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Specialized Structures in the Leaf Epidermis of Basal Angiosperms: Morphology, Distribution, and Homology1

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Specialized Structures in the Leaf Epidermis of Basal Angiosperms: Morphology, Distribution, and Homology1 American Journal of Botany 93(5): 665–681. 2006. SPECIALIZED STRUCTURES IN THE LEAF EPIDERMIS OF BASAL ANGIOSPERMS: MORPHOLOGY, DISTRIBUTION, AND HOMOLOGY1 KEVIN J. CARPENTER2 Canadian Institute for Advanced Research, Botany Department, University of British Columbia, 3529-6270 University Boulevard, Vancouver, British Columbia V6T 1Z4 Canada The morphology of specialized structures in the leaf epidermis of 32 species of basal (ANITA: Amborella, Nymphaeales, Illiciales, Trimeniaceae, and Austrobaileyaceae) angiosperms, representing all seven families and 11 of 14 genera, was investigated using light and scanning electron microscopy. Distribution, density, and size of structures were also measured, and character evolution was analyzed. Hydropotes are a synapomorphy of Nymphaeales and ethereal oil cells are a synapomorphy of Austrobaileyales, but uniseriate nonglandular trichomes appear to have arisen independently several times. Specialized structures are frequently characterized by adjacent epidermal cells that have striking similarities in their form and arrangement (i.e., architecture) to subsidiary cells of certain types of stomatal complexes. Additionally, forms intermediate to oil cells and stomata, to trichomes and stomata, and to hydropotes and oil cells are present in some taxa. Thus, all of these specialized structures and their adjacent epidermal cells form complexes that may be homologous with, and evolutionarily derived from stomatal complexes, and the specialized structure, or portion thereof, may be homologous to the stoma or guard mother cell. Improved knowledge of the morphology and evolution of these structures in the earliest branching extant angiosperm lineages has a bearing on many diverse areas of botany. Key words: Amborellaceae, Austrobaileyales, evolution, hydropotes, leaf epidermal anatomy, Nymphaeales, oil cells, trichomes. Since 1999 and 2000, when several large-scale phylogenetic completed a comparative survey of stomatal architecture across analyses (e.g., Mathews and Donoghue, 1999; Qiu et al., 1999, all ANITA-grade families and Chloranthaceae (Carpenter, 2000; Graham and Olmstead, 2000) placed Amborella 2005). However, the morphology, distribution, and evolution trichopoda Baill., Nymphaeales, and Austrobaileyales at the of other specialized structures in the leaf epidermis of these base of the extant angiosperm phylogenetic tree, the renewed plants (e.g., trichomes, ethereal oil cells, and hydropotes— interest in these groups resulted in numerous studies of various specialized trichome-like structures in Nymphaeales) have aspects of their biology (e.g., Endress and Igersheim, 2000; been little examined or discussed. Carlquist and Schneider, 2001, 2002; Bernhardt et al., 2003; Because plants communicate with their external environment Feild et al., 2004; Carpenter, 2005). One aspect of ANITA and protect and maintain essential internal physiological and (acronym of the families and orders within the first three biochemical processes through such specialized epidermal clades: Amborella, Nymphaeales, Illiciales, Trimeniaceae, and structures, information on their morphology and evolution has Austrobaileyaceae) angiosperms that has attracted relatively bearing on a wide variety of issues. Aside from their proven little attention is leaf epidermal anatomy. Carlquist (2001) and value in the systematics and taxonomy of extant and fossil Baranova (2004) presented brief treatments of Austrobaileya plants (e.g., Stace, 1965; Upchurch, 1984; Baranova, 1992a), scandens C. T. White, and Amborella trichopoda was specialized epidermal structures represent adaptations to a wide summarized by Carlquist and Schneider (2001). I recently range of ecologies (cf. hydropotes and stomatodes of aquatic plants as in Kaul [1976] and Wilkinson [1979], and trichomes 1 Manuscript received 4 August 2005; revision accepted 20 February 2006. in xerophytic plants as in Ehleringer and Clark [1987]) and are The author thanks G. Vermeij for guidance during the course of this of practical interest in agriculture because of their influence on project and for critical review of the manuscript; D. Potter and J. Jernstedt the uptake of pesticides and fertilizers and their role in host– for the same, as well as for the use of laboratory and photomicroscope parasite interactions (e.g., Harr et al., 1991; Harr and facilities, respectively; G. Upchurch for instruction on specimen Guggenheim, 1995). Recent workers interested in the preparation; and D. Canington, B. Ertter, H. Gang, R. Harris, J. Henrich, molecular basis of plant development have been attracted to D. Lorence, C. Prychid, M. Romanova, P. Romanov, P. Rudall, R. Saunders, and the following institutions for material and other assistance: the leaf epidermis and its specialized structures such as Conservatory of Flowers (San Francisco, California, USA); Royal Botanic trichomes, as a system offering many advantages and Gardens: the Jodrell Laboratory and Micromorphology group (Kew, UK); interesting questions for study (e.g., Ramsay and Glover, National Tropical Botanical Garden (McBryde, Kalaheo, Hawaii, USA); 2005). South China Botanic Garden and IBSC (Guangzhou, China); University of The potential importance of specialized leaf epidermal California: Berkeley Botanic Gardens, UC, DAV, Davis Botanical structures in ANITA angiosperms in particular has been Conservatory, and Santa Cruz Arboretum; and HKU. Research was suggested by the few studies on such structures in these taxa supported by Jastro Shields Graduate Research Grants, the Davis prior to the formation of the ANITA hypothesis in 1999 and Botanical Society, the Center for Biosystematics, and a UCD Dissertation Year Fellowship. This represents a portion of a doctoral dissertation 2000. The presence of ethereal oil cells in leaves and other carried out in the Plant Biology Graduate Group, University of California, organs of Austrobaileya was considered by Bailey and Swamy Davis. (1949) to be a major line of evidence against a relationship with 2 Author for correspondence (e-mail: [email protected], Dilleniaceae. Bailey and Swamy (1948) considered the lack of [email protected]) ethereal oil cells in Amborella to be an important character 665 666 AMERICAN JOURNAL OF BOTANY [Vol. 93 separating it from Monimiaceae. The presence of ethereal oil removed under a dissecting microscope, leaving only the epidermes to be cells in the leaf epidermis in particular, led Baranova (1992a) to mounted. Specimens were examined and photographed with an Olympus BH-2 argue against a relationship between Austrobaileya and light microscope (Tokyo, Japan) and Microfire digital camera (Tokyo, Japan). Leaf samples of Amborellaceae and Austrobaileyales were prepared for Annononaceae, or Myristicaceae, in favor of a relationship scanning electron microscopy by sampling pieces as described. Samples were with Schisandraceae (as supported by Qiu et al., 1999, 2000). placed in 1500-lL plastic reaction tubes, immersed in 100% chloroform, and The increasing diversity of leaf epidermal secretory cells, hair placed in a water bath sonicator for 10 min. to remove epicuticular waxes and bases, and other leaf characters seen through the Early other debris. Samples were then rinsed several times in deionized water, and set Cretaceous, led Upchurch (1984) to conclude that angiosperms to dry overnight on paper towels covered by inverted beakers. Leaf samples of were undergoing a major adaptive radiation at that time. Yet Victoria amazonica were immersed in 10% Tween overnight, rinsed in deionized water, sonicated in chloroform as before, rinsed in deionized water, despite these intriguing findings, these structures have been dehydrated in an ethanol series, and critical point dried in a Tousimis Sam dri- mentioned sporadically, and even less frequently illustrated in 780A critical point dryer (Rockville, Maryland, United States). Samples were the literature on ANITA taxa. Some authors who mention then mounted onto aluminum stubs with Ted Pella double stick adhesive ethereal oil cells in the leaf mesophyll of a given species or (Redding, California, United States), sputter coated with gold with a Pelco Auto family fail to mention their occurrence in the leaf epidermis, as Sputter Coater SC-7 (Redding, California, United States), and examined and in Metcalfe’s (1987) treatment of Austrobaileya, Philipson’s photographed at 10 kV in a Philips XL30 TMP scanning electron microscope (1993) treatment of Trimeniaceae, and Keng’s (1993) treatment (Eindhoven, Netherlands). of Schisandraceae. With the current strongly supported and widely accepted rooting of the extant angiosperm tree, I believe Character coding—For each sample (i.e., leaf), 20 of each type of specialized structure present on each surface (abaxial and adaxial) were coded that a comparative study of these structures from a large sample for characters enumerated in the Results (Characters) section. While some of representing all ANITA families will yield data of taxonomic these characters have been previously mentioned in the literature (e.g., cuticular and systematic value for studies of living and fossil striations on ethereal oil cells and adjacent epidermal cells; Upchurch, 1984; angiosperms, as well as hypotheses pertaining to many Baranova 1992a), many have not, and I noted additional characters for each questions about their taxonomic distribution, evolution, and type of specialized structure after careful examination of all the taxa included homology. here. Densities of structures on abaxial
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