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Genome Size and Karyotype Evolution in the Slipper Orchids (Cypripedioideae:Orchidaceae)1

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Genome Size and Karyotype Evolution in the Slipper Orchids (Cypripedioideae:Orchidaceae)1 American Journal of Botany 85(5): 681±687. 1998. GENOME SIZE AND KARYOTYPE EVOLUTION IN THE SLIPPER ORCHIDS (CYPRIPEDIOIDEAE:ORCHIDACEAE)1 ANTONY V. C OX,2 GREGORY J. ABDELNOUR,MICHAEL D. BENNETT, AND ILIA J. LEITCH Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3DS, UK Nuclear DNA contents (4C) were estimated by Feulgen microdensitometry in 27 species of slipper orchids. These data and recent information concerning the molecular systematics of Cypripedioideae allow an interesting re-evaluation of karyo- type and genome size variation among slipper orchids in a phylogenetic context. DNA amounts differed 5.7-fold, from 24.4 pg in Phragmipedium longifolium to 138.1 pg in Paphiopedilum wardii. The most derived clades of the conduplicate-leaved slipper orchids have undergone a radical process of genome fragmentation that is most parsimoniously explained by Rob- ertsonian changes involving centric ®ssion. This process seems to have occurred independently of genome size variation. However, it may re¯ect environmental or selective pressures favoring higher numbers of linkage groups in the karyotype. Key words: Cypripedioideae; centric ®ssion; genome size; karyotype evolution; Orchidaceae; phylogeny. Slipper orchids (Cypripedioideae: Orchidaceae) are of genome size data prevented Cox et al. from determin- probably the best characterized of the orchid subfamilies. ing whether the change in chromosome number was ac- Great horticultural importance has contributed signi®- companied by a change in genome size. cantly to prolonged scienti®c interest, not least because To investigate the interrelationship among genome extensive collections have made much material available size, karyotype evolution, and phylogenetic af®nities we for examination. Indeed, studies spanning over 150 years measured nuclear genome sizes for 27 slipper orchid spe- provide a substantial body of information concerning cies sampled from the three largest genera, Phragmipe- their cytology (Karasawa, 1979, 1980, 1986; Karasawa dium, Paphiopedilum, and Cypripedium. The data of Cox and Tanaka, 1980, 1981; Karasawa and Saito, 1982; At- et al. (1997) were used to place genome size and karyo- wood, 1984; Karasawa and Aoyama, 1986, 1988), mor- type data in a phylogenetic context and to suggest mech- phology (Rosso, 1966; Atwood, 1984), taxonomy (Rei- anisms and directionality of change. chenbach, 1854; Rolfe, 1896; Atwood, 1984; Albert and Pettersson, 1994), molecular systematics (Albert and MATERIALS AND METHODS Chase, 1992; Cox et al., 1997), and pollination biology (Dodson, 1966; Vogt, 1990; BaÈnziger, 1994, 1996; Chris- Plant materialÐRoot tips for chromosome counts and DNA mea- surements were taken from the orchid collection at the Royal Botanic tensen, 1994). Gardens, Kew. Plant accession numbers, vouchers, and karyotypic com- Detailed taxonomic studies have been made of the positions are presented in Table 1. The recent molecular phylogeny of three major genera, Cypripedium (Cox, 1995; Cribb, in Cox et al. (in press) was used to assist sampling. All sections in genus press), Paphiopedilum (Cribb, 1987), and Phragmipe- Phragmipedium and Paphiopedilum (except section Pardalopetalum) dium (Garay, 1979; McCook, 1989). The two remaining were represented in the study, but reduced sampling in Cypripedium genera, Selenipedium and monotypic Mexipedium, are occurred due to lack of living material. Living material of Mexipedium poorly known, owing to their rarity in nature and, in the and Selenipedium was unavailable for study. case of the former, great dif®culty in maintaining plants in cultivation. Chromosome countsÐActively growing root tips were collected and Extensive chromosome data are available for slipper pretreated with 0.002 mol/L 8-hydroxyquinoline for 4±5 h at 188C (Kar- orchids. Chromosome counts are published for almost all asawa, 1979) prior to ®xing in freshly prepared 3:1 (v/v) absolute eth- species of Paphiopedilum and Phragmipedium and many anol/glacial acetic acid at 48C for a minimum of 1 h. Root tips were of Cypripedium; detailed karyotypes are available for transferred to 45% acetic acid for 5 min at 48C, hydrolyzed in 1 mol/ most species of the former two genera. Recently, parsi- L HCl at 608C for 15 s (Karasawa, 1979), and stained in the dark with mony analysis of nuclear ribosomal internal transcribed Feulgen solution for a minimum of 30 min and a maximum of 24 h at spacer (ITS) sequence data from nearly 100 slipper or- 48C. The preparation was then squashed under a coverslip in 2% aceto- chids elucidated the phylogeny of slipper orchids (Cox orcein for cytological analysis. et al., 1997). A survey of the karyotype data in the con- DNA measurementsÐThree root tips of each species of slipper or- text of the phylogenetic tree revealed a general trend to- chid and the calibration standard Allium cepa cv. ``Ailsa Craig'' (4C 5 ward increased chromosome number. However, paucity 67.1 pg; Bennett and Smith, 1976) were collected on the same day and ®xed in freshly prepared 3:1 (v/v) absolute ethanol/glacial acetic acid for a minimum of 24 h at 48C before hydrolysis in 5 mol/L HCl at 258C 1 Manuscript received 28 May 1997; revision accepted 12 September 1997. for 40 min. Root tips were then rinsed in distilled water, stained in The authors thank Lynda Hanson for valuable technical assistance pararosanoline solution for 2 h at 248C, washed in three aliquots of and Mark Chase and Keith Jones for helpful discussions. Sandra Bell SO2-water for 10 min each, transferred to distilled water, and stored in kindly provided root tips of slipper orchids. the dark at 48C for up to 24 h. Finally, the roots were squashed in 45% 2 Author for correspondence ([email protected]). acetic acid. Readings of ten prophase (4C) nuclei on each of three slides 681 682 AMERICAN JOURNAL OF BOTANY [Vol. 85 TABLE 1. Plant material used in this study: accession number, chromosome number, and genome size.a Cytology reference Chromosome Mean 4C DNA Taxon Accession number number numberb amount (pg) Paphiopedilum Sect. Barbata P. appletonianum (Gower) Rolfe 1981-1534 96-61 38(24) 129.7 P. wardii Summerh. 1990-266 96-66 41(29) 138.1 P. callosum (Rchb.f.) Stein 1990-3253 96-155 32(12) 96.2 P. purpuratum (Lindl.) Stein 1988-2124 96-158 40(28) 108.5 P. barbatum (Lindl.) P®tzer 1990-252 96-62 38(24) 135.0 P. tonsum (Rchb.f.) P®tzer 1988-3165 96-67 32(12) 112.6 M. mastersianum (Rchb.f) Stein 1993-522 96-63 36(20) 118.9 P. sukhukulii Schoser & Senghas 1990-265 96-65 40(28) 118.9 P. urbanianum Fowlie TP4 2653 96-87 40 Ð Sect. Coryopedilum P. philippinense (Rchb.f.) Stein 1990-198 96-107 26 93.0 P. rothschildianum (Rchb.f.) Stein 1986-2479 96-108 26 90.3 P. glanduliferum (Blume) Stein 1953-38501 96-159 26 94.9 P. dianthum T. Tang & F. T. Wang 23-10-90 GREL 96-85 26 Ð Sect. Paphiopedilum P. insigne (Wall. ex Lindl.) P®tzer Ð Ð 26 92.1c P. druryi (Bedd.) Stein 1976-952 96-74 30(8) 106.5 P. gratrixianum (Masters) Guill. 1979-0975 96-160 26d 100.0 P. villosum (Lindl.) Stein Ð Ð 26 89.9e Sect. Cochlopetalum P. primulinum M. Wood & Taylor 1981-1628 95-156 32(14) 83.6 P. victoria-mariae (Rolfe) Rolfe 1988-3173 96-84 36 85.6 Sect. Brachypetalum P. concolor (Lindl.) P®tzer 1988-1641 96-76 26 77.9 P. godefroyae (Godefr.-Lebeuf) Stein 1988-1642 97-77 26 71.2 Sect. Parvisepalum P. micranthum T. Tang & F. T. Wang 1990-195 96-73 26 91.0 P. delenatti Guill. 1989-3408 96-72 26 87.3 Phragmipedium Sect. Phragmipedium P. caudatum (Lindl.) Rolfe 1986-2307 96-69 28(20) 36.7 Sect. Platypetalum P. lindleyanum (Lindl.) Rolfe 1983-341 96-71 22(10) 32.1 Sect. Lorifolia P. pearcei (Rchb.f.) Rauh & Senghas 1987-4033 96-154 20,21,22 25.3 P. longifolium (Rchb.f. & Wasc.) Rolfe 1976-2035 96-70 21(5) 24.4 Sect. Micropetalum P. besseae Dodson & J. Kuhn 1992-3664 96-83 24 28.3 Cypripedium C. pubescens Willd. 1991-1118 96-103 20 129.5 C. formosanum Hay 1986-684 96-105 20 113.9 C. californicum A. Gray K541 96-106 N/A 86.2 a Dash indicates data not available. b Number of telocentric chromosomes (where known) shown in parentheses. c Cox et al. (1993). d New chromosome record. e Narayan, Parida, and Vij (1989). were made using a Vickers M85 scanning microdensitometer (Vickers, Genome sizeÐThe genome sizes of 27 slipper orchids, UK) and mean values calculated. measured by Feulgen microdensitometry, ranged from 24.4 pg in Phragmipedium longifolium to 138.1 pg in RESULTS Paphiopedilum wardii (Table 1). Table 1 also includes the genome sizes of Paphiopedilum insigne and P. vil- Chromosome numberÐA chromosome count was losum previously reported by Cox et al. (1993) and Na- made for one species of Paphiopedilum not previously rayan, Parida, and Vij (1989), respectively. The 4C DNA determined (P. gratrixianum) and is listed in Table 1. amounts for three Cypripedium species ranged from 86.2 May 1998] COX ET AL.ÐKARYOTYPE EVOLUTION IN SLIPPER ORCHIDS 683 TABLE 2. Range in chromosome number, karyotype structure (where known), nombre fondamental (n.f.; Mathey, 1949), and range of 4C DNA amount. (Chromosome data taken from Karasawa [1979]). Range in 4C DNA Genus Section 2n n.f. amount (pg) Paphiopedilum Barbata 28 to 42 52±54 96.2±138.1 Pardalopetalum 26 52 Ð Coryopedilum 26 52 90.3±94.9 Paphiopedilum 26 (excluding P. druryi 52 89.9±106.5 and P. spicerianum) Cochlopetalum 32±37 50 83.6±85.6 Brachypetalum 26 52 71.2±77.9 Parvisepalum 26 52 87.3±91.0 Phragmipedium Phragmipedium 28 36 36.7 Platypetalum 22 34 32.1 Lorifolia 18±21 36±37 24.4±25.3 Micropetalum 24, 30 36 28.3 Cypripedium Ð 20 40 86.2±129.5 to 129.5 pg.
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