1726American Journal of Botany 91(10): 1726–1741. 2004.THE EVOLUTION OF PLANT DEVELOPMENT1WILLIAME. FRIEDMAN,2,4RICHARDC. MOORE,3,4ANDMICHAELD. PURUGGANAN3,52Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, Colorado 80309 USA; and3Department ofGenetics, Box 7614, North Carolina State University, Raleigh, North Carolina 27695 USAThe last decade has witnessed a resurgence in the study of the evolution of plant development, combining investigations in system-atics, 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 andtestable hypotheses for the evolution of morphological characters. These comprehensive approaches provide opportunities to dissectthe evolution of major developmental transitions among land plants, including those associated with apical meristems, the origins ofthe root/shoot dichotomy, diversification of leaves, and origin and subsequent modification of flower structure. The evolution of thesemajor developmental innovations is discussed within both phylogenetic and molecular genetic contexts. We conclude that it is thecombination 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 un-derlying developmental basis for the origin and diversificationof organismic structure, has matured into a vigorous disciplinein the last 20 years. Beginning in the 1970s, with such seminalworks as those by Eldredge and Gould (on punctuated equi-librium; 1972), Gould (Ontogeny and Phylogeny; 1977), Al-berch et al. (on the formalization of heterochronic models ofdevelopmental evolution; 1979), and McKinney and McNa-mara (Heterochrony: The Evolution of Ontogeny; 1991, aswell as earlier papers), attention was focused on the role ofdevelopment during the evolutionary diversification of meta-zoan morphology. Within only a few years, modification ofdevelopment with respect to timing (heterochrony), ontoge-netic sequence (addition or deletion of specific developmentalevents), and positional status (heterotopy), as well as analysisof the rate of evolutionary change (i.e., gradual vs. saltationalor punctuated), had become central themes in the search forexplanation of the historical pattern of metazoan diversity.At approximately the same time, the century-and-a-half-olddiscipline of animal embryology, which had been excludedfrom the evolutionary ‘‘modern synthesis’’ of the 1940s and1950s (Gilbert et al., 1996), began to undergo a resurgence.Embryologists began to incorporate molecular and genetictechniques into their studies of early developmental events.Discovery of the homeobox genes in Drosophila (Scott andWeiner, 1984; McGinnis et al., 1984) and elucidation of theubiquitous roles of homeobox-containing genes in the estab-lishment of developmental pattern in phylogenetically diversemetazoans (Caenorhabditis elegans, Drosophila, Xenopus, andMus; Wilkins, 2002; Arthur, 2002) led to a revival of interestin the mechanistic basis of evolutionary diversification. By themid-1980s, molecular biologists, embryologists, comparativemorphologists, and paleontologists shared a common vision1Manuscript received 27 April 2004; revision accepted 22 June 2004.The authors thank Pamela Diggle, Joseph Williams, Jennifer Winther, Jon-athan Krieger, and Devin O’Connor for helpful discussions. The authors alsothank three reviewers, Mark Chase, Michael Frolich and one anonymous re-viewer, for their helpful comments and suggestions. This work was funded inpart by grants from NSF to W.E.F. and M.D.P.4These authors contributed equally to the paper.5E-mail: [email protected] goal: the complete explanation of the evolutionary historyof developmental modifications that have given rise to the di-versity of extant (and extinct) metazoans.The study of the evolution of development was initiallydriven by studies of animal systems. However, it remains un-clear to what extent the results from animal systems can begeneralized to plants. Plants and animals each evolved inde-pendently from unicellular ancestors. For this reason alone, itseems likely that many, if not most, of the specific moleculardevelopmental mechanisms underlying the evolution of mul-ticellularity and structural complexity in these two majorgroups of complex eukaryotes will differ in significant ways(Kaplan and Hagemann, 1991; Meyerowitz, 2002). Thus, theprinciples that have been elucidated in the study of animalevolutionary developmental biology may have limited explan-atory powers in the realm of plant diversification.The resurgence in the study of the evolution of plant de-velopment in recent years has been accelerated, in part, byrecent successes in elucidating the molecular genetic basis ofplant developmental processes, including the isolation andcharacterization of genes that underlie flower, leaf, and rootdevelopment (see also reviews by Cronk, 2001; Shepard andPurugganan, 2002; Kellogg, 2004). For example, the identifi-cation of the role of MADS-box transcription factor genes inflower development in several model angiosperm species suchas Arabidopsis thaliana, Antirrhinum majus, and Zea maysprovided the basis for early studies on the molecular evolutionof genes that control the development of floral structure aswell as subsequent analyses of these genes in a number ofother nonflowering plant taxa (Purugganan et al., 1995; Theis-sen, 2001; Lawton-Rauh et al., 2000).There remain, however, major gaps in our understanding ofthe evolution of plant development and morphological ho-mology. Progress in the field will have to be driven both bysuccesses and opportunities provided by molecular develop-mental genetic studies, as well as a more robust understandingof plant phylogenetic relationships, and continued analysis ofcomparative plant morphologies of extant and (most impor-tantly) extinct taxa. In this review, we will address basic ques-tions associated with the broad evolutionary developmentalhistory of the bauplan and organs of land plants. We will alsoOctober 2004] 1727FRIEDMAN ET AL.—EVOLUTION OF PLANT DEVELOPMENTFig. 1. Evolution of apical growth. The common ancestor of embryo-phytes and their closest relatives
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