Department of Biology, University of Massachusetts Boston, Boston, MA, USA.
Whitney Laboratory for Marine Bioscience, University of Florida, St. Augustine, FL, USA.
Mol Biol Evol. 2023 Jun 1;40(6). doi: 10.1093/molbev/msad137.
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.
基因表达的差异调控产生了地球上令人惊叹的生命多样性。因此，了解控制基因表达的机制创新的起源和进化对于进化和发育生物学来说是不可或缺的。细胞质多聚腺苷酸化是细胞质 mRNA 3'端多聚腺苷酸化的生化延伸。这个过程调节特定母本转录物的翻译，由细胞质多聚腺苷酸化元件结合蛋白家族（CPEBs）介导。编码 CPEB 的基因是少数存在于动物中而不存在于非动物谱系中的基因之一。细胞质多聚腺苷酸化是否存在于非双侧动物（即海绵、栉水母、扁盘动物和刺胞动物）中仍然未知。我们对 CPEB 进行了系统发育分析，结果表明 CPEB1 和 CPEB2 亚家族起源于动物的祖系。我们对海葵（刺胞动物）和栉水母（栉水母）的表达评估表明，CPEB1 和细胞质多聚腺苷酸化机制的催化亚基（GLD2）的母本表达是一种古老的特征，在动物中是保守的。此外，我们对 poly(A)-尾伸长的测量表明，细胞质多聚腺苷酸化的关键靶标在脊椎动物、刺胞动物和栉水母之间是共享的，这表明这种机制协调了一个在动物进化过程中保守的调控网络。我们假设，通过 CPEB 的细胞质多聚腺苷酸化是一种基本的创新，它促进了从单细胞生命到动物进化的过程。
