Genome mapping of a LYST mutation in corn snakes indicates that vertebrate chromatophore vesicles are lysosome-related organelles

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.

Catabolism of lysosome-related organelles in color-changing spiders supports intracellular turnover of pigments

“…Overall, pigment organelles of crab spiders join the growing list of pigment LROs in distantly-related animals, including mammalian melanosomes (3), insect ommochromasomes and pterinosomes (43), fish pterinosomes (44), lepidopteran riboflavin and uric acid granules (45, 46), as well as snake melanosomes, pterinosomes and iridosomes (4). Our study therefore provides another piece of evidence that all pigment organelles, from invertebrates to vertebrates, share a common intracellular identity, as postulated 40 years ago by Bagnara and colleagues (2).…”

“…Bagnara and colleagues postulated in 1979 that all pigment organelles of vertebrates derive from a common primordial organelle (2). Since then, an increasing body of evidence has shown that pigment organelles, from mammal melanosomes to snake pterinosomes, belong to the lysosome-related organelle (LRO) family (3, 4). LROs intersect the endolysosomal system (5), which forms a complex and active network of membrane-bound compartments produced by endocytic and secretory pathways (6).…”

“…Melanosome formation is controlled by a range of genes involved in the endolysosomal system of mammals (3, 5). The finding of homologous genes controlling pterinosomes, iridisomes and ommochromasomes of snakes and insects, among others, has led to a general model of pigment organelle formation (3, 4, 7). However, coloration does not only involve pigmentation phases but also bleaching phases that lead to pigment removal; a process that is far less understood, even for melanosomes (8).…”

A nonsense mutation inTFECis the likely cause of the recessive piebald phenotype in ball pythons (Python regius)

“…However, our current knowledge of the genetics of vertebrate colouration comes primarily from studies on model species, particularly the mouse (e.g. Baxter et al 2004; Hoekstra 2006; San-Jose and Roulin 2017; but see Ullate-Agote et al 2020). This bias in the literature provides a limited view of the ways in which genetic variation can affect vertebrate colouration.…”

“…The extensive phenotypic variation in pigment and pattern found in captive-bred ball pythons can therefore help correct the bias (e.g. Ullate-Agote et al 2020) associated with mammalian models and melanin-based pigmentation in the scientific literature on vertebrate colouration.…”