Abstract
BackgroundInsertions of spliceosomal introns are very rare events during evolution of vertebrates and the mechanisms governing creation of novel intron(s) remain obscure. Largely, gene structures of melanocortin (MC) receptors are characterized by intron-less architecture. However, recently a few exceptions have been reported in some fishes. This warrants a systematic survey of MC receptors for understanding intron insertion events during vertebrate evolution.Methodology/Principal FindingsWe have compiled an extended list of MC receptors from different vertebrate genomes with variations in fishes. Notably, the closely linked MC2Rs and MC5Rs from a group of ray-finned fishes have three and one intron insertion(s), respectively, with conserved positions and intron phase. In both genes, one novel insertion was in the highly conserved DRY motif at the end of helix TM3. Further, the proto-splice site MAG↑R is maintained at intron insertion sites in these two genes. However, the orthologs of these receptors from zebrafish and tetrapods are intron-less, suggesting these introns are simultaneously created in selected fishes. Surprisingly, these novel introns are traceable only in four fish genomes. We found that these fish genomes are severely compacted after the separation from zebrafish. Furthermore, we also report novel intron insertions in P2Y receptors and in CHRM3. Finally, we report ultrasmall introns in MC2R genes from selected fishes.Conclusions/SignificanceThe current repository of MC receptors illustrates that fishes have no MC3R ortholog. MC2R, MC5R, P2Y receptors and CHRM3 have novel intron insertions only in ray-finned fishes that underwent genome compaction. These receptors share one intron at an identical position suggestive of being inserted contemporaneously. In addition to repetitive elements, genome compaction is now believed to be a new hallmark that promotes intron insertions, as it requires rapid DNA breakage and subsequent repair processes to gain back normal functionality.
Highlights
Spliceosomal introns are associated with a well-defined splicing machinery in the nuclear genomes of all characterized eukaryotes, but the origin of these introns remains a puzzle [1,2,3]
When we traced for MC receptors in basal fishes, we detected three MC receptors, which are similar to melanocortin 1 receptor (MC1R) (AAVX01456471.1, length- 854 bp), MC3R (AAVX01131452.1, length- 1728 bp) and MC5R (AAVX01069419.1, length- 4869 bp) from the elephant shark (Callorhinchus milii) genome
The missing MC5R and MC2R from anole lizard and the frog genomes, respectively are due to the fragmental nature of current genome assembly of these two organisms. When we searched this genomic fragment in different fish genomes, we found that the closely linked MC5R and MC2R genes are conserved on a similar fragment in T. rubripes, O. latipes and G. aculeatus
Summary
Spliceosomal introns are associated with a well-defined splicing machinery in the nuclear genomes of all characterized eukaryotes, but the origin of these introns remains a puzzle [1,2,3]. Insertion or deletions of spliceosomal introns are rare events in evolution. Intron insertions have been reported to be very rare in many metazoan lineages, including mammals and other vertebrates [5,6,7]. Definitive evolutionary processes governing novel intron acquisition in vertebrate genomes have largely remained elusive [1]. Insertions of spliceosomal introns are very rare events during evolution of vertebrates and the mechanisms governing creation of novel intron(s) remain obscure. Recently a few exceptions have been reported in some fishes This warrants a systematic survey of MC receptors for understanding intron insertion events during vertebrate evolution
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