The gene encoding the insulin-like androgenic gland hormone in an all-female parthenogenetic crayfish

Abstract

Male sexual differentiation in crustaceans is controlled by the androgenic gland (AG), a unique male endocrine organ that, in decapods, is located at the base of the 5th pereiopod. In these animals, the insulin-like androgenic gland hormone (IAG) is the major factor secreted from the AG to induce masculinization and maintain male characteristics. It has, however, recently been proposed that this hormone also plays a role in growth and ovarian development in females. In this study, we tested such a possibility by searching for the IAG gene in the marbled crayfish, a parthenogenetic animal that reproduces asexually to form an all-female genetic clone. Based on the phylogenetic relationship between the marbled crayfish and Procambarus fallax, a gonochoristic species of the same North American Cambaridae family, we searched for the IAG gene in the marbled crayfish and then fully sequenced it. The open reading frame of the gene was found to be completely identical in the two species, and their introns shared over 94% identity. It was also found that, in addition to its expression at the base of the 5th pereiopod and in the testes of male P. fallax crayfish, IAG was expressed in the muscle tissue of P. fallax males and females and even of the parthenogenetic marbled crayfish. These findings provide new insight into possible functions of IAG, in addition to its role as a masculinization-inducing factor, and also constitute the basis for a discussion of the evolutionary relationship between the above two species.

Gonadulins, the fourth type of Insulin-related peptides in Decapods

“…Similar findings have been reported previously (e.g. Chung, 2014;Huang et al, 2014;Levy et al, 2017;Shi et al, 2019).…”

Identification of an insulin‐like androgenic gland hormone transcript highly expressed in male precociousness of the Chinese mitten crab Eriocheir sinensis

“…The deduced sequence of the EsIAG pre‐peptide contains a signal peptide on N terminus (19 aa), A chain (44 aa), B chain (31 aa), and C peptide (57 aa). The A and B chains were separated by the putative cleavage sites RRTR and RFRR in C peptide (Levy, Rosen, Simons, Savaya Alkalay, & Sagi, ). In addition, N‐linked glycosylated site (NCT) (Aizen et al, ; Ventura, Fitzgibbon, Battaglene, Sagi, & Elizur, ) in the A chain was also found in the deduced EsIAG.…”

“…To date, full‐length homologous IAG cDNA have been cloned in many commercially important decapod crustaceans, including crabs (Chung, Manor, & Sagi, ; Huang et al, ; Lawrence et al, ), crayfish (Levy et al, ; Manor et al, ; Rosen et al, ), prawns (Banzai et al, ; Ma et al, ; Phoungpetchara et al, ), and other shrimps (Li, Li, Sun, & Xiang, ; Vazquez‐Islas, Garza‐Torres, Guerrero‐Tortolero, & Campos‐Ramos, ; Zhang, Sun, & Liu, ). However, multiple sequence alignment showed that these IAG shared low similarities among different genus.…”

“…Similar to previous reports, the E. sinensis EsIAG shared very low identities with other reported IAGs (15%–46%), suggesting that gene sequences of IAGs exhibit considerable variation in the course of evolution. However, like other proteins encoded by IAGs , EsIAG contains the conserved characteristics of structures, including the signal peptide, A, B, C peptides, NCT, and six conserved Cys residues, which are considered as the functional keystone of the insulin‐like peptides (Levy et al, ; Ventura & Sagi, ).…”

“…In many crustacean species, the IAG gene was found in both the male and female genomes, but it was expressed exclusively in the AG of male individuals (Levy et al, ). In accordance with this, the EsIAG gene was first identified in the genome of female crabs, while RT‐PCR and in situ hybridization analysis showed that EsIAG was only expressed in AG.…”