Analysis of a novel gene, <i>Sdgc</i>, reveals sex chromosome-dependent differences of medaka germ cells prior to gonad formation

Nishimura, T.; Herpin, Amaury; Kimura, Tetsuaki; Hara, Ikuyo; Kawasaki, Toshihiro; Nakamura, Shuhei; Yamamoto, Yasuhiro; Saito, Taro; Yoshimura, Junichi; Morishita, Shinichi; Tsukahara, Tatsuya; Kobayashi, Satoru; Naruse, Kiyoshi; Shigenobu, Shuji; Sakai, Noriyoshi; Schartl, Manfred; Tanaka, Minoru

doi:10.1242/dev.106864

Cited by 15 publications

(15 citation statements)

References 38 publications

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“…We also used published data (46,47) to assign crossover events in male meiosis to terminal or nonterminal regions of all medaka chromosomes (SI Appendix, Table S3). These results, together with the evidence just cited from Xiphophorus, suggest that the guppy's strong heterochiasmy is a derived state.…”

Section: Resultsmentioning

confidence: 99%

Exaggerated heterochiasmy in a fish with sex-linked male coloration polymorphisms

Bergero

Gardner

Bader

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

109

215

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It is often stated that polymorphisms for mutations affecting fitness of males and females in opposite directions [sexually antagonistic (SA) polymorphisms] are the main selective force for the evolution of recombination suppression between sex chromosomes. However, empirical evidence to discriminate between different hypotheses is difficult to obtain. We report genetic mapping results in laboratory-raised families of the guppy (Poecilia reticulata), a sexually dimorphic fish with SA polymorphisms for male coloration genes, mostly on the sex chromosomes. Comparison of the genetic and physical maps shows that crossovers are distributed very differently in the two sexes (heterochiasmy); in male meiosis, they are restricted to the termini of all four chromosomes studied, including chromosome 12, which carries the sex-determining locus. Genome resequencing of male and female guppies from a population also indicates sex linkage of variants across almost the entire chromosome 12. More than 90% of the chromosome carrying the male-determining locus is therefore transmitted largely through the male lineage. A lack of heterochiasmy in a related fish species suggests that it originated recently in the lineage leading to the guppy. Our findings do not support the hypothesis that suppressed recombination evolved in response to the presence of SA polymorphisms. Instead, a low frequency of recombination on a chromosome that carries a male-determining locus and has not undergone genetic degeneration has probably facilitated the establishment of male-beneficial coloration polymorphisms.

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Section: Resultsmentioning

confidence: 99%

Exaggerated heterochiasmy in a fish with sex-linked male coloration polymorphisms

Bergero

Gardner

Bader

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

109

215

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“…Genes chosen were 2 ovarian markers foxl2 and cyp19a1 ( aromatase ) 28 32 and 5 testicular markers gsdf , dmy 12 13 , sdgc , dmrt1 and sox9b . sdgc is linked closely to dmy and expressed predominantly in spermatogonia but weakly in early oocytes 33 . dmrt1 and sox9b are autosomal male markers, as dmrt1 is expressed in the Sertoli cell lineage and essential for the maintenance of testis differentiation 17 ; while sox9b is expressed in both sexes during early gonadal sex differentiation 34 but maintained mainly in the XY gonads later during testicular tubules development 35 .…”

Section: Resultsmentioning

confidence: 99%

Autosomal gsdf acts as a male sex initiator in the fish medaka

Zhang¹,

Guan²,

Li³

et al. 2016

Sci Rep

Self Cite

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Sex is pivotal for reproduction, healthcare and evolution. In the fish medaka, the Y-chromosomal dmy (also dmrt1bY) serves the sex determiner, which activates dmrt1 for male sex maintenance. However, how dmy makes the male decision via initiating testicular differentiation has remained unknown. Here we report that autosomal gsdf serves a male sex initiator. Gene addition and deletion revealed that gsdf was necessary and sufficient for maleness via initiating testicular differentiation. We show that gsdf transcription is activated directly by dmy. These results establish the autosomal gsdf as the first male sex initiator. We propose that dmy determines maleness through activating gsdf and dmrt1 without its own participation in developmental processes of sex initiation and maintenance. gsdf may easily become a sex determiner or other autosomal genes can be recruited as new sex determiners to initiate gsdf expression. Our findings offer new insights into molecular mechanisms underlying sex development and evolution of sex-controlling genes in vertebrates.

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“…Though none are considered as a standard, the most cited definition is from Gerstein et al: “a union of genomic sequences encoding a coherent set of potentially overlapping functional products.” Current definitions, such as the above, have replaced the original view of genes as discrete inherited effects with discrete physical characters. In the new context, “novel gene” is used most often for communication of the content of a paper, namely that the authors are describing a gene as a physical entity that has been newly identified or when a new function was discovered for a previously known gene (Steeg et al 1988 ; MacDonald et al 1993 ; Fleury et al 1997 ; Nishimura et al 2014 ; Agaram et al 2015 ; Mangino et al 2015 ). Articles that identify a specific “novel gene” typically do not focus on the mechanisms behind the emergence of genes or comment on theoretical concerns about their origins.…”

Section: Novelty Usages Outside Of Evodevomentioning

confidence: 99%

Phenotypic Novelty in EvoDevo: The Distinction Between Continuous and Discontinuous Variation and Its Importance in Evolutionary Theory

Peterson

Müller

2016

Evol Biol

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The introduction of novel phenotypic structures is one of the most significant aspects of organismal evolution. Yet the concept of evolutionary novelty is used with drastically different connotations in various fields of research, and debate exists about whether novelties represent features that are distinct from standard forms of phenotypic variation. This article contrasts four separate uses for novelty in genetics, population genetics, morphology, and behavioral science, before establishing how novelties are used in evolutionary developmental biology (EvoDevo). In particular, it is detailed how an EvoDevo-specific research approach to novelty produces insight distinct from other fields, gives the concept explanatory power with predictive capacities, and brings new consequences to evolutionary theory. This includes the outlining of research strategies that draw attention to productive areas of inquiry, such as threshold dynamics in development. It is argued that an EvoDevo-based approach to novelty is inherently mechanistic, treats the phenotype as an agent with generative potential, and prompts a distinction between continuous and discontinuous variation in evolutionary theory.

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Analysis of a novel gene, Sdgc, reveals sex chromosome-dependent differences of medaka germ cells prior to gonad formation

Cited by 15 publications

References 38 publications

Exaggerated heterochiasmy in a fish with sex-linked male coloration polymorphisms

Exaggerated heterochiasmy in a fish with sex-linked male coloration polymorphisms

Autosomal gsdf acts as a male sex initiator in the fish medaka

Phenotypic Novelty in EvoDevo: The Distinction Between Continuous and Discontinuous Variation and Its Importance in Evolutionary Theory

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