Triploid-induced complete sterility in the scallop Nodipecten subnodosus might be triggered by an early and sustained DNA damage response

Abstract

Triploid Nodipecten subnodosus scallops, unlike other mollusks, are completely sterile. In this study we focused on understanding the underlying molecular changes of triploid sterility using a transcriptomic approach. Total RNA from the gonad of diploid scallops in inactive and initial gametogenic stages and triploid scallops of the same cohort and ages were sequenced employing Illumina RNA-Seq. From 68,244 assembled and annotated transcripts, 1120 had terms associated with meiosis checkpoint or arrest, DNA damage response, or recombination. Differential gene expression analyses were conducted by contrasting initial vs. inactive stages of gametogenesis in each ploidy. In diploids, genes participating in homologous recombination during meiosis (msh5 and kdm8), spindle organization (nup62), centrosome formation (cenp-T), and sex differentiation (Ns-dmta2 and pum3), were up-regulated during initial gametogenesis. In triploids, a different set of genes were up-regulated during initial gametogenesis, and included genes involved in the DNA damage response and double strand break repair (rad51-C, xpc, myoVI), in the transition of metaphase/anaphase of mitosis (slp1 and nuf2), as well as genes that trigger both the intrinsic and extrinsic (caspase-3, icad, bmcc1) and extrinsic apoptosis pathways only (tnfr1, dab2ip). The results suggest significant DNA damage in triploids initial gametogenesis, possibly as a consequence of failing to repair double-strand breaks during DNA replication. This coincides with previous observations in which few triploid scallops showed gametic stages more advanced than oogonia or spermatogonia, and when present they were few.