1. Introduction
Hook snout carp, Opsariichthys bidens Günther, an endemic Asiatic
cyprinid with high economic value, has become a commercially emerging
aquaculture fish. O. bidens inhabits the tributaries of rivers
and prefers to occupy mountainous streams. It has been cultured in large
mountain communities and has significantly increased farmer income in
the past two decades (Du, 2021; Fu et al., 2012). The hook snout carp is
a small to medium-sized fish distributed across China’s main drainages,
including the Jiulongjiang, Huaihe, Yellow, Yangtze, and Pearl rivers,
and expansions to Hainan drainages in China, Korea, Japan, and Vietnam
(Chen et al., 2018b). The long-distance dispersal distribution of hook
snout carp was driven by the uplift of the Qinghai-Tibet Plateau and
Pleistocene glacial cycles, causing morphological variations, such as
lateral line scales and shaped particular populations (Chen et al.,
2018b). Genetic diversity examined via mitochondria-based phylogeny has
revealed hook snout carp clustering in five different evolutionary
lineages (Perdices et al., 2005), revealing potential candidates for
fishery resources for hook snout carp breeding in the future.
O.
bidensexhibits
sexual dimorphism in growth, with male individuals showing faster growth
than females, possibly because of the sexually different systems (Potau
et al., 1999). Sex-related genes, such as dazl , dnd ,nanog , piwi , vasa , zp4 , amh ,cyp19a , and dmrt1 , were identified in hook snout carp
using transcription analysis (Tang et al., 2022b). In addition,
sex-biased miRNAs of O. bidens were investigated (Tang et al.,
2022a). Furthermore, most recently, long-term-cultured spermatogonia
stem cell line that could produce sperm in vitro was established
in O. bidens (Chen et al., 2022). Regarding the morphological
traits of hook snout carp, female individuals have plain bodies, while
male individuals have irregular dark bars aside from the body (Lian et
al., 2017; Xu et al., 2021). During the reproductive season,
male
individuals exhibit nuptial coloration on the sides of the body and the
surfaces of the head, pectoral, and extended-anal fins with nuptial
organs, which facilitates matching with females and improves
fertilization and reproductive success rates (Lian et al., 2017). This
reproductive strategy drives chromosome evolution by altering the
strength of sexually
antagonistic
selection (Kirkpatrick, 2017). However, the presumed sex-related
chromosomes of hook snout carp have not been previously identified,
hindering the deciphering of the sexual dimorphism mechanism of hook
snout carp due to the absence of a fully sequenced genome.
High-quality genome assembly at the chromosome level would be helpful
for aquaculture breeding and genetic research. The available genomes
were used as references for the genetic architecture of morphological
characters and dig-specific markers to help molecular breeding with
important traits (Fan et al., 2022). The whole genomes of economically
important aquaculture fishes, including the common carp Cyprinus
carpio Linnaeus (Xu et al., 2014), half-smooth tongue soleCynoglossus semilaevis (Chen et al., 2014), grass carpCtenopharyngodon idella (Valenciennes)(Wang et al., 2015),
Japanese flounder Paralichthys olivaceus (Shao et al., 2017) ,
yellow catfish Pelteobagrus fulvidraco (Gong et al., 2018), and
bighead carp Hypophthalmichthys nobilis (Richardson) (Jian et
al., 2021), gibel carp/Prussian carp Carassius gibelio (Wang et
al., 2022) have been released. Genetic analyses of complex traits,
including sex control, disease resistance, hypoxia tolerance, and feed
efficient utilization, have been widely performed, and breeding of a new
aquaculture variety is being conducted in fisheries, greatly relying on
genome data (Gui et al., 2022).
Although the female hook snout carp genome was presented in data format
(Xu et al., 2021), its annotation profile is still lacking. It is
limited to serving as a reference for finely mapping and characterizing
quantitative trait loci, sex-linked DNA markers, sex control, and
genetic breeding of hook snout carp. The female hook snout carp genome
is 814.71Mb and anchored to 39 chromosomes (2n = 78), the largest number
in the Danioninae subfamily (Chen, 1998; Xu et al., 2021). The diploid
chromosome number of hook snout carp varies in different populations: 74
for Sichuan in Yangtze River drainages, 76 for Guangdong in Pearl River
drainages, and
78
for Japan (Li and Li, 1987). The female O. bidens individuals
whose 78-chromosome genome has been sequenced were collected from
Zhejiang in the Yangtze River drainages (Xu et al., 2021). A few fish
species show different chromosome numbers due to sex chromosomes. For
example, a rocky reef fish, Oplegnathus fasciatus (Temminck and
Schlegel), showed 2n = 48 for female individuals and 47 for male
individuals because of a centric fusion of male acrocentric chromosomes
in the formation of the sex-determining system (Xiao et al., 2019). Sex
chromosomes are responsible for sex regulation and determination (Ueno
and Takai, 2008). Hook snout carp display a variety of chromosome
numbers, providing insight into the evolution of sex-related chromosomes
in fish.
Here, we report the chromosome-level genome assembly of male O.
bidens using Illumina short-read sequencing, Nanopore long-read
sequencing, and the Hi-C technique. The assembled genome of 992.9 Mb was
anchored to 38 chromosomes, corresponding to our karyotype analysis. In
total, 36,738 functional genes were identified. This allowed us to
further discover male hormone release via the gonadotropin-releasing
hormone (GnRH) pathway, which plays a vital role in developing secondary
sex characteristics in O. bidens . For the first time, we
identified a reunion of male chromosomes carrying expanded genes
involved in the GnRH pathway by synteny-based chromosome comparison
between male and female O. bidens . In addition, the genome of
male O. bidens compared to that of C. idella showed that
the chromosome broke off to increase the chromosome number during the
evolutionary history of fish. The male O. bidens genome provides
valuable genomic data for further studies on conservation genetics,
sex-determining mechanisms, and all-male and hypoxia-resistant breeding.