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A Screen of Low-Copy Nuclear Genes Reveals the LFY Gene As Phylogenetically Informative in Closely Related Species of Orchids (Ophrys)

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A Screen of Low-Copy Nuclear Genes Reveals the LFY Gene As Phylogenetically Informative in Closely Related Species of Orchids (Ophrys) TAXON 56 (2) • May 2007: 493–504 Schlüter & al. • A screen of low-copy nuclear genes A screen of low-copy nuclear genes reveals the LFY gene as phylogenetically informative in closely related species of orchids (Ophrys) Philipp M. Schlüter1,2,*, Gudrun Kohl1, Tod F. Stuessy1 & Hannes F. Paulus2 1 Department of Systematic and Evolutionary Botany, University of Vienna, Rennweg 14, 1030 Vienna, Austria. [email protected] (author for correspondence) 2 Department of Evolutionary Biology, University of Vienna, Althanstraße 14, 1090 Vienna, Austria * Current address: Ecological Plant Genetics, Swiss Federal Institute of Technology Zürich (ETH), CHN G29, Universitätsstrasse 16, 8092 Zürich, Switzerland This paper presents PCR primers and PCR conditions for low-copy nuclear genes in Ophrys and related orchid genera identified via screening of both published and newly designed primers. For Ophrys, the most useful markers identified in this screen are the LFY/FLO gene which contains an intron of 2 kb size and the MADS-box PI/GLO gene whose 2 first introns contain single nucleotide polymorphisms with variation at the populational level. In the taxa tested, our PCR primers amplified single-copy regions. Phylogenetic analysis of closely related taxa of Ophrys section Pseudophrys, based on LFY, revealed the following groups that are delimited by morphology: O. lutea s.l.; O. omegaifera s.l. with O. iricolor nested in this group; the two O. fusca s.l. taxa, O. leucadica and O. bilunulata; and the O. fusca s.l. taxon O. cinereophila together with a group of endemics from Crete. KEYWORDS: LEAFY/FLORICAULA (LFY/FLO), low-copy nuclear sequence markers, Ophrys fusca s.l., Ophrys section Pseudophrys, PISTILLATA/GLOBOSA (PI/GLO), sexually deceptive orchids data not permitting additional insights apart from the INTRODUCTION identification of tetraploid taxa in the east Mediterranean The European orchid genus Ophrys is remarkable (Greilhuber & Ehrendorfer, 1975; Bernardos & al., 2003; for its pollination by sexual deception which makes it an D’Emerico & al., 2005). interesting system for evolutionary studies (Kullenberg, The present study therefore seeks to evaluate nuclear 1961; Paulus & Gack, 1990). However, the reconstruction low-copy genes, to identify sequence markers that are of relationships within Ophrys, especially among very phylogenetically informative and can be used to infer closely related species, has been hindered by the lack of relationships within Ophrys at a fine level, using sect. resolution obtained with standard chloroplast or nuclear Pseudophrys as a model system. The usefulness of low- ribosomal internal transcribed spacer (ITS) sequence copy nuclear sequence markers is becoming increasingly markers (Pridgeon & al., 1997; Aceto & al., 1999; Soliva & recognised since they frequently outperform ITS and al., 2001; Bateman & al., 2003). The availability of highly plastid markers (e.g., Bailey & Doyle, 1999; Emshwil- variable sequence markers is therefore highly desirable ler & Doyle, 1999; Lewis & Doyle, 2002; Sang, 2002; to address the question of species relationships within Oh & Potter, 2003; Howarth & Baum, 2005). We have Ophrys. screened a large number of available PCR primers for Ophrys section Pseudophrys represents a monophy- nuclear genes to identify gene regions that may be useful letic group within which standard sequence markers do not within Ophrys and related orchids and in addition, have provide any resolution (Soliva & al., 2001; Bateman & al., designed novel primers from sequences in the sequence 2003; Bernardos & al., 2005). This section is characterised databases. by attachment of pollinia to a pollinator’s abdomen rather than its head. Section Pseudophrys contains the morpho- logically readily distinguishable O. lutea s.l., O. fusca s.l. and O. omegaifera s.l. complexes, and the O. iricolor/O. MATERIALS AND METHODS mesaritica species group which has often been considered Plant material and DNA extraction. — Ophrys to be a sub-group of the O. fusca s.l. complex (Paulus plant material (Table 1) was collected in the field and & al., 1990; Paulus, 1998). The relationships among and leaves preserved in silica gel. Non-Ophrys material within these complexes have so far been amenable only was from Orchis italica, Serapias cf. bergonii, Himan- to speculation based upon morphology, chromosomal toglossum hircinum and Himantoglossum (syn. Barlia) 493 Schlüter & al. • A screen of low-copy nuclear genes TAXON 56 (2) • May 2007: 493–504 Table 1. Taxa used and EMBL sequence database accession numbers for LFY. Species Acces- Taxon groupa Country, Island, Locality Dateb sion EMBL Sequence No. O. atlantica Munby O Spain, Alhaurin de la Torre 08.04.2004 196A AM489434 O. basilissa Alibertis & Reinhard O Greece, Samos, Klima 21.02.2004 174A AM489432 O. basilissa Alibertis & Reinhard O Greece, Kos, Asklepion 27.02.2002 66A AM489423 O. bilunulata Risso F Spain, Coin Las Delicias 09.04.2004 198A AM489435 O. cinereophila Paulus & Gack F Greece, Crete, Akoumia 02.04.2003 114A AM489427, AM489428 O. creticola Paulus F Greece, Crete, Jouchtas 30.03.2003 104A AM489426 O. iricolor Desfontaines F Greece, Crete, Kato Horio 29.03.2003 100C AM489425 O. iricolor Desfontaines F Greece, Crete, Ag. Paraskies 30.03.2003 106A AM489419 O. iricolor Desfontaines F Greece, Athens 26.03.2004 208A AM489436 O. “kedra” Paulus (nom. prov.) F Greece, Crete, Spili/Gerakari 07.05.2003 150A AM489431 O. leucadica Renz F Greece, Kos, Kephalos 01.03.2002 67A AM489424 O. omegaifera Fleischmann O Greece, Crete, Thripti 25.03.2002 37A AM489420 O. “pallidula” Paulus (nom. prov.) F Greece, Crete, Thripti 04.05.2003 145C AM489430 O. phryganae Devillers-Terschuren & Devillers L Greece, Rhodes, Kattavia 21.04.2003 120A AM489429 O. sicula Tineo L Greece, Samos, Klima 22.02.2004 177A AM489433 O. sitiaca Paulus, Alibertis & Alibertis O or F Greece, Crete, Jouchtas 14.02.2001 61A AM489422 O. tenthredinifera Willdenow E Greece, Crete, Gourtinia ??.02.2001 56A AM489421 Note: All plants collected by HFP with vouchers in WU, except accessions 120A and 208A, collected by PMS and M. Fiedler, respectively. aPutative membership of the listed taxa in morphological species groups within Ophrys sect. Pseudophrys are indicated, where F, Ophrys fusca s.l.; L, O. lutea s.l.; O, O. omegaifera s.l.; while E is Ophrys sect. Ophrys (syn. Euophrys). bDates are given in DD.MM.YYYY format. robertianum. Additional plant material (Dendrobium, and 3) were screened with standard PCR protocols on a Vanilla, Asparagus) was obtained from plants grown at gradient PCR machine (Thermo Hybaid PX2 or Corbett the Botanical Garden of the University of Vienna. DNA Research Palm-Cycler) using annealing temperatures was extracted using DNeasy Plant Mini Kit (Qiagen) between 40°C and 65°C degrees. Initial reactions were and the manufacturer’s protocol, eluting DNA in 200 performed in a volume of 25 µL containing 12.5 µL RED- µL Tris-EDTA, pH 8.0. In addition, genomic DNA from Taq ReadyMix PCR Reaction Mix (Sigma-Aldrich), 1 Arabidopsis thaliana (Invitrogen, included in the AFLP µL of each, 5 µM forward and reverse primers, and c. Core Reagent Kit) was used. 25 ng genomic DNA. Thermal cycling conditions were Primer design. — For design of new primers, we 95°C 4 min.; 38× (95°C 40 sec.; TA 40 sec.; 72°C 3 min.); used sequences available in the public databases and 72°C 10 min.; 4°C hold, where in each PCR, annealing amino-acid alignments of exons between distantly related temperatures (TA ) varied over a 15°C temperature gra- taxa (where available, including orchid sequences) to iden- dient depending on the expected melting temperatures tify highly conserved regions and noted known intron of the primers used. PCR products were loaded on 1% positions. Alignments were carried out using Clustal agarose gels in TAE (tris acetate EDTA) buffer stained X (Thompson & al., 1997) and Bioedit 7 (Hall, 2001). with ethidium bromide (0.28 mg/L) and photographed Primers were then designed from nucleotide sequence under UV light using a Gel Doc 2000 system (BioRad). If alignments such that (1) their binding sites would lie in no amplification product was obtained, DNA and primer conserved exonic gene regions, (2) PCR would amplify concentrations were varied, different polymerases (e.g., enough exonic sequence to allow gene identification by Taq DNA polymerase, recombinant, from Fermentas) BLAST searches and (3) also variable intronic or exonic used, and in some cases, the thermal cycling conditions sequence would be amplified. In particular, PI and LFY altered. PCR reactions that yielded either a smear or weak primer design was aided by GenBank sequence AB094985 amplification products were subjected to a two-step PCR from Orchis italica and the orchid LFY sequences ob- optimisation testing different buffer systems and PCR en- tained by Montieri & al. (2004), respectively. Primers hancers, using PCR Optimization Kit II (Sigma-Aldrich) were checked for expected melting temperature, loops and the manufacturer’s protocol. If multiple bands were and primer-primer interactions using Oligo Analyzer 1.0.2 obtained, they were separated by excision and elution from software (Kuulasmaa, 2002). gel using QIAquick Gel Extraction Kit (Qiagen). Ampli- Marker screening via polymerase chain reaction fied fragments were then sequenced directly to check a (PCR). — Both published and new primers (Tables 2 PCR product’s identity by BLAST searches, or cloned and 494 TAXON 56 (2) • May 2007: 493–504 Schlüter & al. • A screen of low-copy
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