Cytoplasmic Polyadenylation Is an Ancestral Hallmark of Early Development in Animals

Author:

Rouhana Labib1ORCID,Edgar Allison2,Hugosson Fredrik2,Dountcheva Valeria1,Martindale Mark Q23,Ryan Joseph F23ORCID

Affiliation:

1. Department of Biology, University of Massachusetts Boston , Boston, MA , USA

2. Whitney Laboratory for Marine Bioscience, University of Florida , St. Augustine, FL , USA

3. Department of Biology, University of Florida , Gainesville, FL , USA

Abstract

Abstract Differential regulation of gene expression has produced the astonishing diversity of life on Earth. Understanding the origin and evolution of mechanistic innovations for control of gene expression is therefore integral to evolutionary and developmental biology. Cytoplasmic polyadenylation is the biochemical extension of polyadenosine at the 3′-end of cytoplasmic mRNAs. This process regulates the translation of specific maternal transcripts and is mediated by the Cytoplasmic Polyadenylation Element-Binding Protein family (CPEBs). Genes that code for CPEBs are amongst a very few that are present in animals but missing in nonanimal lineages. Whether cytoplasmic polyadenylation is present in non-bilaterian animals (i.e., sponges, ctenophores, placozoans, and cnidarians) remains unknown. We have conducted phylogenetic analyses of CPEBs, and our results show that CPEB1 and CPEB2 subfamilies originated in the animal stem lineage. Our assessment of expression in the sea anemone, Nematostella vectensis (Cnidaria), and the comb jelly, Mnemiopsis leidyi (Ctenophora), demonstrates that maternal expression of CPEB1 and the catalytic subunit of the cytoplasmic polyadenylation machinery (GLD2) is an ancient feature that is conserved across animals. Furthermore, our measurements of poly(A)-tail elongation reveal that key targets of cytoplasmic polyadenylation are shared between vertebrates, cnidarians, and ctenophores, indicating that this mechanism orchestrates a regulatory network that is conserved throughout animal evolution. We postulate that cytoplasmic polyadenylation through CPEBs was a fundamental innovation that contributed to animal evolution from unicellular life.

Funder

The Eunice Kennedy Shriver National Institute of Child Health and Human Development of the National Institutes of Health

Paul G. Allen Family Foundation

National Science Foundation

National Aeronautics and Space Administration

National Science Foundation Postdoctoral Research Fellowship in Biology

Publisher

Oxford University Press (OUP)

Subject

Genetics,Molecular Biology,Ecology, Evolution, Behavior and Systematics

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