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Abstract
Reptiles exhibit a spectacular diversity of skin colors and patterns brought about by the interactions among three chromatophore types: black melanophores with melanin-packed melanosomes, red and yellow xanthophores with pteridine- and/or carotenoid-containing vesicles, and iridophores filled with light-reflecting platelets generating structural colors. Whereas the melanosome, the only color-producing endosome in mammals and birds, has been documented as a lysosome-related organelle, the maturation paths of xanthosomes and iridosomes are unknown. Here, we first use 10x Genomics linked-reads and optical mapping to assemble and annotate a nearly chromosome-quality genome of the corn snake Pantherophis guttatus The assembly is 1.71 Gb long, with an N50 of 16.8 Mb and L50 of 24. Second, we perform mapping-by-sequencing analyses and identify a 3.9-Mb genomic interval where the lavender variant resides. The lavender color morph in corn snakes is characterized by gray, rather than red, blotches on a pink, instead of orange, background. Third, our sequencing analyses reveal a single nucleotide polymorphism introducing a premature stop codon in the lysosomal trafficking regulator gene (LYST) that shortens the corresponding protein by 603 amino acids and removes evolutionary-conserved domains. Fourth, we use light and transmission electron microscopy comparative analyses of wild type versus lavender corn snakes and show that the color-producing endosomes of all chromatophores are substantially affected in the LYST mutant. Our work provides evidence characterizing xanthosomes in xanthophores and iridosomes in iridophores as lysosome-related organelles.
Highlights
Classical model species represent remarkable resources to efficiently investigate the mechanisms producing a wealth of phenotypes and to develop tools and techniques that can be applied to emerging models
It is well documented that melanosomes are lysosomerelated organelles (LROs), which start as nonpigmented vacuolar early endosomes in stage I of their biogenesis, acquire internal striations in stage II, and progressively accumulate melanin in stage III, until they are fully melanized in stage IV [10]
By comparing the DNA content in corn snake and chicken nucleated erythrocytes using fluorescenceactivated cell sorting (FACS), we estimated the corn snake genome size to about 1.68 Gb (SI Appendix, Fig. S1), in accordance with the 1.74 to 1.79 Gb value obtained from our draft assembly on the basis of k-mer distribution [27]
Summary
Classical model species represent remarkable resources to efficiently investigate the mechanisms producing a wealth of phenotypes and to develop tools and techniques that can be applied to emerging models. The zebrafish (Danio rerio) is the main nonmammalian vertebrate model of skin coloration, and its study has provided important insights into the development and organization of chromatophore cells, as well as their interactions that bring about its pattern of yellow and black stripes [1, 2]. The numerous spontaneously occurring or mutagenesis-induced skin color and color-pattern phenotypes in zebrafish, along with its established position as a model species for developmental studies, facilitated the identification of the signaling pathways and cell interactions involved in vertebrate skin color and color patterning. Genetic studies on naturally occurring human and mouse color phenotypes presenting hypopigmentation and amelanism identified genes exhibiting key functions in neural crest cells development and survival No study focused on the origin and the characterization of xanthosomes and iridosomes (i.e., compartments containing reflecting guanine platelets)
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