Multi-Tissue Transcriptome Analysis Identifies Key Sexual Development-Related Genes of the Ornate Spiny Lobster (Panulirus ornatus)

Abstract

Sexual development involves the successive and overlapping processes of sex determination, sexual differentiation, and ultimately sexual maturation, enabling animals to reproduce. This provides a mechanism for enriched genetic variation which enables populations to withstand ever-changing environments, selecting for adapted individuals and driving speciation. The molecular mechanisms of sexual development display a bewildering diversity, even in closely related taxa. Many sex determination mechanisms across animals include the key family of “doublesex- and male abnormal3-related transcription factors” (Dmrts). In a few exceptional species, a single Dmrt residing on a sex chromosome acts as the master sex regulator. In this study, we provide compelling evidence for this model of sex determination in the ornate spiny lobster Panulius ornatus, concurrent with recent reports in the eastern spiny lobster Sagmariasus verreauxi. Using a multi-tissue transcriptomic database established for P. ornatus, we screened for the key factors associated with sexual development (by homology search and using previous knowledge of these factors from related species), providing an in-depth understanding of sexual development in decapods. Further research has the potential to close significant gaps in our understanding of reproductive development in this ecologically and commercially significant order.

Signaling Pathways That Regulate the Crustacean Molting Gland

“…GPCRs are characterized by seven transmembrane domains, an external N-terminal domain, and a C-terminal cytosolic domain (25). These are divided among three large classes: rhodopsin-like (Class A), which represents the largest number of GPCRs; secretinlike (Class B); and metabotropic glutamate (Class C) (25)(26)(27)(28)(29)(30)(31)(32)(33)(34)(35)(36)(37)(38)(39)(40)(41)(42)(43)(44).…”

The Regulatory Mechanism of Sexual Development in Decapod Crustaceans

“…In ornate spiny lobster (Panulirus ornatus), Sxl and Tra-2 isoform-encoding transcripts showed broad tissue expression, with no clear bias between males and females, suggesting that Sxl-Tra-Dsx may be unique to Drosophilidae and not conserved among decapods. However, the male-specific iDMY was conserved between the eastern (Sagmariasus verreauxi) and ornate spiny lobsters (P. ornatus), indicating a conserved central function in sex determination (Ventura et al, 2020).…”

“…An insulin family-based signaling system has been proposed based on the structure similarity of IAG to the insulin/IGF family (Sharabi et al, 2016). Several peptide receptors including tyrosine kinase insulin receptor (TKIR), G-protein-coupled receptor (GPCR), insulin receptor (IR), and insulin-like growth factorbinding peptide (IGFBP) have been identified to be the receptor for IAG (Rosen et al, 2010;Aizen et al, 2016;Chandler et al, 2017;Jiang et al, 2020c;Ventura et al, 2020).…”

Sex Determination and Differentiation in Decapod and Cladoceran Crustaceans: An Overview of Endocrine Regulation

“…Unlike in insect species, the dsx function is known to be regulated via sex-biased expression (with the majority of cases in males) rather than alternative sex-specific splicing in non-insect arthropods such as the crustacea (details in following sections) and chelicerata (including the common house spider) [ 47 ]. Moreover, in addition to dsx genes, the invertebrate Y-chromosome-linked iDMY genes have recently been identified as a masculinization factor during embryogenesis in the Eastern spiny lobster Sagmariasus verreauxi [ 48 ] and in the ornate spiny lobster Panulirus ornatus [ 49 ]. High-throughput next generation sequencing techniques have successfully enabled the decoding of draft genomes in many Malacostracans ( Table 1 ).…”

“…Especially genome information of following species: the marbled crayfish Procambarus fallax f. virginalis [ 26 ], the Pacific white shrimp Litopenaeus vannamei [ 22 ], the giant freshwater prawn Macrobrachium rosenbergii [ 24 ], and the terrestrial isopod Armadillidium vulgare [ 29 ], will accelerate sex determination and differentiation studies, since they have been used in the studies of endocrinology and sex differentiation as experimental animals (details in following sections). Moreover, several transcriptome studies have revealed the existence of female- or male-biased genes in various decapods, shedding light on the understanding of molecular mechanisms underlying sex determination, sexual differentiation, and sexual maturation [ 48 , 49 , 50 , 51 , 52 , 53 ]. Improving the sequencing depth and algorithm for de novo assembly will help to identify the loci of sex-determining genes on sex chromosomes.…”