4.3 Mechanism underlying O. bidens chromosome number
variety
During
vertebrate evolution, the entire genome has undergone two rounds (2R) of
duplication, and fish-specific genome duplication, namely the third
round of whole-genome duplication (3R) approximately 320 million years
ago, subsequently developed into new diploids (Meyer and Van de Peer,
2005). Therefore, most teleosts carry about 50 chromosomes in diploid
fish species (Jaillon et al., 2004). The 4R has occurred in certain
Cyprinidae fish, resulting in palaeopolyploids with 100 chromosomes in
their nuclear genome, such as the common carp C. carpio andS. rhinocerous in the tetraploidized chromosome (David et al.,
2003; Meyer and Van de Peer, 2005; Wang et al., 2012; Xu et al., 2014).
Multiple
rounds of whole genome duplication produce redundant genes that provide
important genetic material for phenotypic complexity, which would
potentially benefit an organism in its molecular functions.
Interestingly,
the Cyprinid fishO.
bidens is an exception, and different populations show various
chromosome numbers (between 74 and 78) (Li and Li, 1987). The
chromosomal evolution of Cyprinid remains a subject of debate.
Recently, the released genome of female O. bidens has provided an
opportunity to investigate the mechanism underlying chromosome changes
(Xu et al., 2021). The female O. bidens carried 39 (2n = 78)
chromosomes. In comparison, the male O. bidens carried 38 (2n =
76) chromosomes in the present study, suggesting a difference in the
regulation of sexual dimorphism in hook snout carp at the chromosomal
level. The male O. bidens LG06 chromosome was a reunion of female
GH14 and GH38 chromosomes and showed more than 97% sequence similarity
between males and females. Male LG06-special genes have two functions in
chromosome replication, recombination, and repair, and one well-known
DNA polymerase epsilon subunit 2 (pole2). Pole2 is required for cell
growth, chromosomal DNA replication, and double-strand break repair
(Hashimoto et al., 2003), indicating the fidelity of the reunion
chromosomes provided by pole2 gene function. It has been verified thatO. fasciatus, which possesses 2n = 47 in males and 2n = 48 in
females, carries a large metacentric Y chromosome (Xiao et al., 2020).
Different karyotypes in O. punctatus are responsible for the
genome size discrepancy between male and female individuals (Xu et al.,
2019). This suggests that O. bidens has a sex-dependent system.
In the male O. bidens genome, GnRH-induced hormone-releasing
related gene families underwent expansions, and up to seven expanded
genes were distributed in the LG06 chromosome, and LG06 was a reunion of
female O. bidens GH14 and GH38 chromosomes. Therefore, it is
reasonable to regard LG06 as a sexual dimorphic chromosome, and the
related molecular mechanisms are worth investigating in future studies.
The hook snout carp displayed an atypical karyotype of 3R. Our genome
assembly for male O. bidens led to 38 chromosomes, directly
corresponding to male karyotypes (2n = 76). Although different
populations carry different chromosome numbers, the fundamental arm
number of their karyotypes is 86 (Li and Li, 1987; Li et al., 1985). The
leuciscin fishes, including Ochetobius elongatus (Kner),Luciobrama macrocephalus (Lacepède), Elopichthys bambusa(Richardson), Squaliobarbus curriculus (Richardson), and C.
idellus, carry 2n = 48 chromosomes, with fundamental arm numbers of 74,
82, 82,90, and 92 (Li et al., 1985). Hook snout carp have similar
fundamental arm numbers to Leuciscin fishes, suggesting that the 76
chromosomes of male O. bidens resulted from the 2n = 48
chromosomes of Leuciscin fishes by breakage at centromere sites.
Considering that C. idellus is regarded as a primitive species in
Leuciscin fish species evolution (Wu et al., 2022), the synteny-based
chromosome comparison between male O. bidens and C.
idellus showed that out of the 24 chromosomes in C. idellus , one
breakage into two chromosomes occurred in 12 chromosomes, providing
evidence of added chromosome number via breakage. Our results could
serve as a framework for studies on sex-determining mechanisms and
genome evolution in fish.