Trends in Genetics
ReviewIs pigment patterning in fish skin determined by the Turing mechanism?
Section snippets
How do skin patterns form?
The beauty and variety of animal pigmentation patterns have an attraction not only for the public, but also for developmental biologists interested in understanding the formation of such patterns 1, 2. Two characteristics have piqued the curiosity of developmental biologists about the underlying mechanism of pattern formation. The first is the variation in patterns among closely related species. For example, one can see by going to an aquarium that pigment patterns of fish vary extensively
Zebrafish as a model organism to study pigment patterning
Among the many animal species that have skin patterns, the zebrafish is the only model organism for which a variety of techniques for genetic manipulation 20, 21 and a library of mutant lines 22, 23, 24 are both available. As a result of these obvious advantages, studies involving zebrafish have been the leading source for information about patterning in skin pigmentation [25]. These studies have also produced several mutants, and have uncovered the involvement of numerous genes in the
Involvement of pigment cells in pattern formation
When one of the pigment cell types that constitute the pattern of stripes in zebrafish is lost due to a mutation, the entire pattern is lost, suggesting that the pattern is induced by the mutual interaction between the pigment cells. In zebrafish mutants lacking melanophores (Figure 2, nac) [42] or xanthophores (Figure 2, pfe) [43], no distinct patterns form in the body or in the fins. In zebrafish lacking iridophores, the pattern of stripes in the body is lost, but the stripes in the fins are
Interactions between pigment cells
To illuminate the patterning mechanism, the exact nature of the actual interactions between the pigment cells first needs to be elucidated. Given that the interactions between melanophores and xanthophores can drive pattern formation, at least in the fins, we focus first on these cells. The contribution of iridophores to body patterning is discussed thereafter.
To understand the role of the interactions between melanophores and xanthophores in stripe formation, Maderspacher and Nuesslein-Volhard
Identification of feedback loops consistent with the Turing model
The inferred interaction network between melanophores and xanthophores is shown in Figure 3. There are two feedback loops in this network. One involves mutual inhibitory interactions that function locally. Given that this feedback loop contains two negative interactions, it produces a similar result to that of a positive feedback loop. The second feedback loop is one in which melanophores exhibit a local, negative effect on xanthophores, while the latter induce a long-range, positive effect on
Mechanisms of cell–cell interactions
Recent attempts to identify the molecular and cellular factors involved in the cell–cell interactions that are responsible for pattern formation have revealed some unexpected cellular events and roles in the interaction network. For example, Inaba et al. isolated pigment cells from fins and plated them in a culture dish to study the in vitro behavior of mixed melanophores and xanthophores [60]. They found that xanthophores extend dendrites toward melanophores, and that contact with a
The role of iridophores in body stripes
In the fins, where the pigment pattern comprises melanophores and xanthophores, the interaction network described above is sufficient to explain pattern formation. However, in the body trunk, pigment patterns cannot form without iridophores 45, 46, 55, 56. Recent investigations focused on iridophores are gradually revealing the role of this cell type in pigment pattern formation. Iridophores are the first cell type to form clusters in the hypodermis of the body trunk 55, 63. Detailed tracking
Directionality of stripes
Local interactions, such as those responsible for pattern formation in the Turing model, cannot establish the global directionality of the pattern. Specifying the direction of the stripes first requires settling on an orientation, based on some specific biological indicator [15]. In the absence of directionality, a labyrinthine pattern develops [15]. In contrast to the body trunk, which grows uniformly during development, the fins grow mainly at the end (i.e., they undergo appositional growth).
A Turing mechanism is consistent with the current model
As discussed above, experimental studies over 15 years have gradually revealed the underlying mechanism of pigment pattern formation in zebrafish. Some findings were expected based on the original Turing model, but others were not.
Artificial ablation of pigment cells induced the dynamic regeneration of the pigment pattern that is specifically predicted based on the mathematical model [14], and the interaction network that is deduced from various cellular analyses satisfies the conditions that
Concluding remarks and future directions
Although the actual biological mechanism for pigment pattern formation has been outlined, many of the molecular details remain unknown. The nature of the signal transduction at the tip of the cell projection should be verified through more experiments of a definitive nature, and it is possible that some important interactions have not yet been identified. The role of iridophores is also an important subject for further study, and our understanding of the putative network that is currently known
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2021, Current Opinion in Genetics and DevelopmentCitation Excerpt :Exquisite pigmentation markings have served as emblematic examples. Natural and laboratory-induced zebra fish pigmentation variants or differences between jaguar and leopard spots can be recapitulated with the same Turing models using value modifications of diffusion, degradation, or concentration [25,26]. Modifying the size or shape of simulation frames reproduced different snake pigment patterns [27], changes in stripe numbers in marine angelfish at different stages of growth [28], or changes from stripes to spots according to body location in wildcats [29].