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Chloroplast Dna Systematics of Lilioid Monocots: Resources, Feasibility, and an Example from the Orchidaceaei

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Chloroplast Dna Systematics of Lilioid Monocots: Resources, Feasibility, and an Example from the Orchidaceaei Amer. J. Bot. 76(12): 1720-1730. 1989. CHLOROPLAST DNA SYSTEMATICS OF LILIOID MONOCOTS: RESOURCES, FEASIBILITY, AND AN EXAMPLE FROM THE ORCHIDACEAEI MARK W. CHASE2 AND JEFFREY D. PALMER3 Department of Biology, University of Michigan, Ann Arbor, Michigan 48109-1048 ABSTRACT Although chloroplast DNA (cpDNA) analysis has been widely and successfully applied to systematic and evolutionary problems in a wide variety of dicots, its use in monocots has thus far been limited to the Poaceae. The cpDNAs ofgrasses are significantly altered in arrangement relative to the genomes of most vascular plants, and thus the available clone banks ofgrasses are not particularly useful in studying variation in the cpDNA ofother monocots. In this report, we present mapping studies demonstrating that cpDNAs offour lilioid monocots (Allium cepa, Alliaceae; Asparagus sprengeri, Asparagaceae; Narcissus x hybridus, Amaryllidaceae; and On­ cidium excavatum, Orchidaceae), which, while varying in size over as much as 18 kilobase pairs, conform to the genome arrangement typical of most vascular plants. A nearly complete (99.2%) clone bank was constructed from restriction fragments of the chloroplast genome of Oncidium excavatum; this bank should be useful in cpDNA analysis among the monocots and is available upon request. As an example of the utility of filter hybridization using this clone bank to detect systematically useful variation, we present a Wagner parsimony analysis of restriction site data from the controversial genus Trichocentrum and several sections of Oncid­ ium, popularly known as the "mule ear" and "rat tail oncidiums." Because of their vastly different floral morphology, the species of Trichocentrum have never been placed in Oncidium, although several authors have recently suggested a close relationship to this vegetatively modified group. The analysis of cpDNA presented here supports this affinity; in fact, it places Tricho­ centrum as a derivative of the mule ear oncidiums. AMONG THE meers, systematic studies ofchlo­ least three large inversions (Palmer, 1985; roplast DNA (cpDNA) variation are relatively Howe et aI., 1988). Clone banks constructed common and have been applied to a wide va­ from these highly rearranged genomes are of riety ofspecies at several taxonomic levels (see limited use in mapping studies of other vas­ review in Palmer et aI., 1988a). As is true of cular plants, and th us far the sources ofcpDNA systematic studies ofmonocots in general, the probes in filter hybridizations have been lim­ principal focus of molecular studies in the ited to those ofdicots, such as spinach, petunia, monocots has been the Poaceae (Tsunewaki and tobacco, that have the consensus arrange­ and Ogihara, 1983; Enomoto, Ogihara, and ment for flowering plants. The chloroplast ge­ Tsunewaki, 1985; Doebley, Renfroe, and Blan­ nomeofSpirodela oligorhiza (Araceae) has been ton, 1987; Lehvaslaiho, Saura, and Lokki, 1987; mapped (de Heij et aI., 1983) and was found Hilu, 1988). The chloroplast genome in the to be colinearwith theconsensus vascular plant grasses differs significantly from those found arrangement, although it was 30 kilo base pairs thus far in the dicots in the possession of at (kb) larger than that of Petunia. In this study we focused on four lilioid monocots: Allium cepa (Alliaceae), Asparagus I Received for publication 20 January 1989; revision sprengeri(Asparagaceae), Narcissus x hybridus accepted 25 May 1989. (Amaryllidaceae), and Oncidium excavatum We wish to acknowledge the support of a National Sci­ ence Foundation Fellowship in Environmental Biology, (Orchidaceae). Physical and gene mapping BSR-8600179, to MWC. We are also grateful for permis­ studies reveal that, unlike the grasses, the ge­ sion to remove leaves and flowers from the orchid collec­ nome arrangement ofthese monocots is typical tions ofAlexis and Ted Linder (Great Lakes Orchids) and of that of most land plants. Ron Cnesinski (Taylor Orchids). Requests for the orchid cpDNA clone bank described here should be directed to Furthermore, we have constructed a clone MWC. We are grateful to William F. Thompson for pro­ bank of restriction fragments of one of these viding laboratory facilities for the portion of the work species, Oncidium excavatum and have used performed in 1982-1983. this bank in filter hybridizations to discover 2 Current address: Department of Biology, University of North Carolina, Chapel Hill, NC 27599-3280. systematically useful variation in the cpDNA 3 Current address: Department ofBiology, Indiana Uni­ of other orchids. As an example of the utility versity, Bloomington, IN 47405. of this approach in gathering useful new in- 1720 December 1989] CHASE AND PALMER-DNA SYSTEMATICS OF MONOCOTS 1721 TABLE I. Sources of DNA from species in the Oncidiinae (vouchered by jlowers in FAA in the first author's private collection) Species Origin- Voucher number I. Oncidium excavatum Cajamarca, Peru (GLO) 83427 2. Rossioglossum schlieperianum Chiriqui, Panama (GLO) 83449 3. Oncidium ampliatum Chiriqui, Panama (MWC) 84104 4. Psychopsis sanderae Peru (TO) 86126 5. Oncidium jonesianum Paraguay (TO) 86118 6. Oncidium ascendens Chiapas, Mexico (MWC) 82109 7. Oncidium flavovirens Colima, Mexico (MWC) 83109 8. Oncidium splendidum Guatemala (UMBG) 84552 9. Oncidium bicallosum Chiapas, Mexico (MWC) 83387 10. Trichocentrum panduratum Peru (TO) 86179 II. Trichocentrum tigrinurn Peru (RO) 83439 12. Oncidium pulvinatum Brazil (GLO) 82228 13. Oncidium hians Brazil (SBOE) 86134 a GLO = Great Lakes Orchids; MWC = Mark W. Chase, field collected; TO = Taylor Orchids; UMBG = Matthaei Botanical Garden, University of Michigan; RO = R. J. Rands Orchids; SBOE = Santa Barbara Orchid Estate. formation that differentiates opposing hypoth­ Sources of material ofeach orchid species are eses about phylogenetic relationships, we pre­ listed in Table 1. All DNAs were further pu­ sent an analysis ofcpDNA variation among a rified by means of cesium chloride-ethidium controversial group oforchids. Some members bromide gradients. ofthe oncidioid orchids (subtribe Oncidiinae) Restriction endonuclease digests, electro­ display a series of vegetative modifications phoresis, transfer to nylon filters, labelling of (succulence) that have earned for them the recombinant plasmids, filter hybridizations, common names of "mule ear" and "rat tail and autoradiography were carried out accord­ oncidiums." Members ofthe genus Trichocen­ ing to Palmer (1986). Washing ofthe filters was trum also exhibit the "mule ear" condition but done under the following conditions: two have a floral morphology that is radically dif­ washes of 15 minutes at room temperature, ferent from any species on Oncidium. Dressler followed by two washes for 30-60 min at 65 and Williams (1982) suggested that Trichocen­ C, with a 2 x SSC, 0.5% SDS wash buffer. After trum is closely related to these vegetatively a round of hybridization, the probes were modified oncidiums. Others (Wirth, 1964; stripped from the filters by 3-4 washes ofboi1­ Chase, 1986) viewed the exceptionally dis­ ing 0.1 x SSe. These filters (Zetabind, AMF tinctive floral morphology of Trichocentrum Cuno) went through over 30 rounds of hy­ as support for a view that the similar vegetative bridizations and were still in usable condition. features are due to parallelism. A series ofother A restriction site map for 6 enzymes was members of Oncidium have less extreme veg­ constructed for O. excavatum (Fig. 1) using the etative features that also suggest a relationship mapping strategy ofPalmer(1986). The cpDNA to the mule eargroup. We examined restriction probes for this mapping were the clone bank site variation in cpDNA, as detected by filter of Lactuca sativa (Jansen and Palmer, 1987). hybridization, among these species in order to For the region in which L. sativa has a 22 kb test the conflicting ideas of their phylogenetic inversion, we substituted the three uninverted relationships. Petunia x hybrida clones (Palmer et aI., 1983). Once this restriction fragment map was com­ MATERIALS AND METHODS-CpDNAs ofAl­ pleted, gene probes from tobacco, spinach, and lium cepa, Asparagus sprengeri, Narcissus pea were hybridized to the same filters to iden­ x hybridus and Oncidium excavatum were iso­ tify their locations in this genome (for probe lated by the sucrose gradient technique (Palm­ descriptions, see Jansen and Palmer, 1987). er, 1986). For all other taxa, total cellular DNAs The representatives of three other lilioid were isolated by the modified CTAB method monocots, Allium cepa, Asparagus sprengeri, ofDoyle and Doyle (1987). Most ofthe mem­ and Narcissus x hybridus, were mapped for two bers of the mule ear oncidium group are suc­ restriction enzymes, Pvull and Sad, using the culent, and the standard method of isolation cloned genome of Vigna radiata (mung bean; of total cellular DNA did not work well or at Palmer and Thompson, 1981) as the source of all. This problem was remedied by using a 3 x cpDNA probes. (At the time this mapping was CTAB buffer rather than the standard 2 x . performed, more appropriate clone banks [i.e., --.J ..-- 4 4 N ", N N-NN... ... ... -< : UU... - '" r;; ... ... '" ... ... ~ ~~:. o 0 ..e A. A. 0."1. '0 '0 . - ...~ ... ; ... - ~ '" '" '" ~ . 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