Transcriptomic Profiling of Gametogenesis in Triploid Pacific Oysters Crassostrea gigas: Towards an Understanding of Partial Sterility Associated with Triploidy

Abstract

BackgroundTriploidy can occur in many animal species but is often lethal. Among invertebrates, amphibians and fishes, triploids are viable although often sterile or infertile. Most triploids of the Pacific oyster Crassostrea gigas are almost sterile (named “3nβ”) yet a low but significant proportion show an advanced gametogenesis (named “3nα”). These oysters thus constitute an interesting model to study the effect of triploidy on germ cell development. We used microarrays to compare the gonad transcriptomes of diploid 2n and the abovementioned triploid 3nβ and 3nα male and female oysters throughout gametogenesis.ResultsAll triploids displayed an upregulation of genes related to DNA repair and apoptosis and a downregulation of genes associated with cell division. The comparison of 3nα and 3nβ transcriptomes with 2n revealed the likely involvement of a cell cycle checkpoint during mitosis in the successful but delayed development of gonads in 3nα individuals. In contrast, a disruption of sex differentiation mechanisms may explain the sterility of 3nβ individuals with 3nβ females expressing male-specific genes and 3nβ males expressing female-specific genes.ConclusionsThe disruption of sex differentiation and mitosis may be responsible for the impaired gametogenesis of triploid Pacific oysters. The function of the numerous candidate genes identified in our study should now be studied in detail in order to elucidate their role in sex determination, mitosis/meiosis control, pachytene cell cycle checkpoint, and the control of DNA repair/apoptosis.

GigaTON: an extensive publicly searchable database providing a new reference transcriptome in the pacific oyster Crassostrea gigas

“…In this context, knowledge about the physiology of C. gigas is of fundamental, ecological and applied interests, leading to the generation of an important amount of transcriptomic data, as illustrated by the Gigasdatabase expressed-sequenced tags (EST) database [ 1 ]. These ESTs have enabled the development of microarrays used in physiological studies notably focusing on reproduction [ 2 , 3 ], resistance to summer mortality [ 4 – 6 ], hypoxia [ 7 ], thermal stress [ 8 ] or ploïdy [ 9 ]. Additionally, MPSS or RNA-Seq analyses have been performed to investigate molecular processes involved in larval growth heterosis [ 10 ], immune responses to pathogenic bacteria [ 11 ] or response to salinity stress [ 12 ].…”

Gamete quality in triploid Pacific oyster (Crassostrea gigas)

“…Two types of gametogenic pattern were identified, named α, for Pacific oysters unblocked during their gametogenesis and able to produce a significant number of gametes and β, for individuals presenting locking events during their gametogenesis and producing few or no gametes (Jouaux et al, 2010). At the molecular level, the gametogenesis of β individuals slowed down because of impaired sex differentiation caused by the presence of a third set of chromosomes (Dheilly et al, 2014). In northern quahogs, Mercenaria mercenaria, no triploids produced gametes, compared with 82% of diploid individuals (Eversole et al, 1996).…”

Evaluation of using veliger stage larvae for the preparation of metaphase spreads from the pacific abalone (Haliotis discus hannai)

“…35,No. 3, September 2020 equivalent segregation does not happen clearly during the meiosis of its germ cells, which finally causes infertility or sex maturation delay (Arai et al, 2001;Piferrer et al, 2009;Dheilly et al, 2014). It makes triploid abalone consume more energy in somatic growth instead of in sexual maturation, which eventually contributes to an increase of its value as a food resource (Allen and Downing, 1986).…”