American Journal of Botany 91 10 1726 1741 2004 THE EVOLUTION OF PLANT DEVELOPMENT1 WILLIAM E FRIEDMAN 2 4 RICHARD C MOORE 3 4 MICHAEL D PURUGGANAN3 5 AND Department of Ecology and Evolutionary Biology University of Colorado Boulder Colorado 80309 USA and 3Department of Genetics Box 7614 North Carolina State University Raleigh North Carolina 27695 USA 2 The last decade has witnessed a resurgence in the study of the evolution of plant development combining investigations in systematics developmental morphology molecular developmental genetics and molecular evolution The integration of phylogenetic studies structural analyses of fossil and extant taxa and molecular developmental genetic information allows the formulation of explicit and testable hypotheses for the evolution of morphological characters These comprehensive approaches provide opportunities to dissect the evolution of major developmental transitions among land plants including those associated with apical meristems the origins of the root shoot dichotomy diversification of leaves and origin and subsequent modification of flower structure The evolution of these major developmental innovations is discussed within both phylogenetic and molecular genetic contexts We conclude that it is the combination of these approaches that will lead to the greatest understanding of the evolution of plant development Key words apical meristem flower leaf origin plant systematics root shoot Evolutionary developmental biology or the study of the underlying developmental basis for the origin and diversification of organismic structure has matured into a vigorous discipline in the last 20 years Beginning in the 1970s with such seminal works as those by Eldredge and Gould on punctuated equilibrium 1972 Gould Ontogeny and Phylogeny 1977 Alberch et al on the formalization of heterochronic models of developmental evolution 1979 and McKinney and McNamara Heterochrony The Evolution of Ontogeny 1991 as well as earlier papers attention was focused on the role of development during the evolutionary diversification of metazoan morphology Within only a few years modification of development with respect to timing heterochrony ontogenetic sequence addition or deletion of specific developmental events and positional status heterotopy as well as analysis of the rate of evolutionary change i e gradual vs saltational or punctuated had become central themes in the search for explanation of the historical pattern of metazoan diversity At approximately the same time the century and a half old discipline of animal embryology which had been excluded from the evolutionary modern synthesis of the 1940s and 1950s Gilbert et al 1996 began to undergo a resurgence Embryologists began to incorporate molecular and genetic techniques into their studies of early developmental events Discovery of the homeobox genes in Drosophila Scott and Weiner 1984 McGinnis et al 1984 and elucidation of the ubiquitous roles of homeobox containing genes in the establishment of developmental pattern in phylogenetically diverse metazoans Caenorhabditis elegans Drosophila Xenopus and Mus Wilkins 2002 Arthur 2002 led to a revival of interest in the mechanistic basis of evolutionary diversification By the mid 1980s molecular biologists embryologists comparative morphologists and paleontologists shared a common vision Manuscript received 27 April 2004 revision accepted 22 June 2004 The authors thank Pamela Diggle Joseph Williams Jennifer Winther Jonathan Krieger and Devin O Connor for helpful discussions The authors also thank three reviewers Mark Chase Michael Frolich and one anonymous reviewer for their helpful comments and suggestions This work was funded in part by grants from NSF to W E F and M D P 4 These authors contributed equally to the paper 5 E mail michaelp unity ncsu edu 1 and goal the complete explanation of the evolutionary history of developmental modifications that have given rise to the diversity of extant and extinct metazoans The study of the evolution of development was initially driven by studies of animal systems However it remains unclear to what extent the results from animal systems can be generalized to plants Plants and animals each evolved independently from unicellular ancestors For this reason alone it seems likely that many if not most of the specific molecular developmental mechanisms underlying the evolution of multicellularity and structural complexity in these two major groups of complex eukaryotes will differ in significant ways Kaplan and Hagemann 1991 Meyerowitz 2002 Thus the principles that have been elucidated in the study of animal evolutionary developmental biology may have limited explanatory powers in the realm of plant diversification The resurgence in the study of the evolution of plant development in recent years has been accelerated in part by recent successes in elucidating the molecular genetic basis of plant developmental processes including the isolation and characterization of genes that underlie flower leaf and root development see also reviews by Cronk 2001 Shepard and Purugganan 2002 Kellogg 2004 For example the identification of the role of MADS box transcription factor genes in flower development in several model angiosperm species such as Arabidopsis thaliana Antirrhinum majus and Zea mays provided the basis for early studies on the molecular evolution of genes that control the development of floral structure as well as subsequent analyses of these genes in a number of other nonflowering plant taxa Purugganan et al 1995 Theissen 2001 Lawton Rauh et al 2000 There remain however major gaps in our understanding of the evolution of plant development and morphological homology Progress in the field will have to be driven both by successes and opportunities provided by molecular developmental genetic studies as well as a more robust understanding of plant phylogenetic relationships and continued analysis of comparative plant morphologies of extant and most importantly extinct taxa In this review we will address basic questions associated with the broad evolutionary developmental history of the bauplan and organs of land plants We will also 1726 October 2004 FRIEDMAN ET AL EVOLUTION OF PLANT DEVELOPMENT Fig 1 Evolution of apical growth The common ancestor of embryophytes and their closest relatives display apical growth in the gametophyte generation Charales lack an alternation of generations the only diploid phase is the zygote Apical
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