Diversity of PBI-DdeI satellite DNA in snakes correlates with rapid independent evolution and different functional roles

Abstract

To better understand PBI-DdeI satellite DNA located in the centromeric region of python, molecular evolution analysis was conducted on 40 snake species. A ladder-like pattern of DNA bands with repetition of the 194–210 bp monomer was observed in 15 species using PCR. Molecular cloning was performed to obtain 97 AT-rich monomer sequences. Phylogenetic and network analyses showed three PBI-DdeI subfamilies with sequences grouped in species-specific clusters, suggesting rapid evolution. Slow evolution was found in eight species with shared PBI-DdeI sequences, suggesting recent species diversification, allowing PBI-DdeI no time to diverge, with limited homogenization and fixation processes. Quantitative real-time PCR showed large differences in copy number between Python bivittatus and other snakes, consistent with repeat scanning of whole genome sequences. Copy numbers were significantly higher in female Naja kaouthia than in males, concurring with chromosomal distribution of PBI-DdeI specifically localized to female W chromosomes. PBI-DdeI might act as an evolutionary driver with several repeats to promote W chromosome differentiation and heterochromatinization in N. kaouthia. Analysis revealed PBI-DdeI with a reduced copy number, compared to P. bivittatus, in most snakes studied, and it is possible that it subsequently dispersed and amplified on W chromosomes with different functional roles in N. kaouthia.

Consequence of Paradigm Shift with Repeat Landscapes in Reptiles: Powerful Facilitators of Chromosomal Rearrangements for Diversity and Evolution

“…Their results indicate high variation in copy number between P. bivittatus and other snakes. The PBI-DdeI satellites identified in scaffolds account for approximately 0.353% (5.070 Mb) of the P. bivittatus genome, which differs from the copy number estimated by quantitative PCR of approximately 5.73 × 10 6 copies accounting for 82.53% of the genome [36]. This specific satellite is not identified in any of the genome sequences for snakes, although the PCR approach has successfully detected satellites of many snake species.…”

“…These satellite families include (1) PFL-MspI (168 bp) from Protobothrops flavoviridis, (2) PBI-DdeI (196 bp), and (3) PBI-MspI (174 bp) from Python bivittatus. Thongchum and co-workers [36] studied 40 snake species to gain an improved understanding of the conservation of PBI-DdeI satellite evolution and function. Their results indicate high variation in copy number between P. bivittatus and other snakes.…”

“…Interestingly, PBI-DdeI satellites are frequently localized to the W sex chromosome of Naja kaouthia. Localization of high copy numbers in female rather than male individuals suggests that PBI-DdeI might act as an evolutionary driver with several repeats and facilitate W chromosome differentiation and heterochromatinization [20,21,36]. Satellites have been extensively studied in lacertids [103][104][105][106][107][108][109][110][111], scincids [102,108], and varanids [40,70].…”

“…Why these repeats are preferentially clustered in sex-linked regions remains unclear. One hypothesis states that amplification of these repeats might promote the suppression of recombination and result in the genetic degradation of Y or W and, ultimately, a heteromorphic sex chromosome system might evolve [20,21,36,45,69,177]. Chromosomal changes, including larger inversions and deletions mediated by TE activity, have also been linked to sex chromosome differentiation and evolution [20,179].…”

“…This finding suggests that repeats on the snake W chromosome also share sex chromosomal linkage homology to SR2 and GGAZ. Such repeats (the telomeric sequence, (GATA) n , (AAGG) n , and (ACAG) n ) are commonly observed in snake W chromosomes and also in neognathous birds [20,36,38,78,193,194] although the repeats are non-homologous. Similarly, bird and snake W chromosomes share blocks of three repeats (Bkm repeats, 18S-related repeats, and DMRT-related repeats) [185].…”