Phylogenetic Relationships in Opuntia (Cactaceae, Opuntioideae) from Southern South America
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Plant Syst Evol DOI 10.1007/s00606-014-1154-1 ORIGINAL ARTICLE Phylogenetic relationships in Opuntia (Cactaceae, Opuntioideae) from southern South America Marı´a F. Realini • Graciela E. Gonza´lez • Fabia´n Font • Pablo I. Picca • Lidia Poggio • Alexandra M. Gottlieb Received: 17 January 2014 / Accepted: 2 September 2014 Ó Springer-Verlag Wien 2014 Abstract The patterns of relationships between species O. elata, O. megapotamica, O. monacantha, O. penicilli- of Opuntia from southern South America are scarcely gera, O. quimilo, O. salmiana, O. schickendantzii, O. sul- known in spite of the importance of this region as a phurea, and O. ventanensis. The genetic distance-based diversification center for the Cactaceae. This paper con- analysis of 110 ISSR bands, applying the Neighbor-Joining tributes to the better understanding of the genetic and and NeighborNet algorithms, evidenced considerable phylogenetic relationships of 15 Opuntia species from intraspecific variation in O. aurantiaca, O. elata, O. dis- Argentina, Bolivia, Brazil, Paraguay, and Uruguay by color, and O. salmiana. The emergent clustering pattern generating new genetic data through Inter-Simple and the species assignment to taxonomic series show a Sequence Repeat (ISSR) genotyping and the sequencing of general agreement for Armatae and Aurantiacae. The plastid intergenic spacers trnL-trnF and psbJ-petA. The phylogenetic relationships were investigated via haplotype species surveyed are: O. anacantha, O. arechavaletae, network and maximum likelihood approaches, within a O. aurantiaca, O. bonaerensis, O. colubrina, O. discolor, broader sampling that involves most species currently accepted for South America, and samples from throughout the American continent. Hence, 15 haplotypes are recog- nized for southern South American opuntias whereas eight Electronic supplementary material The online version of this haplotypes are established for Northern Hemisphere op- article (doi:10.1007/s00606-014-1154-1) contains supplementary untias. Biparentally and maternally inherited genetic data material, which is available to authorized users. yield partially consistent results, giving genetic support for M. F. Realini Á G. E. Gonza´lez Á L. Poggio Á A. M. Gottlieb (&) morphologically defined taxonomic series. Departamento de Ecologı´a, Gene´tica y Evolucio´n, Facultad de ´ Ciencias Exactas y Naturales, Laboratorio de Citogenetica y Keywords Cacti Á ISSR Á Plastid intergenic spacers Á Evolucio´n (LaCyE), Universidad de Buenos Aires, IEGEBA (UBA-CONICET), Buenos Aires, Argentina Phylogenetic analyses e-mail: [email protected] M. F. Realini Á G. E. Gonza´lez Á L. Poggio Á A. M. Gottlieb Introduction Consejo Nacional de Investigaciones Cientı´ficas y Te´cnicas (CONICET), Buenos Aires, Argentina The cacti of the genus Opuntia Mill., commonly known as F. Font prickly pears or nopales, are native plants from the Museo de Farmacobota´nica ‘‘Juan A. Domı´nguez’’, Facultad de American continent, which usually show flattened stem Farmacia y Bioquı´mica, Universidad de Buenos Aires, Buenos Aires, Argentina segments or cladodes, and a number of adaptations for drought resistance. Since pre-Hispanic times, Opuntia P. I. Picca species have had economic relevance throughout its dis- Departamento de Biodiversidad y Biologı´a Experimental, tribution range. Some species are currently commercialized Facultad de Ciencias Exactas y Naturales, Laboratorio de Plantas Vasculares, Universidad de Buenos Aires, Buenos Aires, as forage, ornamentals and food source, while others have Argentina succeeded as exotic weeds (Anderson 2001). 123 M. F. Realini et al. The number of species in Opuntia sensu stricto has been highly branched, and easily removable. Another taxonomic estimated in 250 (Britton and Rose 1919), 160 (Gibson and series is Armatae Schum. (= Elatae Britton and Rose), Nobel 1986), 181 (Anderson 2001), and lately in 75 (Hunt revised by Leuenberger (2002), Hunt et al. (2006) and F. et al. 2006). The main reasons for such taxonomical Font unpubl. data. This series includes the species O. are- conundrum are the paucity of diagnostic morphological chavaletae, O. bonaerensis, O. elata, O. megapotamica, O. characters, the high level of phenotypic plasticity, an monacantha, and O. penicilligera. These cacti are tall alleged recent diversification and the prevalent occurrence bushes with large, orbicular to elliptic cladodes, except for of hybridization and introgression between sympatric and O. penicilligera which shows a prostrate habit. The series allopatric species (Benson and Walkington 1965; Grant Sulphureae Britton and Rose solely includes O. sulphurea, and Grant 1971, 1979; Baker and Pinkava 1987, 1999; which has a prostrate habit with thick, oval and tuberculate Griffith 2001a, b, 2004; Wallace and Gibson 2002; Pinkava cladodes, and morphological variable populations that 2002; Reyes-Agu¨ero et al. 2006; del Castillo and Argueta develop from southern Bolivia and western Paraguay to 2009; Caruso et al. 2010). northern Argentinean Patagonia. The elusive species O. Despite the importance of southern South America as a quimilo is now considered as an isolate entity, though it source of cacti biodiversity (Barthlott and Hunt 1993; was previously placed in Streptacanthae Britton and Rose, Anderson 2001; Boyle and Anderson 2002), the Opuntia and more recently within an Armatae clade (Majure et al. species from this region have received less attention than 2012). Opuntia quimilo is a perennial shrub with a wide the opuntias from the Northern Hemisphere. While several geographical distribution in Argentina, Paraguay, and molecular phylogenetic studies have focused in the north- Bolivia, and a particular reproductive biology for a cactus: ern species (e.g. Griffith 2004; Griffith and Porter 2009; gynodioecy (Dı´az and Cocucci 2003; Nattero and Malerba Ba´rcenas et al. 2011; Herna´ndez-Herna´ndez et al. 2011; 2011). Majure et al. 2012), southern South American (sSA) op- To explore the interspecific genetic relationships among untias have been primarily investigated at the traditional these Opuntia species, we carried out a genotyping with morphological level; also some studies have been achieved Inter-Simple Sequence Repeat markers (ISSR; Zietkiewicz on physiological aspects, and on reproductive biology and et al. 1994), followed by genetic distance-based analyses. pollination issues (Britton and Rose 1919; Schlindwein and Besides the use of ISSR markers in microevolutionary Wittmann 1997; Leuenberger 2002;Dı´az and Cocucci studies, this technique has also been used in the estimation 2003; Hunt et al. 2006; Nattero and Malerba 2011; Lenzi of genetic diversity and differentiation among individuals and Orth 2012; F. Font unpubl. data). and closely related plant species (Ruas et al. 2003; Mans- In the present study, we aimed at investigating the yah et al. 2010; Gaiero et al. 2011; Wang 2011; Rana et al. genetic and phylogenetic relationships of 15 species of 2012). However, few studies have applied ISSR finger- Opuntia sensu stricto from Argentina, Bolivia, Brazil, printing in Opuntia. For instance, Luna-Pa´ez et al. (2007) Paraguay, and Uruguay (namely O. anacantha Speg.,O. employed this technique for variety distinction, whereas arechavaletae Speg., O. aurantiaca Lindl., O. bonaerensis Souto Alves et al. (2009) used it to develop cultivar-spe- Speg., O. colubrina A. Cast., O. discolor Britton and Rose, cific markers. This PCR-based technique generates mul- O. elata Link and Otto ex Salm-Dyck, O. megapotamica tilocus highly polymorphic dominant genomic markers Arechav., O. monacantha Haw., O. penicilligera Speg., O. without the need of prior DNA sequence knowledge quimilo K. Schum., O. salmiana J. Parm. ex Pfeiff.,O. (Zietkiewicz et al. 1994; Mishra et al. 2003). schickendantzii Weber, O. sulphurea Gillies ex Salm- To accomplish a probabilistic phylogenetic analysis Dyck, and O. ventanensis Long). For this set of species, the within a broader sampling framework, we generated patterns of relationships are scarcely known, and the chloroplastic nucleotide sequences. In phylogenetic studies genetic information available is very limited or inexistent. concerning taxa prone to hybridization processes, such as From a taxonomic perspective, the species surveyed cacti, the chloroplast DNA with its uniparental inheritance, roughly correspond to three taxonomic series (Hunt et al. haploidy and lack of recombination, becomes the preferred 2006; F. Font unpubl. data). Aurantiacae Britton and Rose, source of nucleotide data (Porter et al. 2000; Nyffeler comprises the species: O. anacantha, O. aurantiaca, O. 2002; Arias et al. 2005; Butterworth and Wallace 2004; colubrina, O. discolor, O. salmiana, and O. schi- Ritz et al. 2007; Bonatelli et al. 2013). Herein, we have ckendantzii. Also, the recently described O. ventanensis surveyed most of the species currently accepted for has been associated with this series (Long 2012). These South America (Hunt et al. 2006; F. Font unpubl. data) species exhibit a prostrate to creeping habit; the cladodes excepting 5–7 entities for which living plant materials are are elongated, lanceolate, flattened to cylindroid or terete, inaccessible. 123 Southern South American Opuntias Table 1 Southern South American species of Opuntia from which fresh cladodes were used for DNA extraction and subsequent processing as explained in ‘‘Materials and methods’’ section Species Voucher Collection number Collection site Genbank accession number (FF)a number trnL-trnF psbJ-petA O. anacantha Speg. Font