High‐quality chromosome‐level genomes of two tilapia species reveal their evolution of repeat sequences and sex chromosomes

Abstract

Tilapias are one of the most farmed fishes that are coined as “aquatic chicken” by the food industry. Nile tilapia and blue tilapia exhibit very recent transition of sex chromosome systems since their divergence approximately five million years ago, making them a great model for elucidating the molecular and evolutionary mechanisms of sex chromosome turnovers. Studies of their sex‐determining pathways are also critical for developing genetic sex control in aquaculture. We report here the newly produced genomes of Nile tilapia and blue tilapia that integrate long‐read sequencing and chromatin conformation data. The two nearly complete genomes have anchored over 97% of the sequences into linkage groups (LGs), and assembled majorities of complex repetitive regions including telomeres, centromeres and rDNA clusters. In particular, we inferred two episodes of repeat expansion at LG3 respectively in the ancestor of cichlids and that of tilapias. The consequential large heterochromatic region concentrated at one end of LG3 comprises tandem arrays of mRNA and small RNA genes, among which we have identified a candidate female determining gene Paics in blue tilapia. Paics shows female‐specific patterns of single‐nucleotide variants, copy numbers and expression patterns in gonads during early gonadogenesis. Our work provides a very important genomic resource for functional studies of cichlids, and suggested that unequal distribution of repeat content that impacts the local recombination rate might make some chromosomes more likely to become sex chromosomes.

Gene Variant of Barrier to Autointegration Factor 2 (Banf2w) Is Concordant with Female Determination in Cichlids

“…The Ychromosome (LG23Y) carries an extra copy of anti-Müllerian hormone (amh), which is different from the regular amh gene due to a 5 bp insertion and a 232 bp deletion in exons 6 and 7, respectively [26,34,36]. The WZ/ZZ system on LG3 was initially studied 40 years ago using sex-reversal and gynogenetic techniques and has attracted many studies since [31,37,38,[40][41][42][43][44][45][46]. However, the effective MKR has not been found due to the size and complexity of LG3.…”

“…However, the effective MKR has not been found due to the size and complexity of LG3. LG3 is considered to be a mega-chromosome with a high proportion of repetitive elements, recombination repression and a limited feasibility for genetic mapping [41,43]. Indeed, sex chromosomes and sex-determining regions demonstrate a common recombination repression phenomenon during meiosis [47,48].…”

“…A recent study has reduced the SD critical region of Oa to 9.2 Mbp [42,43], and, most importantly, it has also identified an embedded critical region with a high female-specific variation density, which harbors only three genes: banf2, paics-1 and paics-2. The same study suggests paics as a candidate gene for the SD MKR based on chromosomal linkage and the sex-specific expression profile, although mammalian PAICS is known to encode the phosphoribosylaminoimidazole carboxylase that participates in the purine biosynthesis without sex-related functions [43].…”

“…In the current study, we focused on the genomic region on LG3 noted by Tao et al for its high density of female-specific patterns of nucleotide variation [43]. To map the SD region, we used a hybrid Oa stock with a restored mono-factorial SD locus, which demonstrated a release of recombination repression in the SD region [29].…”

Telomere-to-telomere assembly of a fish Y chromosome reveals the origin of a young sex chromosome pair

“…We used Last (1042) [72] to align the genomes of seven species, swamp eel (Monopterus albus) [73], Nile tilapia (Oreochromis niloticus) [37], yellow perch (Perca flavescens) [74], threespine stickleback (Gasterosteus aculeatus) [21], yellowbelly pufferfish (Takifugu flavidus) [75], big-bellied seahorse (Hippocampus abdominalis), and pricklefish (Acanthochaenus luetkenii) [36], against the hap-Y genome with the option "-m100 -E0.05 -C2". The one-to-one best alignments were retained to build 7-way multiple alignments using MULTIZ (v11.2) [76].…”