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Creativity and development¹

⁰ Department of Environmental, Population and Organismic Biology, University of Colorado, Boulder 80309-0334 USA

	INTRODUCTION

TOP INTRODUCTION A MODEL OF DEVELOPMENTAL... CREATIVITY AND DEVELOPMENT HISTORICAL CONTEXT CONCLUSIONS LITERATURE CITED

 
The goal of The art of genes: how organisms make themselves, by Enrico Coen, is to create a "broadly accessible picture of our current knowledge of how organisms develop." Coen is ideally qualified to provide this synthetic overview of genes and development. He has been a leader in the field of molecular genetics for over two decades and his work on the snapdragon, Antirhhinum majus, has provided one of the two most widely used model systems for study of the genetic control of development. In order to communicate the essence of organismal development to a broad audience that includes nonbiologists, Coen weaves a comparison of painting and development throughout the text. He uses not only the mechanics of art, how different effects of color, light, and shadow are achieved, but he also makes extensive reference to the artistic or creative process by which a painting emerges. This dual aspect of the analogy is important for an extended subtext of the book. Although the primary goal is to explain mechanism, Coen also argues persuasively for the view that development should not be understood as a process of replicating organisms according to a blue-print or set of instructions. Rather, development should be viewed as a creative process.

	A MODEL OF DEVELOPMENTAL COLORS

TOP INTRODUCTION A MODEL OF DEVELOPMENTAL... CREATIVITY AND DEVELOPMENT HISTORICAL CONTEXT CONCLUSIONS LITERATURE CITED

 
Coen uses the analogy with art to create a simple genetic model that explains an astonishing variety of developmental processes in plants and animals. The centerpiece of this model is the notion of "hidden colors." Hidden colors are initially introduced as properties of regions of cells or tissues that only become apparent as "interpreting genes" respond to them. In addition to hidden colors and interpreting genes, the model includes "scents" or signaling proteins, and "sensitivities" or receptor proteins. To introduce each of these elements of developmental genetics, Coen draws examples and analogies from a variety of sources that include literature (from Kafka to Conan Doyle), language, manners, games, and even a dog's view of the world. Examples from paintings, some familiar and some less so, are always included. Coen assembles the model in stages over the course of several chapters, each of which addresses an important aspect of organismal development.

There are many ways to begin to describe the process of development. One choice would be to begin at the beginning with the zygote, and to describe the various processes that transform the single-celled zygote to the adult. Coen chooses an alternative strategy and begins by addressing the more fundamental process of pattern formation. "Plants, animals and fungi display a remarkable array of highly ordered and coherent patterns. ...[H]ow is this wonderful diversity of natural pattern produced?" Coen uses concrete examples of experimental approaches to understanding pattern formation in flies and butterflies (e.g., Stearns, 1968 ), and more fanciful examples such as a cheering section at a football stadium using cards to spell out messages, to introduce the first component of his basic model of development, "hidden colors." "Hidden colors" are an underlying prepattern or frame of reference that exists within developing organisms. Regions of hidden color (e.g., the regions of a floral meristem in the familiar ABC model [Coen and Meyerowitz, 1991 ]) are the result of the production of master proteins by one or more genes. Neither these genes, nor the colors they produce represent instructions for how to construct a particular type of structure, tissue, or organ. That is the task of other genes that interpret the colors. Coen calls these interpreting genes.

The description of development as dependent on a pattern of hidden colors to which interpreting genes respond begs the next question: where does the pattern of hidden colors come from? What pattern establishes the pattern? The chapter entitled "Refining a Pattern" tackles this question of how pattern is established, and is perhaps the best chapter in the entire book for the elegance of both explanation and process explained. Coen begins with a fertilized Drosophila egg, in which there is already a concentration gradient of hidden color (master protein) established within the cytoplasm. Coen illustrates this as a gray scale, grading from black (high concentration) at one end through shades of gray (decreasing concentrations) to white. Coen then describes the potential for varying the response of interpreting genes within this gradient by introducing two concepts: (1) variation in the threshold level of master proteins required for activation of interpreting genes; and (2) variation in the affinity of those genes to a single level of master protein. Both mechanisms allow the gradient to be interpreted in different ways. Coen then describes how a gray scale (a continuous gradient of a single gene product) in the zygote is transformed into a rainbow of colors (distinct bands of expression of many different interpreting genes) in a fly larva. It is unfortunate that the book did not include some color illustrations; these would have enhanced the sense of magic at the transformation of a dull gradient of shades of gray (in fact, a gradient of a single master protein produced by the bicoid gene) into a multicolored rainbow of differential gene expression. This chapter ends with one of the paradoxes of development: egg cells contain a variety of gradients that are critical to establishing the "hidden colors" on which subsequent rainbow patterns of differentiation depend. How do these gradients originate? They depend on patterns already present in the maternal tissues that produce and surround the egg. Pattern is always the result of previous pattern.

The preceding discussions build upon the first two elements of Coen's model: interactions between hidden colors and interpreting genes. In a chapter with the Austenesque title "Scents and Sensitivities" Coen introduces the remaining components of his model of gene expression and regulation: signaling proteins and receptor proteins. He begins by developing an analogy with smell to explain how cells communicate with one another. Scents are signals, sensibilities are the receptors, and the process of "cellular sniffing" can result in further developmental complexities because cells can respond to one another. One cell can influence gene expression in its neighbors.

Having introduced new mechanisms to modify gene expression, scents, and sensitivities, Coen uses these in subsequent chapters to expand on the processes of pattern formation and to explore how organismic complexity arises during development. The first topic is symmetry. Organisms usually display a greater degree of symmetry during early development than they do at maturity. How do initially symmetrical organisms come to have a head and a tail, a back and a front (bilateral symmetry)? How does a radially symmetrical flower meristem produce a bilaterally symmetrical flower? The discussion of symmetry and asymmetry then moves "Beneath the Surface" to show how the distinction between "inside" and "outside" is established. A description of gastrulation is obviously appropriate here, and Coen shows how the pattern of gastrulation is related to a prepattern of asymmetry established in the egg. The analysis of the establishment of the internal/external asymmetry of plants is one of the few instances where I felt that Coen's discussion was lacking. He merely states that because there is no cell movement, the "outside" of the plant is established in the egg/zygote. This hardly provides insights into the complex factors or processes that establish the distinctive differences between the dermal tissue system and the internal tissues of a developing plant embryo (see, e.g., Bruck and Walker, 1985 ; Kaplan and Cooke, 1997 ).

"The Expanding Canvas" (Chapter 8) introduces timing and scale to the discussion of pattern formation. Development involves not only differentiation but it involves growth. Although the organism becomes larger, the scale of variation in hidden colors (and hence differences in expression of interpreting genes) is relatively uniform and typically encompasses regions of a few cells. There is a uniformity of scale at the level of gene expression. However, genes that will affect more comprehensive parts of structures (e.g., whole flowers) are expressed early, and as a result they ultimately affect large areas due to growth and cell proliferation. Pattern is continually refined as the organism expands, but the refinements occur at a constant scale. In later chapters Coen shows how deformations and differential growth (allometry) can be explained by patterns of "hidden colors," and how growth itself can change patterns of gene expression. There is a two-way interaction between color and canvas (genes and organism).

The penultimate chapter, "The Story of Color," considers the evolution of "hidden colors," i.e., the evolution of development. What is the origin of the complex patterns of variation in gene expression that creates a multicellular organism from a single-celled zygote? Coen begins with a discussion of the complexity of gene expression in unicellular organisms. In considering the evolution of multicellularity, he moves from the capacity of unicells to respond to changes in their environment over time, to the ability of cells within multicellular organisms to respond to variation in location. Response to temporal variation has been recruited for the establishment of spatial variation. "The history of internal painting [multicellular development] is a story of putting old genes to new uses." Coen elaborates on this notion of genetic recruitment in the final chapter with an exploration of the well-known idea of evolution as tinkering (Bower, 1898 ; Jacob, 1982 ).

	CREATIVITY AND DEVELOPMENT

TOP INTRODUCTION A MODEL OF DEVELOPMENTAL... CREATIVITY AND DEVELOPMENT HISTORICAL CONTEXT CONCLUSIONS LITERATURE CITED

 
Coen not only uses the analogy with art to explain mechanisms of development, he also makes use of the analogy for an extended discussion of the parallels between development and creativity. The first chapter begins with a review of the understanding of development throughout history and ends with a summary of modern metaphors for development. Coen criticizes the usual metaphors for how a single cell, the zygote, becomes a complex organism. If development is likened to following a set of instructions or a blueprint or computer program (encoded in the genome), this analogy breaks down when you ask how the instructions are followed. Where does the factory or assembly line or computer (choose your model) come from? What is the appropriate model for the developmental process that does not separate the maker from the made (hence, how do organisms make themselves)? In this way, Coen introduces one of the themes of the book, "...that human creativity comes much nearer to the process of development than the notion of manufacturing according to a set of instructions, or the running of a computer program." Coen also sets the stage for his emphasis on the interactive and contingent nature of development. Development is too often conceived of or modeled as a linear process. In fact, as Coen emphasizes throughout the book, each step in a developmental process is dependent on the interpretation of what came before. Epigenetic processes, although not encoded in the DNA, are critical to development.

Coen returns to this theme of creativity and development in several chapters. For example, in "Creative Reproduction" (Chapter 10) he asks: Is there a fundamental contradiction between creativity and reproducibility? Creativity is associated with the production of something new and novel, whereas development is associated with reproducibility, the production of the "same" thing, over and over. Coen draws parallels between creativity and development by noting that both depend upon a complex process of action, interaction, and reaction in which plan and execution are deeply interwoven and inseparable. In a chapter on plasticity (Chapter 12) Coen emphasizes that "development is a highly interactive process in which each step is an interpretation of what went before." And that "development ...always [occurs] in the context of a particular set of environmental conditions." Consideration of the influence of the environment on development of both plants and animals leads to the wonderful assertion that learning is "simply a more plant-like form of development [!], in which the organism modifies its internal patterns in response to variation in its surroundings." The internal patterns here refer to the set of connections between the neurons of the brain. The culmination of this running argument on development and creativity is the conclusion that creativity is, in part, the result of brain development. Creativity is a developmental process and development is a creative process.

	HISTORICAL CONTEXT

TOP INTRODUCTION A MODEL OF DEVELOPMENTAL... CREATIVITY AND DEVELOPMENT HISTORICAL CONTEXT CONCLUSIONS LITERATURE CITED

 
In addition to the themes of painting, color, and creativity that are a constant motif throughout the book, Coen also draws upon the history of biology. He meticulously describes the seminal studies that first established the genetic mechanisms he explains. Moreover, he uses results from modern developmental genetics to provide new insights (or at least new perspectives) into old problems of comparative morphology. For example, in "The Hidden Skeleton" (Chapter 7), Coen brings the discovery of the universality of hox genes to bear on the well-known 19^th century debate between Georges Cuvier and Etienne Geoffroy Saint-Hilaire (summarized in Appel 1987 ). Coen argues that, ultimately, they were both correct. The two men were well-respected professors of comparative anatomy at the Musée d'Histoire Naturelle in Paris. Each was searching for an underlying principle with which to organize the diversity of animal anatomy. Cuvier's system was based on functional integration and he recognized four basic types of animals. Animals within each type could be compared fruitfully with one another, but to compare among groups, for example vertebrates with insects, was pointless. Geoffroy Saint-Hilaire approached the problem differently. He developed the "Principle of Connections" and maintained that there was a basic body layout that was common to all animals. Insects and vertebrates could be compared to discover the basic similarities. Darwin's theory of descent with modification seemed to reject Geoffroy Saint-Hilare's principle. The common ancestor of insects and vertebrates probably resembled neither group and the body plans of the two were derived independently. Over 100 years after Darwin, however, the discovery of hox genes showed that there is a common aspect to the organization of insects and vertebrates. They share a basic pattern of expression of hox genes (Duboule and Dollé, 1989 ; Graham, Papalopulu, and Krumlauf 1989 ). As Geoffroy Saint-Hilaire had proposed, there is a remarkable uniformity of organization, however it is at the level of developmental genetics. As Cuvier had proposed, the particular manifestations of development (the result of expression of many interpreting genes) have been accumulated separately in these groups and are not comparable.

Coen also addresses the issue, familiar to all botanists, of serial homology. How do we recognize repetition in the design of organisms, and what is the nature of this repetition? Coen returns to the analogy of art to introduce the notion of theme and variation (Chapter 15) and makes a distinction between explicit and implicit themes. Coen argues that much confusion about the nature of repetition in the living world has come from confounding implicit with explicit themes and uses Goethe's hypothesis of metamorphosis as an example. Goethe (1790) proposed that all lateral organs of plants were variations on a theme. Goethe needed a word for that "theme," that is, the underlying unity or similarity of these organs. He used the word "leaf" (blatt); he did not mean, however, the concrete "leaf," rather, the implicit theme of a leaf. Coen uses this story as an entrée to the larger issue of how to identify "implicit" themes, and his answer is, by their pattern of hidden colors; what is the repeated unit of gene expression? "The visible structures on a plant are based on the interpretation and elaboration of hidden patterns; patterns that can only be revealed by studying the activity of genes. ...[V]ariation is superimposed on the repeating patterns so that [the units] become manifest in different ways." Although Goethe is used to motivate this discussion, the genetic example provided is that of segmentation in flies. Many features of a fly larva show translational symmetry; they are repeated in the different segments, albeit with variation. Coen shows that the common "theme" expressed in segments can be identified as a repeated pattern of gene expression that is established during development. Similar studies are evidently not yet available for plants; we still cannot identify the "essence of a leaf" at the level of genes. These examples of the Cuvier-Saint Hilaire debate and Goethe's metamorphosis are but two of the many scattered throughout the chapters. They are integrated into the discussion of developmental genetics and serve to emphasize the continuity of scientific thought and discovery.

	CONCLUSIONS

TOP INTRODUCTION A MODEL OF DEVELOPMENTAL... CREATIVITY AND DEVELOPMENT HISTORICAL CONTEXT CONCLUSIONS LITERATURE CITED

 
This book was written for a lay audience, which the readers of the American Journal of Botany are not. Is it worth the read? It depends. As a learning tool for students, or a teaching tool for a biologist, its utility is limited in several ways. First, there are no citations. Thus, there is no straightforward way for a reader to pursue topics of interest. There is a short bibliography, however the text does not refer directly to those references; it is difficult to know how to use such a bibliography. The lack of citations is also troubling from the point of view of scholarship. Are all of the ideas developed in the book unique to Coen? Certainly not. Yet, a naive reader may well be confused or mislead about the origins of many of the concepts and conclusions expounded here. An additional limitation is a pedagogical one. Although the analogy to art is lovely and well developed, and the explanations are easily understood, a teacher must ultimately substitute the actual (initially unfamiliar) terms for those used to introduce concepts. Yet, throughout the text, "hidden colors" remain colors and never become the master proteins they were used to introduce. Likewise, "scents" never become signaling proteins and "sensitivities" never become receptors. As a result, although the reader comes to understand the genetics of development through use of analogy, the leap to actual biological terminology is not facilitated by the book. On the other hand, the explanations are elegant and easily followed without having any previous knowledge. Coen's explanations, models, and examples could be modified for use in lectures. For example, Coen emphasizes the use of mutants to unravel the mechanisms of developmental genetics and his explanations are some of the best I've read.

I suspect that for many, if not most, non-molecular biologists interested in learning more about developmental genetics, it would be more efficient to go directly to the primary literature for information on developmental genetics. However, the experience would not be nearly so enjoyable. The many subtexts of the book maintain one's interest, even when some of the most basic aspects of biology are reviewed. The analogies of art and creativity with development are engagingly intertwined throughout the text as the genetic model is introduced and elaborated. The analogy to art and painting is not only a useful heuristic device, it is also very entertaining to see this analogy grow and to evaluate the various nuances of color, paint, artists, and artistry. Does each new piece of the analogy work? For the most part, they do, although the analogy does become a bit strained in places. The comparison of creativity and development is perhaps the more profound subtext. It continually focused my attention on the critical importance of the models or metaphors that we use to communicate basic biological processes. If we continue to think about development as a linear process of reading a blueprint, then we ultimately limit our ability to study and to understand how development is actually accomplished. I would recommend this book less as a description of developmental genetics (although it is a good one) and more as a general thought-provoking read.

Submitted by Spencer C. H.BarrettBook Review Editor

	FOOTNOTES

 
¹ The art of genes: how organisms make themselves. Enrico Coen. 1999. Oxford University Press. viii + 386 pp., ISBN 0 19 85 03 43.

² Phone 303-492-4860, FAX 303-492-8699, e-mail Pamela.Diggle{at}colorado.edu

	LITERATURE CITED

TOP INTRODUCTION A MODEL OF DEVELOPMENTAL... CREATIVITY AND DEVELOPMENT HISTORICAL CONTEXT CONCLUSIONS LITERATURE CITED

 
Appel, T. A. 1987 The Cuvier-Geoffroy debate. Oxford University Press, New York, New York, USA.

Bower, F. O. 1898 The British Association. Bristol Meeting. Section K (Botany). Opening address by Prof. F. O. Bower, Sc.D., F.R.S., President of the section. II. Nature 59: 88–91. [CrossRef]

Bruck, D. K., and D. B. Walker. 1985 Cell determination during embryogenesis in Citrus jambhiri. I. Ontogeny of the epidermis. Botanical Gazette 146: 188–195. [CrossRef][ISI]

Coen, E. S., and E. M. Meyerowitz. 1991 The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37.

Duboule, D. and P. Dollé. 1989 The structural and functional organization of the murine HOX gene family resembles that of Drosophila homeotic genes. EMBO Journal 8: 1497–1505. [ISI][Medline]

Goethe, J. W. 1790 Goethe's botany: the metamorphosis of plants. Translated by A. Arber (1970). Chronica Botanica, Vol. 10, 67–115.

Graham, A., N. Papalopulu, and R. Krumlauf. 1989 The murine and Drosophila homeobox gene complexes have common features of organization and expression. Cell 37: 367–378.

Jacob, F. 1982 The actual and the possible. University of Washington Press, Seattle, Washington, USA.

Kaplan, D. R., and T. J. Cooke. 1997 Fundamental concepts in the embryogenesis of dicotyledons: a morphological interpretation of embryo mutants. Plant Cell 9: 1903–1919. [CrossRef][ISI][Medline]

Stearns, C. 1968 Developmental genetics of pattern. In Genetic mosiacs and other essays, 130–173. Harvard University Press, Cambridge, Massachusetts, USA.

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