Pleiotropic functions of chordin gene causing drastic morphological changes in ornamental goldfish

Abstract

Breeders and fanciers have established many peculiar morphological phenotypes in ornamental goldfish. Among them, the twin-tail and dorsal-finless phenotypes have particularly intrigued early and recent researchers, as equivalent morphologies are extremely rare in nature. These two mutated phenotypes appeared almost simultaneously within a short time frame and were fixed in several strains. However, little is known about how these two different mutations could have co-occurred during such a short time period. Here, we demonstrate that the chordin gene, a key factor in dorsal–ventral patterning, is responsible not only for the twin-tail phenotype but also for the dorsal-finless phenotype. Our F2 backcrossing and functional analyses revealed that the penetrance/expressivity of the dorsal-finless phenotype can be suppressed by the wild-type allele of chdS. Based on these findings, we propose that chdSwt may have masked the expression of the dorsal-finless phenotype, acting as a capacitor buffering gene to allow accumulation of genetic mutations. Once this gene lost its original function in the twin-tail goldfish lineages, the dorsal-finless phenotype could be highly expressed. Thus, this study experimentally demonstrates that the rapid genetic fixation of morphological mutations during a short domestication time period may be related to the robustness of embryonic developmental mechanisms.

On theindependent irritabilityof goldfish eggs and embryos – a living communication on the rhythmic yolk contractions in goldfish

“…Strikingly, altered DV patterning is implicated in the variation of median fin morphotypes in goldfish, such as twin-tail (Abe et al, 2014) and dorsal-finless (Chen et al, 2022). We documented here that embryos of Oranda , a twin-tail goldfish strain, exhibit faster yolk contractions than wild-type goldfish embryos, correlating faster and/or stronger contractions to more ventralized phenotypes in alignment to our current framework.…”

“…Strikingly, altered DV patterning is implicated in the variation of median fin morphotypes in goldfish, such as twintail (Abe et al, 2014) and dorsal-finless (Chen et al, 2022).…”

“…chdS ), which results in a non-functional truncated ChdS protein (Abe et al, 2014). Loss of function of said chordin gene, which naturally inhibits ventralization of the body (Piccolo et al, 1996; Sasai et al, 1994), is sufficient to cause caudal fin bifurcation in wild-type goldfish (Abe et al, 2014; Lee et al, 2023), and this mutation has been also recently implicated in loss of dorsal fin in dorsal finless goldfish strains (Chen et al, 2022). The spatiotemporal dynamics of the contractile gold-fish yolk remains understudied in goldfish development and evolution, in particular, and in cell-developmental biology, in general.…”

Evolutionary Insights into Muscle Fiber Distribution in the Twin Tails of Ornamental Goldfish

“…It is known that the bifurcated caudal musculoskeletal system in the twin-tail goldfish stems from the highly modified dorsal-ventral patterning deriving from the homozygous locus of a stop codon mutation allele in the duplicated chordin gene, referred to as the chdS E127X allele (or chdA E127X in the previous report) (Abe et al, 2014; Kon et al, 2020). This mutation alters the gene’s original function, resulting in ventralized early embryos, the formation of bifurcated caudal fin folds at the embryonic stage, and ultimately, the emergence and stable fixation of various ornamental twin-tail goldfish strains (Abe et al, 2014; Chen et al, 2022).…”