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      The “IAG-Switch”—A Key Controlling Element in Decapod Crustacean Sex Differentiation

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          Abstract

          The androgenic gland (AG)–a unique crustacean endocrine organ that secretes factors such as the insulin-like androgenic gland (IAG) hormone—is a key player in crustacean sex differentiation processes. IAG expression induces masculinization, while the absence of the AG or a deficiency in IAG expression results in feminization. Therefore, by virtue of its universal role as a master regulator of crustacean sexual development, the IAG hormone may be regarded as the sexual “IAG-switch.” The switch functions within an endocrine axis governed by neuropeptides secreted from the eyestalks, and interacts downstream with specific insulin receptors at its target organs. In recent years, IAG hormones have been found—and sequenced—in dozens of decapod crustacean species, including crabs, prawns, crayfish and shrimps, bearing different types of reproductive strategies—from gonochorism, through hermaphroditism and intersexuality, to parthenogenesis. The IAG-switch has thus been the focus of efforts to manipulate sex developmental processes in crustaceans. Most sex manipulations were performed using AG ablation or knock-down of the IAG gene in males in order to sex reverse them into “neo-females,” or using AG implantation/injecting AG extracts or cells into females to produce “neo-males.” These manipulations have highlighted the striking crustacean sexual plasticity in different species and have permitted the manifestation of either maleness or femaleness without altering the genotype of the animals. Furthermore, these sex manipulations have not only facilitated fundamental studies of crustacean sexual mechanisms, but have also enabled the development of the first IAG-switch-based monosex population biotechnologies, primarily for aquaculture but also for pest control. Here, we review the crustacean IAG-switch, a unique crustacean endocrine mechanism, from the early discoveries of the AG and the IAG hormone to recent IAG-switch-based manipulations. Moreover, we discuss this unique early pancrustacean insulin-based sexual differentiation control mechanism in contrast to the extensively studied mechanisms in vertebrates, which are based on sex steroids.

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          DMY is a Y-specific DM-domain gene required for male development in the medaka fish.

          Although the sex-determining gene Sry has been identified in mammals, no comparable genes have been found in non-mammalian vertebrates. Here, we used recombinant breakpoint analysis to restrict the sex-determining region in medaka fish (Oryzias latipes) to a 530-kilobase (kb) stretch of the Y chromosome. Deletion analysis of the Y chromosome of a congenic XY female further shortened the region to 250 kb. Shotgun sequencing of this region predicted 27 genes. Three of these genes were expressed during sexual differentiation. However, only the DM-related PG17 was Y specific; we thus named it DMY. Two naturally occurring mutations establish DMY's critical role in male development. The first heritable mutant--a single insertion in exon 3 and the subsequent truncation of DMY--resulted in all XY female offspring. Similarly, the second XY mutant female showed reduced DMY expression with a high proportion of XY female offspring. During normal development, DMY is expressed only in somatic cells of XY gonads. These findings strongly suggest that the sex-specific DMY is required for testicular development and is a prime candidate for the medaka sex-determining gene.
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            Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig.

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              The avian Z-linked gene DMRT1 is required for male sex determination in the chicken.

              Sex in birds is chromosomally based, as in mammals, but the sex chromosomes are different and the mechanism of avian sex determination has been a long-standing mystery. In the chicken and all other birds, the homogametic sex is male (ZZ) and the heterogametic sex is female (ZW). Two hypotheses have been proposed for the mechanism of avian sex determination. The W (female) chromosome may carry a dominant-acting ovary determinant. Alternatively, the dosage of a Z-linked gene may mediate sex determination, two doses being required for male development (ZZ). A strong candidate avian sex-determinant under the dosage hypothesis is the conserved Z-linked gene, DMRT1 (doublesex and mab-3-related transcription factor 1). Here we used RNA interference (RNAi) to knock down DMRT1 in early chicken embryos. Reduction of DMRT1 protein expression in ovo leads to feminization of the embryonic gonads in genetically male (ZZ) embryos. Affected males show partial sex reversal, characterized by feminization of the gonads. The feminized left gonad shows female-like histology, disorganized testis cords and a decline in the testicular marker, SOX9. The ovarian marker, aromatase, is ectopically activated. The feminized right gonad shows a more variable loss of DMRT1 and ectopic aromatase activation, suggesting differential sensitivity to DMRT1 between left and right gonads. Germ cells also show a female pattern of distribution in the feminized male gonads. These results indicate that DMRT1 is required for testis determination in the chicken. Our data support the Z dosage hypothesis for avian sex determination.
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                Author and article information

                Contributors
                Journal
                Front Endocrinol (Lausanne)
                Front Endocrinol (Lausanne)
                Front. Endocrinol.
                Frontiers in Endocrinology
                Frontiers Media S.A.
                1664-2392
                10 September 2020
                2020
                : 11
                : 651
                Affiliations
                [1] 1Department of Life Sciences, Ben-Gurion University of the Negev , Beer-Sheva, Israel
                [2] 2The National Institute for Biotechnology in the Negev, Ben-Gurion University of the Negev , Beer-Sheva, Israel
                Author notes

                Edited by: Heinrich Dircksen, Stockholm University, Sweden

                Reviewed by: Pierre Greve, University of Poitiers, France; Juan Ignacio Fernandino, CONICET Institute of Biotechnological Research (IIB-INTECH), Argentina

                *Correspondence: Amir Sagi sagia@ 123456bgu.ac.il

                This article was submitted to Experimental Endocrinology, a section of the journal Frontiers in Endocrinology

                Article
                10.3389/fendo.2020.00651
                7511715
                d6989a60-f8b5-490d-8777-1eaa992a7c03
                Copyright © 2020 Levy and Sagi.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 29 May 2020
                : 11 August 2020
                Page count
                Figures: 3, Tables: 2, Equations: 0, References: 203, Pages: 15, Words: 12373
                Funding
                Funded by: Israel Science Foundation 10.13039/501100003977
                Categories
                Endocrinology
                Review

                Endocrinology & Diabetes
                androgenic gland,iag-switch,insulin-like androgenic gland hormone,monosex population,sex determination,sex differentiation,sexual plasticity

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