Mechanisms of pigment pattern formation in the quail embryo

Development ◽  
1990 ◽  
Vol 109 (1) ◽  
pp. 81-89 ◽  
Author(s):  
M.K. Richardson ◽  
A. Hornbruch ◽  
L. Wolpert

One hypothesis to account for pigment patterning in birds is that neural crest cells migrate into all feather papillae. Local cues then act upon the differentiation of crest cells into melanocytes. This hypothesis is derived from a study of the quail-chick chimaera (Richardson et al., Development 107, 805–818, 1989). Another idea, derived from work on larval fish and amphibia, is that pigment patterns arise from the differential migration of crest cells. We want to know which of these mechanisms can best account for pigment pattern formation in the embryonic plumage of the quail wing. Most of the feather papillae on the dorsal surface of the wing are pigmented, while many on the ventral surface are white. When ectoderm from unpigmented feather papillae is grown in culture, it gives rise to melanocytes. This indicates that neural crest cells are present in white feathers but that they fail to differentiate. If the wing tip is inverted experimentally then the pigment pattern is inverted also. This is difficult to explain in terms of a model based on migratory pathways, unless one assumes that the pathways became re-routed. When an extra polarizing region is grafted to the anterior margin of the wing bud, a duplication develops in: (1) the pattern of skeletal elements; (2) the pattern of feather papillae; (3) the feather pigment pattern. The pigment pattern was not a precise mirror image although some groups of papillae showed a high degree of symmetry in their pigmentation. Both the tip inversions and the duplications produce discontinuities in the feather and pigment patterns. No evidence of intercalation was found in these cases. We conclude that pigment patterning in birds is determined by local cues acting on melanocyte differentiation, rather than by the differential migration of crest cells. Positional values along the anteroposterior axis of the pigment pattern are determined by a gradient of positional information. Thus the pigment patterns, feather patterns and cartilage patterns of the wing may all be specified by a similar mechanism.

Development ◽  
1989 ◽  
Vol 107 (4) ◽  
pp. 805-818 ◽  
Author(s):  
M.K. Richardson ◽  
A. Hornbruch ◽  
L. Wolpert

The pattern of pigmentation in birds is dependent on the migration and differentiation of a population of neural crest cells that develop into melanoblasts. On the basis of previous grafting experiments Rawles (1948) concluded that the pigment pattern of the chimaera is determined by the genotype of the donor melanocyte. This led Wolpert (1981) to suggest that melanoblasts from one bird can read the positional value of the ectoderm in the feather papillae of another bird. An alternative view is that an isomorphic prepattern in the feathers determines the pigment pattern. We have examined these ideas in relation to the local pigment patterns of the embryonic quail wing, distal to the elbow, where several rows of feather papillae are consistently unpigmented. Melanin pigment is first seen at stage 35. By stage 39 a characteristic pigment pattern has been established. Most of the dorsal feather papillae are heavily pigmented, whereas many ventral papillae are unpigmented. Of the ventral papillae three rows (E2, E3 and H2) are always unpigmented, and it is these three rows that form the basis of the quail local pattern. The DOPA reaction indicates that no melanoblasts are present in these white feathers, although they are present in all the feathers of the White Leghorn wing. When quail neural crest cells are grafted to the chick, either isotopically or to the wing bud, all or nearly all rows of ventral papillae become pigmented by stage 39. The only evidence of donor influences in the pattern is that, in some grafts, rows E2-3 have a high proportion of unpigmented papillae, and wings from earlier stages resemble the quail. When unpigmented papillae are present, histology shows that they contain undifferentiated crest cells. When introduced into a quail wing bud, chick crest cells enter all the feather papillae of the wing, including those in rows E2-3 and H2. We suggest that neither the positional information nor the prepattern theory alone can account for all of our findings. Contrary to previous claims, local cues may be important in determining crest-cell differentiation. We have established that crest cells migrate into all feather papillae of the quail-chick chimaera, including those that will remain unpigmented. We show that neither differential migration nor differential proliferation is involved in pattern formation in the quail-chick chimaera.


2019 ◽  
Vol 53 (1) ◽  
pp. 505-530 ◽  
Author(s):  
Larissa B. Patterson ◽  
David M. Parichy

Vertebrate pigment patterns are diverse and fascinating adult traits that allow animals to recognize conspecifics, attract mates, and avoid predators. Pigment patterns in fish are among the most amenable traits for studying the cellular basis of adult form, as the cells that produce diverse patterns are readily visible in the skin during development. The genetic basis of pigment pattern development has been most studied in the zebrafish, Danio rerio. Zebrafish adults have alternating dark and light horizontal stripes, resulting from the precise arrangement of three main classes of pigment cells: black melanophores, yellow xanthophores, and iridescent iridophores. The coordination of adult pigment cell lineage specification and differentiation with specific cellular interactions and morphogenetic behaviors is necessary for stripe development. Besides providing a nice example of pattern formation responsible for an adult trait of zebrafish, stripe-forming mechanisms also provide a conceptual framework for posing testable hypotheses about pattern diversification more broadly. Here, we summarize what is known about lineages and molecular interactions required for pattern formation in zebrafish, we review some of what is known about pattern diversification in Danio, and we speculate on how patterns in more distant teleosts may have evolved to produce a stunningly diverse array of patterns in nature.


Development ◽  
1976 ◽  
Vol 35 (3) ◽  
pp. 463-484
Author(s):  
Gillian J. MacMillan

The melanophores of larval Xenopus laevis are disparately distributed on the hypomere in that the upper region (UHT) is densely pigmented, the median region (MHT) is moderately pigmented, and the lower region (LHT) is unpigmented. The roles of the melanoblasts and their tissue environment in determining the melanophore pattern was investigated by heterotopic transplantation of hypomeric tissues, culture of neural crest explants in vesicles derived from hypomeric tissues and radioactive marking of neural crest cells. Somite-situated grafts of UHT, MHT and LHT were found to possess melanophore densities similar to those exhibited by such hypomeric tissues when in their normal situation. The number and distribution of trunk melanophores in ‘crestless’ second host larvae bearing grafts of UHT, MHT and LHT transferred from the somites of primary host embryos indicated that (a) many melanoblasts entered all transplants during neural crest migration in the primary host: subsequently, a small number of melanoblasts were lost from transplants of UHT, a greater number from transplants of MHT and almost all from transplants of LHT; (b) almost all melanoblasts migrated out from transplants of MHT and LHT and entered the tissues of the ‘crestless’ host, whereas a considerable number of melanoblasts remained in the transplant when it was formed from UHT. Grafts of UHT placed mid-ventrally in the hypomere failed to exhibit melanophores. Vesicles of (a) UHT + MHT and (b) LHT containing neural crest tissue possessed similar numbers of melanophores. Vesicles of LHT differed from those of UHT + MHT in that melanophores were densely aggregated in the implanted neural tissues. Following radioactive marking of neural crest cells labelled nuclei were found on the dorsal ridges of the somites, the surfaces of the neural tube and notochord and in the mesoderm of the upper hypomere and the fin, but were absent from the lateral surfaces of the somites. These results showed that the melanophore pattern in larval Xenopus depended upon melanoblast-tissue interactions, which influenced the migration, rather than the differentiation, proliferation or destruction, of melanoblasts and suggested that tissue selection by migrating melanoblasts enabled these cells to distribute themselves in embryonic tissues in accordance with a hierarchy of melanoblast-tissue affinities. Melanoblast-tissue affinities appeared to be related to the adhesiveness of mesodermal cells: melanoblast extensibility appeared to facilitate exploration of the surrounding tissues. The formation of pigment pattern in larval Xenopus appeared to depend upon the interaction between the melanoblast population pressure and melanoblast-tissue affinities. The present results and those of other workers on amphibian pigmentation were used toconstruct a model capable of accounting for species-specific differences in larval amphibian pigment patterns, in terms of interactions between species-specific differences in melanoblast-tissue affinities and melanoblast population pressure.


2018 ◽  
Author(s):  
Karen Camargo-Sosa ◽  
Sarah Colanesi ◽  
Jeanette Müller ◽  
Stefan Schulte-Merker ◽  
Derek Stemple ◽  
...  

AbstractSkin pigment patterns are important, being under strong selection for multiple roles including camouflage and UV protection. Pigment cells underlying these patterns form from adult pigment stem cells (APSCs). In zebrafish, APSCs derive from embryonic neural crest cells, but sit dormant until activated to produce pigment cells during metamorphosis. The APSCs are set-aside in an ErbB signaling dependent manner, but the mechanism maintaining quiescence until metamorphosis remains unknown. Mutants for a pigment pattern gene, parade, exhibit ectopic pigment cells localised to the ventral trunk. We show that parade encodes Endothelin receptor Aa, expressed in the blood vessels. Using chemical genetics, coupled with analysis of cell fate studies, we show that the ectopic pigment cells derive from APSCs. We propose that a novel population of APSCs exists in association with medial blood vessels, and that their quiescence is dependent upon Endothelin-dependent factors expressed by the blood vessels.Lay AbstractPigment patterns are crucial for the many aspects of animal biology, for example, providing camouflage, enabling mate selection and protecting against UV irradiation. These patterns are generated by one or more pigment cell-types, localised in the skin, but derived from specialised stem cells (adult pigment stem cells, APSCs). In mammals, such as humans, but also in birds and fish, these APSCs derive from a transient population of multipotent progenitor cells, the neural crest. Formation of the adult pigment pattern is perhaps best studied in the zebrafish, where the adult pigment pattern is formed during a metamorphosis beginning around 21 days of development. The APSCs are set-aside in the embryo around 1 day of development, but then remain inactive until that metamorphosis, when they become activated to produce the adult pigment cells. We know something of how the cells are set-aside, but what signals maintain them in an inactive state is a mystery. Here we study a zebrafish mutant, called parade, which shows ectopic pigment cells in the embryo. We clone the parade gene, identifying it as ednraa encoding a component of a cell-cell communication process, which is expressed in blood vessels. By characterising the changes in the neural crest and in the pigment cells formed, and by combining this with an innovative assay identifying drugs that prevent the ectopic cells from forming, we deduce that the ectopic cells in the larva derive from precocious activation of APSCs to form pigment cells. We propose that a novel population of APSCs are associated with the blood vessels, that these are held in a quiescent state by signals coming from these vessels, and that these signals depend upon ednraa. Together this opens up an exciting opportunity to identify the signals maintaining APSC quiescence in zebrafish.


Development ◽  
2002 ◽  
Vol 129 (5) ◽  
pp. 1095-1105 ◽  
Author(s):  
Jon P. Golding ◽  
Monica Dixon ◽  
Martin Gassmann

Within the developing vertebrate head, neural crest cells (NCCs) migrate from the dorsal surface of the hindbrain into the mesenchyme adjacent to rhombomeres (r)1 plus r2, r4 and r6 in three segregated streams. NCCs do not enter the intervening mesenchyme adjacent to r3 or r5, suggesting that these regions contain a NCC-repulsive activity. We have used surgical manipulations in the chick to demonstrate that r3 neuroepithelium and its overlying surface ectoderm independently help maintain the NCC-free zone within r3 mesenchyme. In the absence of r3, subpopulations of NCCs enter r3 mesenchyme in a dorsolateral stream and an ectopic cranial nerve forms between the trigeminal and facial ganglia. The NCC-repulsive activity dissipates/degrades within 5-10 hours of r3 removal. Initially, r4 NCCs more readily enter the altered mesenchyme than r2 NCCs, irrespective of their maturational stage. Following surface ectoderm removal, mainly r4 NCCs enter r3 mesenchyme within 5 hours, but after 20 hours the proportions of r2 NCCs and r4 NCCs ectopically within r3 mesenchyme appear similar.


Development ◽  
2000 ◽  
Vol 127 (14) ◽  
pp. 3031-3044 ◽  
Author(s):  
D.M. Parichy ◽  
D.G. Ransom ◽  
B. Paw ◽  
L.I. Zon ◽  
S.L. Johnson

Developmental mechanisms underlying traits expressed in larval and adult vertebrates remain largely unknown. Pigment patterns of fishes provide an opportunity to identify genes and cell behaviors required for postembryonic morphogenesis and differentiation. In the zebrafish, Danio rerio, pigment patterns reflect the spatial arrangements of three classes of neural crest-derived pigment cells: black melanocytes, yellow xanthophores and silver iridophores. We show that the D. rerio pigment pattern mutant panther ablates xanthophores in embryos and adults and has defects in the development of the adult pattern of melanocyte stripes. We find that panther corresponds to an orthologue of the c-fms gene, which encodes a type III receptor tyrosine kinase and is the closest known homologue of the previously identified pigment pattern gene, kit. In mouse, fms is essential for the development of macrophage and osteoclast lineages and has not been implicated in neural crest or pigment cell development. In contrast, our analyses demonstrate that fms is expressed and required by D. rerio xanthophore precursors and that fms promotes the normal patterning of melanocyte death and migration during adult stripe formation. Finally, we show that fms is required for the appearance of a late developing, kit-independent subpopulation of adult melanocytes. These findings reveal an unexpected role for fms in pigment pattern development and demonstrate that parallel neural crest-derived pigment cell populations depend on the activities of two essentially paralogous genes, kit and fms.


2007 ◽  
Vol 27 (1) ◽  
pp. 45-52
Author(s):  
Koh-ichi Atoh ◽  
Manae S. Kurokawa ◽  
Hideshi Yoshikawa ◽  
Chieko Masuda ◽  
Erika Takada ◽  
...  

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