RNA-editing frequency is very high among octopus and squid: Do they differ from other Classes of animals?

The Golden Rule used to be that “all information needed for any phenotype (trait) is right there in our DNA.” Then the concept of epigenetic effects started raising its ugly head. “Epigenetics” represents genetic regulation outside of what can be seen in the DNA sequence. Epigenetics currently includes DNA methylation, RNA-interference (RNAi), histone modification, and chromatin remodeling.

DNA sequence (i.e.”the genome”) is the same in every DNA-containing cell in our bodies, whereas “the epigenome” can vary in each of human’s ~200 different cell-types throughout the body. Hence, each of us has one genome (or two haploid genomes) and ~200 epigenomes, the latter able to be modified by environmental effects. Therefore, any trait –– such as response to a drug or other environmental agent –– depends on the contribution of all genomic, epigenomic and environmental effects.

RNA-editing, a post-transcriptional process, falls in the category of RNAi. RNA-editing allows diversification of proteomes beyond “the genomic blueprint.” There have been some recent reports suggesting increased levels of RNA-editing in squids, thus raising the question of the nature and effects of these events. Authors [see attached] show that RNA-editing is especially common in behaviorally sophisticated coleoid cephalopods,

A cephalopod is any member of the molluscan class Cephalopoda, exclusively marine animals characterized by bilateral body symmetry, a prominent head, and set of arms or tentacles modified from the primitive molluscan foot (e.g. octopus, squid). Cephalopods exhibit tens of thousands of evolutionarily-conserved RNA-editing sites. Their editing is particularly enriched in the nervous system, affecting molecules pertinent for excitability and neuronal morphology. The genomic sequence that flanks editing sites is highly conserved –– suggesting that the process confers a selective advantage.

Due to the large number of RNA-editing sites, the surrounding conservation greatly decreases the number of mutations and genomic polymorphisms in protein-coding regions. This trade-off between genome evolution and transcriptome plasticity highlights the importance of RNA recoding as a strategy for diversifying proteins, particularly those associated with neural function. These data are also consistent with numerous stories about the personalities and very high intelligence of octopuses in captivity.

Cell 544: 169–202.e11 (2017)

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