Transcriptomic profiling of gametogenesis in triploid Pacific Oysters Crassostrea gigas: towards an understanding of partial sterility associated with triploidy.

Nolwenn M Dheilly,Christophe Lelong,Pierre Boudry,Aude Jouaux,Pascal Favrel,Wolfgang Arthofer

doi:10.1371/journal.pone.0112094

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.

Highlights

Triploidy can occur in many animal species but is often lethal
Principal components 2, 3 and 4 discriminated individuals according to their gonad developmental stage, ploidy (3n versus 2n; 0.94%) and sex respectively
We were interested in investigating the unusual ability of 3na individuals to perform advanced gametogenesis by comparing them to 3nb individuals, which show less developed gonadic tubules [20], and to 2n individuals displaying normal gonadal development [26]

Summary

Introduction

Triploidy can occur in many animal species but is often lethal. Among invertebrates, amphibians and fishes, triploids are viable often sterile or infertile. Most triploids of the Pacific oyster Crassostrea gigas are almost sterile (named ‘‘3nb’’) yet a low but significant proportion show an advanced gametogenesis (named ‘‘3na’’) These oysters constitute an interesting model to study the effect of triploidy on germ cell development. Amphibians and fishes, triploids are often difficult to distinguish from diploids, in some species, they have a larger body size and faster growth than diploids. This is often at the expense of gonadal development [4,5,6,7] since in most species, triploids are either sterile or infertile. Differences in growth and reproductive capacity between diploid and triploids have often been used in aquaculture to increase production or to reduce genetic impact of escapes from cultured stock [8,9,10]

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