scholarly journals Differential growth is a critical determinant of zebrafish pigment pattern formation

2021 ◽  
Author(s):  
Robert N. Kelsh ◽  
Jennifer P. Owen ◽  
Christian A. Yates
Keyword(s):  
Pattern Formation ◽  
Pigment Cell ◽  
Model Organism ◽  
Cell Types ◽  
Wild Type ◽  
Differential Growth ◽  
Critical Determinant ◽  
Pigment Pattern ◽  
Pattern Development ◽  
Mechanistic Basis

The skin patterns of vertebrates are formed by complex interactions between pigment-producing cells during development. Adult zebrafish (Danio rerio), a model organism for investigating the underlying patterning processes, display alternating horizontal blue and golden stripes, generated by the self-organisation of three pigment cell-types. Mathematical studies in which these cells are modelled as individual agents communicating via short- and long-range interactions have produced breakthroughs in the understanding of pattern development. These models, incorporating all experimentally evidenced cell-cell interactions, replicate many aspects of wild-type and mutant zebrafish patterns. Although received wisdom suggested that initial iridophore distribution was pivotal in orienting patterning, here we show that growth can override its influence. Altered growth sequences can generate further pattern modulation, including vertical stripes and maze-like patterns. We demonstrate that ventrally-biased (asymmetric) growth of the skin field explains two key zebrafish pattern development features which are otherwise obscure (dorso-ventral pattern asymmetry, and predominant ventral-to-dorsal migration of melanophores) in wild-type and multiple zebrafish mutants, and in the related species Danio nigrofasciatus. By identifying biased growth as a novel patterning mechanism, our study will inform future investigations into the mechanisms and evolution of fish pigment patterning and vertebrate pigment pattern formation. Furthermore, our work has implications for the mechanistic basis of human pigmentation defects.

scholarly journals A quantitative modelling approach to zebrafish pigment pattern formation

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Jennifer P Owen ◽  
Robert N Kelsh ◽  
Christian A Yates
Keyword(s):  
Pattern Formation ◽  
Individual Cell ◽  
Cell Types ◽  
Domain Growth ◽  
Wild Type ◽  
Pigment Pattern ◽  
Rule Set ◽  
Pattern Development ◽  
Self Organisation ◽  
Modelling Approach

Pattern formation is a key aspect of development. Adult zebrafish exhibit a striking striped pattern generated through the self-organisation of three different chromatophores. Numerous investigations have revealed a multitude of individual cell-cell interactions important for this self-organisation, but it has remained unclear whether these known biological rules were sufficient to explain pattern formation. To test this, we present an individual-based mathematical model incorporating all the important cell-types and known interactions. The model qualitatively and quantitatively reproduces wild type and mutant pigment pattern development. We use it to resolve a number of outstanding biological uncertainties, including the roles of domain growth and the initial iridophore stripe, and to generate hypotheses about the functions of leopard. We conclude that our rule-set is sufficient to recapitulate wild-type and mutant patterns. Our work now leads the way for further in silico exploration of the developmental and evolutionary implications of this pigment patterning system.

Zebrafish Pigment Pattern Formation: Insights into the Development and Evolution of Adult Form

2019 ◽  
Vol 53 (1) ◽  
pp. 505-530 ◽  
Author(s):  
Larissa B. Patterson ◽  
David M. Parichy
Keyword(s):  
Pattern Formation ◽  
Pigment Cell ◽  
Cell Lineage ◽  
Pigment Cells ◽  
Cellular Interactions ◽  
Lineage Specification ◽  
Pigment Pattern ◽  
Adult Form ◽  
Pattern Development ◽  
Pigment Patterns

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.

scholarly journals Topological data analysis of zebrafish patterns

2020 ◽  
Vol 117 (10) ◽  
pp. 5113-5124 ◽  
Author(s):  
Melissa R. McGuirl ◽  
Alexandria Volkening ◽  
Björn Sandstede
Keyword(s):  
Data Analysis ◽  
Pattern Formation ◽  
Large Scale ◽  
Model Organism ◽  
Topological Data Analysis ◽  
Wild Type ◽  
Cell Dynamics ◽  
Global Pattern ◽  
Agent Based ◽  
Topological Data

Self-organized pattern behavior is ubiquitous throughout nature, from fish schooling to collective cell dynamics during organism development. Qualitatively these patterns display impressive consistency, yet variability inevitably exists within pattern-forming systems on both microscopic and macroscopic scales. Quantifying variability and measuring pattern features can inform the underlying agent interactions and allow for predictive analyses. Nevertheless, current methods for analyzing patterns that arise from collective behavior capture only macroscopic features or rely on either manual inspection or smoothing algorithms that lose the underlying agent-based nature of the data. Here we introduce methods based on topological data analysis and interpretable machine learning for quantifying both agent-level features and global pattern attributes on a large scale. Because the zebrafish is a model organism for skin pattern formation, we focus specifically on analyzing its skin patterns as a means of illustrating our approach. Using a recent agent-based model, we simulate thousands of wild-type and mutant zebrafish patterns and apply our methodology to better understand pattern variability in zebrafish. Our methodology is able to quantify the differential impact of stochasticity in cell interactions on wild-type and mutant patterns, and we use our methods to predict stripe and spot statistics as a function of varying cellular communication. Our work provides an approach to automatically quantifying biological patterns and analyzing agent-based dynamics so that we can now answer critical questions in pattern formation at a much larger scale.

scholarly journals Airinemes: thin cellular protrusions mediate long-distance signalling guided by macrophages

Open Biology ◽  
2020 ◽  
Vol 10 (8) ◽  
pp. 200039
Author(s):  
Dae Seok Eom
Keyword(s):  
Pigment Cell ◽  
Cell Communication ◽  
Cell Types ◽  
Propagation Model ◽  
Long Distance ◽  
Signalling Molecules ◽  
Intercellular Signalling ◽  
Pattern Development ◽  
Cellular Protrusion ◽  
Distinct Morphology

Understanding the mechanisms of cell-to-cell communication is one of the fundamental questions in biology and medicine. In particular, long-range signalling where cells communicate over several cell diameters is vital during development and homeostasis. The major morphogens, their receptors and intracellular signalling cascades have largely been identified; however, there is a gap in our knowledge of how such signalling factors are propagated over a long distance. In addition to the diffusion-based propagation model, new modalities of disseminating signalling molecules have been identified. It has been shown that cells can communicate with direct contact through long, thin cellular protrusions between signal sending and receiving cells at a distance. Recent studies have revealed a type of cellular protrusion termed ‘airinemes’ in zebrafish pigment cell types. They share similarities with previously reported cellular protrusions; however, they also exhibit distinct morphology and features. Airinemes are indispensable for pigment pattern development by mediating long-distance Delta-Notch signalling between different pigment cell types. Notably, airineme-mediated signalling is dependent on skin-resident macrophages. Key findings of airineme-mediated intercellular signalling in pattern development, their interplay with macrophages and their implications for the understanding of cellular protrusion-mediated intercellular communication will be discussed.

scholarly journals Genetic regulation and pattern formation: A study of the yellow locus in Drosophila melanogaster

1974 ◽  
Vol 24 (1) ◽  
pp. 19-26 ◽  
Author(s):  
William G. Nash ◽  
Rhoda J. Yarkin
Keyword(s):  
Drosophila Melanogaster ◽  
Pattern Formation ◽  
Genetic Regulation ◽  
Phenotypic Expression ◽  
Type A ◽  
Cell Types ◽  
Wild Type ◽  
Unique Pattern ◽  
Distinct Cell ◽  
Different Cell Types

SUMMARYMany of the yellow alleles found in Drosophila melanogaster result in a unique pattern of phenotypic expression. These patterns follow the morphologically distinct cell types of the cuticle, so that for one allele all the bristles of the head and thorax might be mutant, while most of the fly appears wild type. A comparison of many different y mutants demonstrates that the yellow phenotype is expressed independently in most if not all the different cell types which form the cuticle. Control of this expression appears to reside at the yellow locus itself.

scholarly journals Disruption of the mouse MRF4 gene identifies multiple waves of myogenesis in the myotome

Development ◽  
1995 ◽  
Vol 121 (10) ◽  
pp. 3347-3358 ◽  
Author(s):  
A. Patapoutian ◽  
J.K. Yoon ◽  
J.H. Miner ◽  
S. Wang ◽  
K. Stark ◽  
...  
Keyword(s):  
Pattern Formation ◽  
Cell Types ◽  
Wild Type ◽  
Mild Phenotype ◽  
Nonmuscle Cell ◽  
Cellular Recruitment ◽  
Targeted Recombination ◽  
Myod Expression ◽  
Newborn Animals ◽  
Candidate Regulator

MRF4 (herculin/Myf-6) is one of the four member MyoD family of transcription factors identified by their ability to enforce skeletal muscle differentiation upon a wide variety of nonmuscle cell types. In this study the mouse germline MRF4 gene was disrupted by targeted recombination. Animals homozygous for the MRF4bh1 allele, a deletion of the functionally essential bHLH domain, displayed defective axial myogenesis and rib pattern formation, and they died at birth. Differences in somitogenesis between homozygous MRF4bh1 embryos and their wild-type littermates provided evidence for three distinct myogenic regulatory programs (My1-My3) in the somite, which correlate temporally and spatially with three waves of cellular recruitment to the expanding myotome. The first program (My1), marked initially by Myf-5 expression and followed by myogenin, began on schedule in the MRF4bh1/bh1 embryos at day 8 post coitum (E8). A second program (My2) was highly deficient in homozygous mutant MRF4 embryos, and normal expansion of the myotome failed. Moreover, expression of downstream muscle-specific genes, including FGF-6, which is a candidate regulator of inductive interactions, did not occur normally. The onset of MyoD expression around E10.5 in wild-type embryos marks a third myotomal program (My3), the execution of which was somewhat delayed in MRF4 mutant embryos but ultimately led to extensive myogenesis in the trunk. By E15 it appeared to have largely compensated for the defective My2 program in MRF4 mutants. Homozygous MRF4bh1 animals also showed improper rib pattern formation perhaps due to the absence of signals from cells expressing the My2 program. Finally, a later and relatively mild phenotype was detected in intercostal muscles of newborn animals.

The pigmentary system of developing axolotls

Development ◽  
1984 ◽  
Vol 81 (1) ◽  
pp. 105-125
Author(s):  
S. K. Frost ◽  
L. G. Epp ◽  
S. J. Robinson
Keyword(s):  
Developmental Stages ◽  
Pigment Cell ◽  
Cell Types ◽  
Ambystoma Mexicanum ◽  
Pigment Cells ◽  
Wild Type ◽  
Cell Type ◽  
Electron Microscopic ◽  
Transmission Electron ◽  
Mutant Phenotypes

A biochemical and transmission electron microscopic description of the wild-type pigment phenotype in developing Mexican axolotls (Ambystoma mexicanum) is presented. There are three pigment cell types found in adult axolotl skin - melanophores, xanthophores and iridophores. Both pigments and pigment cells undergo specific developmental changes in axolotls. Melanophores are the predominant pigment cell type throughout development; xanthophores occur secondarily and in fewer numbers than melanophores; iridophores do not appear until well into the larval stage and remain thereafter as the least frequently encountered pigment cell type. Ultrastructural differences in xanthophore organelle (pterinosome) structure at different developmental stages correlate with changes in the pattern of pteridine biosynthesis. Sepiapterin, a yellow pteridine, is present in larval axolotl skin but not in adults. Ribofiavin (also yellow) is present in minimal quantities in larval skin and large quantities in adult axolotl skin. Pterinosomes undergo a morphological “reversion” at some point prior to or shortly after axolotls attain sexual maturity. Correlated with the neotenic state of the axolotl, certain larval pigmentary features are retained throughout development. Notably, the pigment cells remain scattered in the dermis such that no two pigment cell bodies overlap, although cell processes may overlap. This study forms the basis for comparison of the wild type pigment phenotype to the three mutant phenotypes-melanoid, axanthic and albino-found in the axolotl.

An orthologue of the kit-related gene fms is required for development of neural crest-derived xanthophores and a subpopulation of adult melanocytes in the zebrafish, Danio rerio

Development ◽  
2000 ◽  
Vol 127 (14) ◽  
pp. 3031-3044 ◽  
Author(s):  
D.M. Parichy ◽  
D.G. Ransom ◽  
B. Paw ◽  
L.I. Zon ◽  
S.L. Johnson
Keyword(s):  
Neural Crest ◽  
Danio Rerio ◽  
Receptor Tyrosine Kinase ◽  
Pigment Cell ◽  
Pigment Cells ◽  
Pigment Pattern ◽  
Cell Behaviors ◽  
Pattern Development ◽  
And Migration ◽  
Pigment Patterns

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.

An experimental investigation into the early development of the chick elbow joint

Development ◽  
1977 ◽  
Vol 39 (1) ◽  
pp. 115-127
Author(s):  
N. Holder
Keyword(s):  
Experimental Investigation ◽  
Pattern Formation ◽  
Early Development ◽  
Elbow Joint ◽  
Cell Types ◽  
Joint Region ◽  
Differential Growth ◽  
Joint Formation ◽  
Early Stages ◽  
Wing Bud

The theory that differential growth of opposed chondrogenic centres is important in early joint formation has been tested experimentally by removing structures in relation to the chick elbow joint. The humerus and its cap of differentiating joint cells were found to develop independently of structures distal to them. Removal of the presumptive joint region at early stages resulted in fusion of the humerus with the radius and ulna. Results are discussed in terms of concepts concerning pattern formation of cell types in the early wing-bud.

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