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Ploidy Levels and Genome Sizes of Berberis L. and Mahonia Nutt

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Ploidy Levels and Genome Sizes of Berberis L. and Mahonia Nutt HORTSCIENCE 45(7):1029–1033. 2010. tion of M. nervosa (Pursh) Nutt.] in subgenus Occidentales Ahrendt. Recent phylogenetic analysis based on Ploidy Levels and Genome Sizes internal transcribed spacer (ITS) sequencing (Kim et al., 2004) has yielded further insight of Berberis L. and Mahonia Nutt. into the taxonomic relationships and evolu- tionary history of Mahonia and Berberis. For Species, Hybrids, and Cultivars example, the postulation of Ahrendt (1961) of Mahonia as the progenitor of Berberis was Todd J. Rounsaville1 and Thomas G. Ranney2,3 supported. Examining the contemporary dis- Department of Horticultural Science, Mountain Horticultural Crops persal of the two genera from South America Research and Extension Center, North Carolina State University, 455 northward reveals that although the distinc- tive compound-leaved Mahonia is first en- Research Drive, Mills River, NC 28759 countered in Central America, a number of Additional index words. chromosome number, cytology, DNA content, flow cytometry, Berberis characters persist within Mahonia genome size, polyploidy, systematics, taxonomy much further north. These transitional species, representing the aforementioned Mahonia sec- Abstract. An extensive survey of genome sizes and ploidy levels was conducted for tion Horridae, showed a closer relationship a diverse collection of Berberis and Mahonia taxa (Berberidaceae). Propidium iodide flow with Berberis and thus a paraphyletic subgenus cytometric analysis was conducted using Pisum sativum L. ‘Ctirad’ (2C DNA = 8.76 pg) as Occidentales (Kim et al., 2004). Although ITS an internal standard to determine genome sizes. Mean 1CX genome sizes varied between phylogeny supported the subgenera proposed the two Mahonia subgenera (Occidentales = 1.17 ± 0.02, Orientales = 1.27 ± 0.01), whereas by Ahrendt (1961) and Schneider (1905), those of Berberis subgenera were similar (Australes = 1.45 ± 0.03, Septentrionales = 1.47 ± groupings below the subgeneric levels were 0.02) and each significantly larger than those of Mahonia. Traditional cytology was not supported (Kim et al., 2004). Furthermore, performed on representative species to calibrate genome sizes with ploidy levels. M. nervosa was retained within the Orientales, Polyploidy among both wild and cultivated taxa was found to be rare. Although the albeit with weak support. majority of species were determined to be diploid with 2n =2x = 28, artificially induced Along with the monotypic herb Ranzania autopolyploid Berberis thunbergii seedlings were confirmed to be tetraploid and an japonica T. Ito, Berberis and Mahonia form accession of Mahonia nervosa was confirmed to be hexaploid. Genome size and ploidy a monophyletic clade within Berberidaceae level reports for the majority of taxa sampled are presented for the first time and are in which base chromosome number is x =7 intended to be of use to plant breeders, ecologists, and systematists. (Kim and Jansen, 1998). As Dermen (1931) noted in his cytological studies, chromo- somes among widespread species of both The sister genera Berberis L. and Maho- structure, and floral anatomy had served to genera are of similar size. Furthermore, nia Nutt. represent the two largest groups distinctly separate Mahonia from Berberis. artificial intergeneric hybridization events within the family Berberidaceae,consistingof However, Mahonia section Horridae Fedde between Mahonia and Berberis originated 400 and 100 species, respectively (Ahrendt, (approximately nine species), which includes in Europe as early as 1854 (Dirr, 2009). 1961; Kim et al., 2004). This highly ornamen- M. freemontii (Torr.) Fedde, M. haematocarpa Despite a number of successful intergeneric tal group of shrubs and small trees is valued (Wooton) Fedde, M. nevinii (A. Gray) Fedde, hybrids (·Mahoberberis C.K. Schneid.), the for their evergreen or multicolored leaves, and M. trifoliolata (Moric.) Fedde, exhibits resulting progeny have been horticultural cu- brilliant flowers, and often showy fruit. The a blend of taxonomic features intermediate riosities at best, typically regarded as inferior two genera have also been recognized for their between Mahonia and Berberis (Ahrendt, to both parent taxa (Phillips and Barber, 1981). pharmaceutical and medicinal properties 1961; Whittemore, 1997). These morphologi- ·Mahoberberis tend to exhibit numerous leaf- (Alvarez et al., 2009) as well as their use in cal inconsistencies have led some (Laferriere, morphs among single plants, and in general the printing and dyeing industry (Yan-Jun 1997; Marroquin, 1993; Whittemore, 1997) to flowering and fruiting of the hybrids is known et al., 2006). Distribution of the two genera adopt a unified treatment of all Berberis and to be rare or nonexistent (Dirr, 2009; Wyman, is nearly worldwide with centers of diversity Mahonia species within Berberis. Neverthe- 1958). In addition, all ·Mahoberberis hybrids in southern Asia as well as Central and South less, the obvious difference in physical appear- have been comprised of only one species of America and with minor representation in ance between the two genera, with compound Mahonia [M. aquifolium (Pursh) Nutt.], and North America, Europe, Africa, and the Pa- leaves within Mahonia versus simple leaves the cross appears uni-directional with Mahonia cific Islands (Ahrendt, 1961). within Berberis, makes a unified circumscrip- only functioning as the maternal parent (Dirr, Taxonomic standing of Mahonia and Ber- tion hard to reconcile, and consequently, the 2009; personal observation), further suggest- beris as distinct genera has been the subject of horticultural field generally maintains the two ing that the two genera are largely incompat- much debate among botanists and horticultur- groups as separate genera (Ahrendt, 1961; ible. Conversely, hybrids among species of ists. Before the development of DNA-based Dirr, 2009; Hinkley, 2009; Huxley et al., Berberis and among species of Mahonia are phylogenetics, morphological characters such 1992; Yan-Jun et al., 2006). commonplace (Huxley et al., 1992; personal as leaf and stem complexity, inflorescence When the taxonomy is viewed sensu observation). Ahrendt, Berberis and Mahonia are each Polyploidization is a significant phenom- broken down into two subgenera set forth enon in the plant kingdom that can play a role Received for publication 22 Apr. 2010. Accepted by Ahrendt (1961) and Schneider (1905). in rapid genomic rearrangement, develop- for publication 28 May 2010. Within Berberis, the Australes C.K. Schneid. ment of novel traits and adaptations, repro- We thank Tom Eaker, Nathan Lynch, Joel Mow- includes all the species from Central and ductive isolation, and can ultimately lead to rey, and the staff of the Mountain Horticultural South America; the remaining species are speciation (Adams and Wendel, 2005; Soltis Crops Research Station for their excellent technical placed in the Septentrionales C.K. Schneid. and Burleigh, 2009). Furthermore, poly- assistance. We also thank Tony Avent, Ozzie and occur entirely in the northern hemisphere ploidy is an important consideration in plant Johnson, Todd Wiegardt, and the staff of the JC save for two in East Africa and one in Java breeding because it can influence crossabil- Raulston Arboretum and Bartlett Arboretum for their generous donations of sample material. and Sumatra (Ahrendt, 1961). Conversely, ity, morphology, fertility, and gene expres- 1Graduate Research Assistant. Mahonia are grouped longitudinally with sion (Chen and Ni, 2006; Soltis et al., 2004). 2Professor. those of the Eastern hemisphere in subgenus Sampling of ploidy levels has been very 3To whom reprint requests should be addressed; Orientales Ahrendt and all those of the limited for Mahonia taxa. Mahonia aquifo- e-mail [email protected]. Western hemisphere [with the notable excep- lium, M. napaulensis DC., M. repens (Lindl.) HORTSCIENCE VOL. 45(7) JULY 2010 1029 G. Don., and M. japonica (Thunb.) DC. have major phylogenetic clade. As a result of the (3:1) 95% ethanol:propionic acid overnight been reported to be diploid with 2n =2x =28 unresolved nature of the generic classification, at room temperature. After 16 to 24 h in (Dermen, 1931; Xu et al., 1992). In other and for purposes of comparison, we accept the fixative, the root tissue was rinsed with 70% cases, M. aquifolium and M. nervosa were treatment of Ahrendt (1961), whom conducted ethanol and transferred to storage in 70% reported to be tetraploid with 2n =4x =56 the last thorough review of the genera. ethanol at 4 °C. When time permitted, root (Taylor and Taylor, 1997). Reports on 45 tissue was removed from cold storage and Berberis species found diploids, 2n =2x = 28, Materials and Methods hydrolyzed in a solution of (3:1) 95% etha- including B. koreana Palib., B. seiboldii nol:12N HCl for 5 to 10 s. Root tips were then Miq., B. thunbergii DC., B. vulgaris L., and A diverse collection of Berberis and placed into a drop of modified carbol fuschin B. yunnanensis Franch. as well as tetraploids, Mahonia taxa were obtained from various stain (Kao, 1975) on a glass microscope slide 2n =4x = 56, including B. buxifolia Lam., B. institutions, gardens, and private collectors. and gently squashed with a coverslip. Chro- heterophylla Juss. ex Poir., and B. turcoman- All sampled plants from the Mountain Hor- mosomes were counted using oil immersion ica Kar. (Bottini et al., 2000; Dermen, 1931). ticulture Crops Research Station (MHCRS) at 1500·. Independent of variations in ploidy level, were container-grown, whereas additional information on base genome size (base
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