NEW YORK (GenomeWeb) – The octopus genome is marked by widespread genomic rearrangements as well as expansions in gene families involved in development, particularly neuronal development, according to researchers led by the University of California, Berkeley's Daniel Rokhsar.
As reported in Nature today, Rokhsar and his colleagues sequenced the genome of the California two-spot octopus, Octopus bimaculoides, to find widespread genomic reorganization and expansion of certain gene families, but no evidence of a previously suggested genome duplication event. Instead, the researchers said it's more likely that the octopus genome was shaped by those rearrangements and gene family expansions, along with the evolution of novel genes and modification of gene regulatory networks.
"With a few notable exceptions, the octopus basically has a normal invertebrate genome that's just been completely rearranged, like it's been put into a blender and mixed," co-first author Caroline Albertin, a graduate student at the University of Chicago, said in a statement. "This leads to genes being placed in new genomic environments with different regulatory elements, and was a completely unexpected finding."
The researchers sequenced O. bimaculoides to about 60-fold coverage and annotated it using transcriptome sequences from a dozen tissues, including developing fetal tissue, suckers, and brain and nerve tissues. From this, they estimated that the octopus genome contains some 33,638 protein-coding genes. They also noted that about 45 percent of the assembled genome is made of repetitive elements, with two bursts of transposon activity tracing back about 25 million and 56 million years ago.
Because of the number of chromosomes the octopus has, it's been suspected that whole-genome duplication may have been a key step in the evolution of the cephalopod body plan. However, Rokhsar and his colleagues reported finding no evidence of such a duplication.
Gene family expansions in the octopus genome, they noted, are organized in clusters, rather than in doubly conserved synteny, as would be expected for a paleopolyploid. In addition, O. bimaculoides only has a single Hox complement, while other organisms that have undergone whole-genome duplications typically retain multiple Hox copies.
Instead, they said that other factors have likely been at play in shaping the octopus genome.
For instance, though the octopus genome is broadly similar to those of the limpet Lottia gigantea, the polychaete annelid Capitella teleta, and the cephalochordate Branchiostoma floridae, the researchers noted gene family expansions affecting protocadherins, C2H2 zinc-finger proteins, interleukin-17-like genes, G-protein-coupled receptors, chitinases, and sialins.
In particular, the octopus genome encodes 168 multi-exonic protocadherin genes, some 10 times more that what's found in the Lottia, Crassostrea gigas, and Capitella genomes and twice as many as found in many mammals. Protocadherins, the researchers noted, are essential for neuronal development and survival in vertebrates, which also show similar protocadherin gene expansions.
The researchers noted that as cephalopod neurons lack myelin, protocadherins could've been important in the evolution of a nervous system that relies on short-range interactions.
Rokhsar and his colleagues noted that the C2H2 ZNFs expansion is greater in octopuses than in other lophotrochozoans and most mammals, and dates back to the burst of transposon activity in the octopus genome some 25 million years ago. In addition, they reported that most of these transcripts are expressed in embryonic and nervous tissue, which they said is consistent with the presumed activity of C2H2 ZNFs in cell fate determination, early development, and transposon silencing.
The researchers surveyed other genes linked to nervous system development to find that neurotransmission gene family sizes in octopus are comparable to those of other lophotrochozoans. They did, though, uncover a set of atypical nicotinic acetylcholine receptor-like genes in tandem array clusters. As these subunits lacked several residues needed to bind acetylcholine and as they were highly expressed in suckers, the researchers hypothesized that they could instead function as sensory receptors that enable octopuses to taste with their suckers.
They also noted the influence of transposon activity on the octopus genome, particularly that a class of short interspersed nuclear element sequences specific to octopus that was highly expressed in neural tissues. In addition, they found that transposon activity appeared to have altered gene regulation in octopus.
"Our analysis suggests that substantial expansion of a handful of gene families, along with extensive remodeling of genome linkage and repetitive content, played a critical role in the evolution of cephalopod morphological innovations, including their large and complex nervous systems," Rokhsar and his colleagues said in their paper.