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Major Lineages Within Apiaceae Subfamily Apioideae: a Comparison of Chloroplast Restriction Site and Dna Sequence Data1

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Major Lineages Within Apiaceae Subfamily Apioideae: a Comparison of Chloroplast Restriction Site and Dna Sequence Data1 American Journal of Botany 86(7): 1014±1026. 1999. MAJOR LINEAGES WITHIN APIACEAE SUBFAMILY APIOIDEAE: A COMPARISON OF CHLOROPLAST RESTRICTION SITE AND DNA SEQUENCE DATA1 GREGORY M. PLUNKETT2 AND STEPHEN R. DOWNIE Department of Plant Biology, University of Illinois, Urbana, Illinois 61801 Traditional sources of taxonomic characters in the large and taxonomically complex subfamily Apioideae (Apiaceae) have been confounding and no classi®cation system of the subfamily has been widely accepted. A restriction site analysis of the chloroplast genome from 78 representatives of Apioideae and related groups provided a data matrix of 990 variable characters (750 of which were potentially parsimony-informative). A comparison of these data to that of three recent DNA sequencing studies of Apioideae (based on ITS, rpoCl intron, and matK sequences) shows that the restriction site analysis provides 2.6± 3.6 times more variable characters for a comparable group of taxa. Moreover, levels of divergence appear to be well suited to studies at the subfamilial and tribal levels of Apiaceae. Cladistic and phenetic analyses of the restriction site data yielded trees that are visually congruent to those derived from the other recent molecular studies. On the basis of these comparisons, six lineages and one paraphyletic grade are provisionally recognized as informal groups. These groups can serve as the starting point for future, more intensive studies of the subfamily. Key words: Apiaceae; Apioideae; chloroplast genome; restriction site analysis; Umbelliferae. Apioideae are the largest and best-known subfamily of tem, and biochemical characters exhibit similarly con- Apiaceae (5 Umbelliferae) and include many familiar ed- founding parallelisms (e.g., Bell, 1971; Harborne, 1971; ible plants (e.g., carrot, parsnips, parsley, celery, fennel, Nielsen, 1971). dill, coriander/cilantro, anise, cumin), as well as several Fruit morphology and anatomy were traditionally deadly poisons (e.g., poison-hemlock, water-hemlock, viewed as the most promising sources of taxonomic char- fool's-parsley). The subfamily is de®ned by a suite of acters, exhibiting some (but not excessive) variation in easily observed and well-known characters, including features such as fruit shape, the degree and direction of pinnately lobed or divided leaves with sheathing petioles, mericarp compression, modi®cations of the pericarp ribs herbaceous stems with hollow internodes, compound-um- (e.g., wings or spines), and the shape of mericarp com- bellate in¯orescences, ¯owers with pentamerous peri- missural faces. Thus, most traditional classi®cations of anths and androecia, and bicarpellate gynoecia that ma- Apiaceae have relied almost exclusively on fruit charac- ture into schizocarpic fruits with two ribbed mericarps. ters (Koch, 1824; Bentham, 1867; Boissier, 1872; Drude, These characters make ®eld recognition of most umbel- 1897±1898; and Koso-Poljansky, 1916; reviewed in Con- lifers a simple task, but the dif®culty in identifying these stance, 1971; Plunkett, Soltis, and Soltis, 1996b). Al- plants to genus and species is renowned. This contrast though these systems are now widely regarded as arti®- re¯ects a complex history of problems in interpreting the cial (e.g., Mathias, 1971; Theobald, 1971; Cronquist, phylogeny of Apioideae, and consequently in producing 1982; Shneyer et al., 1992; Shneyer, Borschtschenko, and a satisfactory classi®cation system. Much of the dif®culty Pimenov, 1995), the lack of acceptable alternatives has can be attributed to the near uniformity of most ¯oral led most students of the family to employ the system characters coupled with repeated examples of apparent proposed by Drude (1897±1898) a century ago in Die parallelisms among other features. Leaf-shape changes NatuÈrlichen P¯anzenfamilian (Table 1). Present-day provide a good illustration of such variation. Many gen- modi®cations of this system (e.g., Heywood, 1993; Pi- era, for example, exhibit interspeci®c transitions from menov and Leonov, 1993) all retain Drude's basic divi- pinnately lobed or divided leaves with broad lea¯ets at sion of Apiaceae into three subfamilies: Hydrocotylo- one extreme to decompound leaves with linear or ®liform ideae, Saniculoideae, and Apioideae. Hydrocotyloideae lea¯ets at the other extreme (e.g., Ammi, Apium, Ligus- and Saniculoideae are much smaller subfamilies (42 gen- ticum, Lomatium, Seseli, and Tauschia, among many oth- era with ;470 species, and nine genera with ;300 spe- ers); in some cases the lea¯ets are lost altogether (as in the ``rachis-leaf'' species of Oenanthe, Oxypolis, and cies, respectively; cf. 250±400 genera with 1800±3000 Ptilimnium). Many other morphological, breeding-sys- species in Apioideae), and although some questions re- garding the relationship of Saniculoideae and Hydroco- 1 Manuscript received 8 June 1998; revision accepted 13 November tyloideae to the apioids persist, recent studies (e.g., 1998. Downie et al., 1998; Plunkett, Soltis, and Soltis, 1996b, The authors thank L. Constance, J. Lahham, B. Lee, J. Lyons-Weiler, 1997) suggest that subfamily Apioideae is monophyletic and many botanical gardens (cited in the text) for kindly providing leaf and that phylogenetic problems in this subfamily can be and/or seed material; and V. Houpis, R. Patel, C. Germann, and M. treated as distinct. Burke for assistance in the laboratory. This work was supported by a grant from the National Science Foundation (DEB-9407712). Providing robust phylogenetic hypotheses is a crucial 2 Author for correspondence, current address: Department of Biology precursor to erecting stable classi®cation systems. This Virginia Commonwealth University, Richmond, VA 23284-2012. goal is especially important for Apioideae, which has 1014 July 1999] PLUNKETT AND DOWNIEÐMAJOR LINEAGES IN APIOIDEAE 1015 TABLE 1. The subfamilial classi®cation of Apiaceae according to Drude (1897±1898; see also Heywood, 1993); the eight tribes of subfamily Apioideae and the two subtribes of Scandiceae are also provided. Vittae and companion canals are schizogenous oil ducts found in apiaceous fruits (companion canals are associated with vascular bundles; vittae are located between vascular bundles). HydrocotyloideaeÐendocarp scleri®ed; fruit lacking free carpophore; companion canals present but vittae lacking. SaniculoideaeÐendocarp parenchymatous, but containing scattered druses; exocarp bearing scales, prickles, or barbs (rarely smooth); stylopodi- um ring-like; oil canals or cells variable. ApioideaeÐendocarp parenchymatous (fruit sometimes hardened by a woody subepidermal layer); styles emerging from the apex of the stylopo- dium; vittae and companion cells present. EchinophoreaeÐumbellets with one to a few sessile female ¯owers enclosed by a crown of male ¯owers; fruits mostly with a single seed. ScandiceaeÐdruse crystals in the parenchyma surrounding the carpophore; seeds curved ScandicinaeÐfruit long-cylindrical and beaked, smooth or with short-prickles CaucalidinaeÐfruit ovoid, strongly bristled over the vallecular ribs. CoriandreaeÐfruit spherical, with scleri®ed subepidermal layers; parenchyma surrounding the carpophore lacking druse crystals; seeds curved. SmyrnieaeÐfruit ovoid, mericarps rounded outward; seeds curved. Apieae (5Ammineae)Ðfruits terete; lateral and dorsal ribs all alike; seeds straight. PeucedaneaeÐlateral ribs much broader than dorsal ribs, often forming wings; seeds straight; fruits dorsally compressed. LaserpitieaeÐsecondary ribs present (in addition to primary ribs), often forming wings. DauceaeÐsecondary ribs present (in addition to primary ribs), armed with spines or prickles. served as an important system in many evolutionary stud- these studies are that subfamily Hydrocotyloideae ap- ies. Most notable among these have been the studies of pears to be polyphyletic, but Apioideae and Saniculo- interactions between umbelliferous host plants and their ideae form monophyletic sister groups. These studies do various insect herbivores (especially the lepidopteran spe- not, however, support any tribal system of the family, cies in the genera Papilio, Depressaria, and Greya; re- particularly within Apioideae. As a complement to the viewed in Berenbaum, 1983, 1986, 1990; Thompson, recent sequencing studies, we undertook an analysis of 1986, 1994). To the extent that taxonomy in Apioideae restriction site data derived from the chloroplast genome is widely held to be inadequate, especially at tribal and of 79 species, with a particular emphasis on subfamily generic levels, the absence of a phylogenetic context Apioideae. Despite certain limitations, restriction site among and within umbellifer groups greatly hampers the data confer a number of advantages over sequence data, ability to interpret coevolutionary patterns (see Thomp- the most important being that a nearly random sample of son, 1986). Studies of mating systems provide another the entire chloroplast genome can be surveyed, including example where Apioideae have been used as a ``model data from both rapidly and more slowly evolving se- system.'' Despite frequent descriptions of the subfamily quences (Olmstead and Palmer, 1994). Phylogenetic hy- as being bisexual (e.g., Cronquist, 1981), many taxa are potheses based on restriction site data can be examined andromonoecious (Bell, 1971; Lovett Doust, 1980; Lov- for areas of congruence and/or con¯ict with other data ett Doust and Harper, 1980; Webb, 1981,1984). It is often sets in the effort to recognize strongly supported evolu- assumed that andromonoecy is a
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