Aliso: A Journal of Systematic and Evolutionary Botany Volume 14 | Issue 4 Article 6 1995 Does the Monocot Mode of Leaf Development Characterize all Monocots? Geeta Bharathan University of California, Davis Follow this and additional works at: http://scholarship.claremont.edu/aliso Part of the Botany Commons Recommended Citation Bharathan, Geeta (1995) "Does the Monocot Mode of Leaf Development Characterize all Monocots?," Aliso: A Journal of Systematic and Evolutionary Botany: Vol. 14: Iss. 4, Article 6. Available at: http://scholarship.claremont.edu/aliso/vol14/iss4/6 Aliso, 14(4}, pp. 271-279 © 1996, by The Rancho Santa Ana Botanic Garden, Claremont, CA 91711-3157 DOES THE MONOCOT MODE OF LEAF DEVELOPMENT CHARACTERIZE ALL MONOCOTS? GEETA BHARATHAN Agronomy and Range Science University of California Davis, California 95616 FAX: 916/152-4361 e-mail: grbharathan@ ucdavis. edu ABSTRACT Patterns of early leaf development in monocots are analyzed in a phylogenetic context. Recent developmental and phylogenetic studies enable this reevaluation of the leaf base model of the devel­ oping monocot leaf. Two questions are addressed: a) is the presence of the Vorlauferspitze (fore-runner tip) invariably correlated with development of the lamina from the lower leaf zone? and b) was the ancestral monocot characterized by the leaf base mode of development? Scanning electron microscopic observations are made of young primorida using the mold and cast method. These data are combined with data from the literature and examined in a phylogenetic context using parsimony analysis. The results suggest that in some taxa the Vorlauferspitze may be associated with a lamina that is derived from the upper leaf zone, and that the ancestral monocot may not have been characterized by the leaf­ base mode of development. It is concluded that the leaf-base model, in a strict sense, may apply to a nested subset, but not all, of the monocotyledons. Key words: development, evolution, leaf, leaf-base model, monocotyledons, morphology, phylogeny, Vorlauferspitze. INTRODUCTION within the monocots that needed to be further studied in order to apply the model more generally. A key question in the study of monocot leaf mor­ The conclusion that the laminae in monocots and phology has been whether the linear parallel-veined dicots are not homologous, based on a "biological" lamina of the monocot leaf is homologous to the broad concept of homology (e.g., Roth 1988; Wagner 1989), reticulate-veined leaf of the dicot leaf. Early anatom­ was transferred to the evolutionary realm and taken to ical and morphological studies suggested that the also imply "historical" (taxic) nonhomology (e.g., monocot blade is a bifacially flattened dicot petiole Dahlgren and Clifford 1983; Donoghue and Doyle, (Arber 1918). Developmental studies revealed differ­ 1989). However, the original generalization was based ences in the origin of the lamina in the two classes on developmental studies of evolutionarily disparate and led to the "leaf base" model of development for taxa. Given this data base it is not clear that the "bi­ the monocot leaf (Troll 1939; Knoll 1948; Kaplan ological" concept can be legitimately converted to the 1970, 1973). Dicots and monocots differ in the origin "historical" concept without making major assump­ of the lamina, which develops from the upper leaf zone tions. One such assumption is that the ancestral mono­ in dicots and from the lower leaf zone in monocots cot had the leaf base mode of development. (Fig. 1). It was shown that the lamina of so-called Two sets of factors suggest that the time is now ripe unifacial leaves of monocots develops from the lower for a reevaluation of this model. First, observations on leaf zone, as do the laminae of linear leaves, e.g., San­ leaf development have been extended into other sevieria, and broad leaves, e.g., Hosta. Both linear and groups such as the Alismatales (Bloedel and Hirsch broad leaves were associated with a unifacial structure 1979), Araceae (Periasamy and Muruganathan 1986), at the tip, the Vorlliuferspitze, that was used as a di­ and Cyclanthales (Wilder 1976). These studies reveal agnostic feature for the leaf base mode of develop­ a range of variation in the origin of the lamina, as ment. Since the Vorlliuferspitze occurs in several mon­ suspected by Kaplan (1973). Second, our understand­ ocots it was suggested that the lamina in most mono­ ing of monocot relationships has improved in recent cots is derived from the lower zone and is therefore years (Bharathan 1993; Duvall et al. 1993 a, b; Bhar­ not homologous to the lamina of dicots (Kaplan 1973). athan and Zimmer 1995; Stevenson and Loconte 1995; The assumption was that the Vorlliuferspitze is invari­ Chase et al. 1995a, b). These phylogenetic studies re­ ably associated with a lamina that develops from the veal taxa that should be included in an evolutionary lower leaf zone. At the same time, Kaplan noted that study of leaf development, particularly dicot outgroups there exists a wide range of morphological variation such as the Piperales, Aristolochiales and Nymphae- 272 ALISO Dicotyledons Monocotyledons vated, plants were mature and the shoots sampled were producing adult leaves. It is assumed that the early stages of development observed here are stages in de­ velopment of adult leaves. Shoots were dissected un­ (al/:'/0 • ~ der water using a binocular research microscope (Zeiss - / (b10 STEMI V8). unifacial ./ A Mold and cast technique.-Molds were made using {~)~ dental vinyl silicone and casts using epoxy resin (Wil­ linear- liams, Vesk and Mullins 1987; Williams and Green (Alli!im) 0 (d) a (c)t • 1988; Jernstedt et al. 1992). Impressions were made Leaf zones in cross section Upper, unifacial 0 Q of successive primordia on the same shoot. Observa­ bifacia:- • Upper, bifacial a (Sagittaria, bifacial tion of primordial stages at plastrochrons one to three Lower, bifacial • Carludovica) (J::!Qili.) (p1-p3) provided the necessary information in most Fig 1. Morphological model of leaf development in monocoty­ cases. Primordial stages of up to p7 were studied in ledons. Early primordia consist of an unifacial upper zone (white) taxa such as the Dioscorea spp. and Lapageria roseus and a bifacial lower zone (stippled). In dicotyledons the upper zone in order to determine the origin of the lamina. differentiates into a lamina, the lower zone differentiates into the leaf base and stipules, and the petiole is intercalated later. In mon­ Scanning electron microscopy (SEM).-The casts ob­ ocots a greater variety of developmental patterns is seen. According tained were mounted on stubs, sputter coated with to early formulations of the model (a~) the upper zone differenti­ gold, observed with a scanning electron microscope ated into unifacial laminae and the lower zone differentiated into bifacial laminae. Later formulations also included bifacial forms de­ (SEM, Hitachi 450), and digital images captured and rived from the upper zone (d). stored using the software package SEMICAPS. Phylogenetic hypotheses.-Topologies used in this study were based on recent morphological and molec­ ales and putative early lineages such as the Dioscore­ ular studies (Bharathan 1993; Duvall et al. 1993a, b; ales that have not so far featured in the discussion. Bharathan and Zimmer 1995; Chase et al. 1995a, b). In this paper I examine two assumptions of the leaf The topologies were pruned to either eliminate taxa base model of leaf development alluded to above, pos­ for which developmental data are not available, or to ing them as two questions: accommodate differences in taxon sampling among 1) Is the Vorlliuferspitze invariably correlated with different phylogenetic studies. Analyses using the development of the lamina from the lower leaf zone? rbcL topology were done with and without the Cy­ 2) Was the lamina of the ancestral monocot derived clanthaceae. The general pattern in all the phylogenetic from the lower leaf zone? studies (barring the studies of Chase et al., which had no bootstrap analyses) is one of relatively poor boot­ MATERIALS AND METHODS strap support for deeper branches and strong support Plant Materials for nested clades in these studies. The differences be­ tween the morphological and molecular data lie largely Young shoot apices were obtained from plants in the rooting. The exemplar topologies used here may growing in the greenhouses of the University of Cal­ serve to take into account weakly supported branches ifornia at Davis. The species sampled were Aristolo­ in the different studies. chia fimbriata Cham. (B90.073); A. labiata Willd. Character reconstruction.-Features of leaf primordia (B82.152); Butomus umbellatus L. (GB127, UA Her­ were encoded as binary traits. Parsimony reconstruc­ barium); Calathea lietzii E. Morr. (B88.033); Cryptan­ tion of these traits was done on topologies of monocot thus sp. (B90.051); Dioscorea discolor Kunth. relationships obtained from above using MacClade 3.0 (B93.330); Dioscorea sp. (B00.069); Gloriosa superba (Maddison and Maddison 1992). Points of agreement L. (B63.339); Lapageria rosea Ruiz and Pav. between all reconstructions (including differences be­ (B63.11 ); Philodendron variifolium Schott (B81.603); tween topologies and alternative reconstructions on a Piper crocatum Ruix and Pav. (B89.235); P. nigrum single topology) provided the basis for conservative L. (B74.003); P. hispidum H. B. and K. (B00.604); conclusions regarding ancestral states. These conclu­ Scindapsus pictus (B00.763). Specimens of all except sions were used to infer trends in character evolution. Butomus umbellatus have been deposited at either the John Tucker Herbarium, University of California, Da­ RESULTS AND DISCUSSION vis, or the herbarium at the University of Arizona, Tuc­ son. Numbers in parentheses are accession numbers of Variation in Development the Botany Collections Greenhouse. Except for Scin­ There was a wide range of variation in early stages dapsus pictus, whose juvenile stage is the one culti- of primordial development (Figs. 2-9). Development VOLUME 14, NUMBER 4 273 Fig.