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Cited by 58melanin and skin pigmentationDevelopmental Biology and Gene RegulationZebrafish Biomedical Research Applications

Evolution of Endothelin signaling and diversification of adult pigment pattern in Danio fishes

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Spiewak, Jessica E., Bain, Emily J., Liu, Jin, Kou, Kellie, Sturiale, Samantha L., Patterson, Larissa B., Diba, Parham, Eisen, Judith S. +3 more·2018·PLOS Genetics
DOI 10.1371/journal.pgen.1007538PMC PMC6161917

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Abstract

Abstract Fishes of the genus Danio exhibit diverse pigment patterns that serve as useful models for understanding the genes and cell behaviors underlying the evolution of adult form. Among these species, zebrafish D. rerio exhibit several dark stripes of melanophores with sparse iridophores that alternate with light interstripes of dense iridophores and xanthophores. By contrast, the closely related species D. nigrofasciatus has an attenuated pattern with fewer melanophores, stripes and interstripes. Here we demonstrate species differences in iridophore development that presage the fully formed patterns. Using genetic and transgenic approaches we identify the secreted peptide Endothelin-3 (Edn3)—a known melanogenic factor of tetrapods—as contributing to reduced iridophore proliferation and fewer stripes and interstripes in D. nigrofasciatus . We further show the locus encoding this factor is expressed at lower levels in D. nigrofasciatus owing to cis -regulatory differences between species. Finally, we show that functions of two paralogous loci encoding Edn3 have been partitioned between skin and non-skin iridophores. Our findings reveal genetic and cellular mechanisms contributing to pattern differences between these species and suggest a model for evolutionary changes in Edn3 requirements across vertebrates. Author Summary Neural crest derived pigment cells generate the spectacular variation in skin pigment patterns among vertebrates. Mammals and birds have just a single skin pigment cell, the melanocyte, whereas ectothermic vertebrates have several pigment cells including melanophores, iridophores and xanthophores, that together organize into a diverse array of patterns. In the teleost zebrafish, Danio rerio , an adult pattern of stripes depends on interactions between pigment cell classes and between pigment cells and their tissue environment. The close relative, D. nigrofasciatus has fewer stripes and prior analyses suggested a difference between these species that lies extrinsic to the pigment cells themselves. A candidate for mediating this difference is Endothelin-3 (Edn3), essential for melanocyte development in warm-blooded animals, and required by all three classes of pigment cells in an amphibian. We show that Edn3 specifically promotes iridophore development in Danio , and that differences in Edn3 expression contribute to differences in iridophore complements, and striping, between D. rerio and D. nigrofasciatus . Our study reveals a novel function for Edn3 and provides new insights into how changes in gene expression yield morphogenetic outcomes to effect diversification of adult form.

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  • An evolutionary truncation in iridophore development leads to an attenuated stripe pattern in the zebrafish relative D. nigrofasciatus.

    “Likewise, an evolutionary truncation in iridophore development leads to an attenuated stripe pattern in the zebrafish relative D. nigrofasciatus18.”

    From In situ differentiation of iridophore crystallotypes underlies zebrafish stripe patterning (2020) · cites this paper as [18]

    The Results report curtailed iridophore expansion and fewer reiterated stripe elements in D. nigrofasciatus than in D. rerio. The Discussion proposes that early cessation of iridophore expansion led to the attenuated pattern, but frames that causal explanation as a suggestion; the citing sentence states it as fact. No page number is available in our copy. (LLM, conf=0.84)

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  • The phenotype of edn3b−/− mutant zebrafish was consistent with previous findings.

    “The phenotype of edn3b−/− mutants was consistent with previous findings (Spiewak et al., 2018).”

    From Chromosome-level genome assembly of the glass catfish (<i>Kryptopterus vitreolus</i>) reveals molecular clues to its transparent phenotype (2024) · cites this paper as Spiewak et al., 2018

  • Proliferation of loose iridophores within stripes was greater than that of dense iridophores within interstripes.

    “We found that proliferation of loose iridophores within stripes was greater than dense iridophores within interstripes, as noted previously18 (Supplementary Fig. 2a).”

    From In situ differentiation of iridophore crystallotypes underlies zebrafish stripe patterning (2020) · cites this paper as [18]

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Cited by

Sorted by citations

Authors
Spiewak, J. E., Bain, E. J., Liu, J., Kou, K., Sturiale, S. L., Patterson, L. B., Diba, P., Eisen, J. S., Braasch, I., Ganz, J., & Parichy, D. M.
Affiliations
  • University of Washington (US)
  • University of Virginia (US)
  • University of Oregon (US)
  • Michigan State University (US)
Corresponding author
  • Spiewak, Jessica E.
  • Bain, Emily J.
  • Liu, Jin
  • Kou, Kellie
  • Sturiale, Samantha L.
  • Patterson, Larissa B.
  • Diba, Parham
  • Eisen, Judith S.
  • Braasch, Ingo
  • Ganz, Julia
  • Parichy, David M.
ORCID
Venue
PLOS Genetics
Publisher
Public Library of Science (PLoS)
Published
2018-09-18
Volume
14
Issue
9
Pages
e1007538
ISSN
  • 1553-7390 (ISSN-L)
  • 1553-7404
DOI
10.1371/journal.pgen.1007538
PMC
PMC6161917
OpenAlex
W2950266515
Cited by
58
References
2
Citations by year
2026: 3 · 2025: 4 · 2024: 4 · 2023: 11 · 2022: 3 · 2021: 14 · 2020: 6 · 2019: 12 · 2018: 1
FWCI
4.52
Type
journal article
Language
en
Update notices
new_version (2018-09-28)
Open access
Licence
Locations
  • PLoS Genetics (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
Funders
  • National Institute of General Medical Sciences (US) (R35 GM122471)
  • Eunice Kennedy Shriver National Institute of Child Health and Human Development (R25 HD070817, P01 HD22486)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › melanin and skin pigmentation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Zebrafish Biomedical Research Applications
Keywords
endothelin-3, iridophores, melanophores, xanthophores, zebrafish, cis-regulatory variation, paralogs, melanogenesis, body coloration
MeSH terms
Animals, Chromatophores, Embryo, Nonmammalian, Phenotype, Pigmentation, Skin, Species Specificity, Zebrafish, Signal Transduction, Gene Expression Regulation, Developmental, Evolution, Molecular, Endothelin-3, Models, Animal, Zebrafish Proteins, Animals, Genetically Modified, Cell Proliferation

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