Oviducal gland transcriptomics of Octopus maya through physiological stages and the negative effects of temperature on fertilization

PeerJ. 2022 Mar 30:10:e12895. doi: 10.7717/peerj.12895. eCollection 2022.

Abstract

Background: Elevated temperatures reduce fertilization and egg-laying rates in the octopus species. However, the molecular mechanisms that control the onset of fertilization and egg-laying in the octopus' oviducal gland are still unclear; and the effect of temperature on the expression of key reproductive genes is unknown. This study aims to better understand the molecular bases of octopus fertilization and egg-laying, and how they are affected by elevated temperatures.

Method: RNA-seq of oviducal glands was performed for samples before, during, and after fertilization and their transcriptomic profiles were compared. Also, at the fertilization stage, the optimal and thermal-stress conditions were contrasted. Expression levels of key reproductive genes were validated via RT-qPCR.

Results: In mated females before egg-laying, genes required for the synthesis of spermine, spermidine, which may prevent premature fertilization, and the myomodulin neuropeptide were upregulated. Among the genes with higher expression at the fertilization stage, we found those encoding the receptors of serotonin, dopamine, and progesterone; genes involved in the assembly and motility of the sperm flagellum; genes that participate in the interaction between male and female gametes; and genes associated with the synthesis of eggshell mucoproteins. At temperatures above the optimal range for reproduction, mated females reduced the fertilization rate. This response coincided with the upregulation of myomodulin and APGW-amide neuropeptides. Also, genes associated with fertilization like LGALS3, VWC2, and Pcsk1 were downregulated at elevated temperatures. Similarly, in senescent females, genes involved in fertilization were downregulated but those involved in the metabolism of steroid hormones like SRD5A1 were highly expressed.

Keywords: Egg-laying; Fertilization; Gamete recognition proteins; RNA-Seq; Thermal stress.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Female
  • Fertilization / genetics
  • Humans
  • Male
  • Octopodiformes* / genetics
  • Semen
  • Temperature
  • Transcriptome* / genetics

Grants and funding

This research was funded by the project SEP-CONACYT-CB-2014-01/241690, and CICESE internal project 682-136 awarded to Clara E. Galindo-Sanchez, also by projects DGAPA-UNAM, PAPIIT IN203022, and CONACYT 61503 awarded to Carlos Rosas. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.