Citation: Kabangu, M.; Cecil, R.;
Strohl, L., II; Timoshevskaya, N.;
Smith, J.J.; Voss, S.R. Leukocyte
Tyrosine Kinase (Ltk) Is the Mendelian
Determinant of the Axolotl Melanoid
Color Variant. Genes 2023, 14, 904.
https://doi.org/10.3390/
genes14040904
Academic Editor: Alexander
V. Ereskovsky
Received: 23 February 2023
Revised: 2 April 2023
Accepted: 10 April 2023
Published: 13 April 2023
Copyright: © 2023 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
genes
G C A T
T A C G
G C A T
Article
Leukocyte Tyrosine Kinase (Ltk) Is the Mendelian Determinant
of the Axolotl Melanoid Color Variant
Mirindi Kabangu
1,2
, Raissa Cecil
1
, Lloyd Strohl II
3
, Nataliya Timoshevskaya
4
, Jeramiah J. Smith
4
and Stephen R. Voss
1,
*
1
Department of Neuroscience, Spinal Cord and Brain Injury Research Center, and Ambystoma Genetic
Stock Center, University of Kentucky, Lexington, KY 40536, USA
2
Indiana University School of Medicine, Indianapolis, IN 46202, USA
3
Independent Researcher, Vevay, IN 47043, USA
4
Department of Biology, University of Kentucky, Lexington, KY 40506, USA
* Correspondence: srvoss@uky.edu
Abstract: The great diversity of color patterns observed among amphibians is largely explained by the
differentiation of relatively few pigment cell types during development. Mexican axolotls present a
variety of color phenotypes that span the continuum from leucistic to highly melanistic. The melanoid
axolotl is a Mendelian variant characterized by large numbers of melanophores, proportionally
fewer xanthophores, and no iridophores. Early studies of melanoid were influential in developing
the single-origin hypothesis of pigment cell development, wherein it has been proposed that all
three pigment cell types derive from a common progenitor cell, with pigment metabolites playing
potential roles in directing the development of organelles that define different pigment cell types.
Specifically, these studies identified xanthine dehydrogenase (XDH) activity as a mechanism for the
permissive differentiation of melanophores at the expense of xanthophores and iridophores. We used
bulked segregant RNA-Seq to screen the axolotl genome for melanoid candidate genes and identify
the associated locus. Dissimilar frequencies of single-nucleotide polymorphisms were identified
between pooled RNA samples of wild-type and melanoid siblings for a region on chromosome 14q.
This region contains gephyrin (Gphn), an enzyme that catalyzes the synthesis of the molybdenum
cofactor that is required for XDH activity, and leukocyte tyrosine kinase (Ltk), a cell surface signaling
receptor that is required for iridophore differentiation in zebrafish. Wild-type Ltk crispants present
similar pigment phenotypes to melanoid, strongly implicating Ltk as the melanoid locus. In concert
with recent findings in zebrafish, our results support the idea of direct fate specification of pigment
cells and, more generally, the single-origin hypothesis of pigment cell development.
Keywords: genetic linkage analysis; axolotl; mutant; pigmentation; neural crest
1. Introduction
The Mexican axolotl has a deep and colorful history. Thirty-three axolotls were
famously imported from Mexico to Europe in 1863 to establish a population at the Jardin
des Plantes in Paris [1]. Descendants from this population were distributed throughout
the world to found laboratory populations that remain in existence today. All of the
original Paris axolotls, except for one, presented approximately olive-green wild-type
axolotl coloration, owing to the intermingling of black melanophores, yellow xanthophores,
and more sparsely distributed iridescent iridophores (Figure 1). The lone non-wild-type
axolotl in the original Paris collection presented a leucistic phenotype (white) characterized
by few to no melanophores. White axolotls proved to be valuable in early embryological
studies because they provided a non-pigmented background to monitor the behaviors of
grafted, melanin-containing cells from wild-type axolotl donors. Today, white axolotls are
preferred over more darkly pigmented wild-type axolotls for visualization of fluorescent
probes and making transgenics with fluorescent reporter constructs. While the white
Genes 2023, 14, 904. https://doi.org/10.3390/genes14040904 https://www.mdpi.com/journal/genes