of selected orthologous genes in A. nanus and C. elegans. Specific homeodomain genes that were further analyzed by in situ (B) are emphasized with dotted outlines. (B) In situ hybridizations for ceh-20 and ceh-34 orthologs in A. nanus.
Fig. 5.
Fig. 5.
Expression divergence between the developmental transcriptomes of C. elegans and A. nanus. (A) Developmental transcriptome of A. nanus. Genes are sorted by the Zavit method (2). (B) Developmental transcriptome of the C. elegans orthologs of A. nanus, sorted as in A. nanus. Arrows indicate orthologs. (C) Developmental transcriptome of the C. elegans orthologs sorted independent of A. nanus. Arrows indicate corresponding genes, sorted in C according to C. elegans time. (D) Box plots indicating the expression divergences between genes in A and C for stages along development. Developmental stages are indicated on the right (Mat., maternal; early; gastrula; Mid-dev., middevelopmental transition; Morphog., morphogenesis; and larva). Note the increased relative conservation of genes expressed early and at middevelopmental transition.
Fig. 6.
Fig. 6.
Ecdysozoan- and Nematode-specific genes are more conserved in their expression between C. elegans and A. nanus. (A) Genes were grouped according to their phylostratigraphic age (Left, see SI Experimental Procedures). Expression divergence index (ED) of C. elegans and A. nanus orthologs in comparison with their phylostratigraphic age. Phylostratigraphic age was calculated by blasting against a previously reported database (47) using the Phylostratigraphy software (https://github.com/AlexGa/Phylostratigraphy.git). A statistical test of difference in ED distributions for phylostratigraphic nodes revealed significance of divergence for comparisons in Nematoda, but not for genes that evolved before the phylum. The ED appears to follow an hourglass shape through evolutionary time, with evolutionary very old and young genes showing less constrained ED than those acquired on intermediate nodes in Nematoda. (B) Average expression profiles of genes of a common phylostratigraphic age for the three indicated species. Black dots indicate the stage for each category at which average expression is at its maximum.
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