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The Absence of Arabidopsis-Type Telomeres in Cestrum and Closely Related Genera Vestia and Sessea (Solanaceae): ®Rst Evidence from Eudicots

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The Absence of Arabidopsis-Type Telomeres in Cestrum and Closely Related Genera Vestia and Sessea (Solanaceae): ®Rst Evidence from Eudicots The Plant Journal (2003) 34, 283±291 The absence of Arabidopsis-type telomeres in Cestrum and closely related genera Vestia and Sessea (Solanaceae): ®rst evidence from eudicots Eva Sykorova1,2,y, Kar Yoong Lim1,y, Mark W. Chase3, Sandra Knapp4, Ilia Judith Leitch3, Andrew Rowland Leitch1,à and Jiri Fajkus2 1School of Biological Sciences, Queen Mary University of London, London E1 4NS, UK, 2Institute of Biophysics, Academy of Sciences of the Czech Republic and Masaryk University of Brno, Brno, Czech Republic, 3Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3AB, UK, and 4Department of Botany, Natural History Museum, Cromwell Road, London SW7 5BD, UK Received 2 October 2002; accepted 24 January 2003. ÃFor correspondence (fax 44 208 983 0973; e-mail [email protected]). yJoint ®rst author. Summary Using slot-blot and ¯uorescent in situ hybridization (FISH), we found no evidence for the presence of the Arabidopsis-type telomeric sequence (TTTAGGG)n at the chromosome termini in any of the Cestrum spe- cies we investigated. Probing for the human-type telomere (TTAGGG)n also revealed no signal. However, polymerase chain reaction experiments indicated that there are short lengths of the sequence TTTAGGG dispersed in the genome but that these sequences are almost certainly too short to act as functional telomeres even if they were at the chromosome termini. An analysis of related genera Vestia and Sessea indicates that they too lack the Arabidopsis-type telomere, and the sequences were lost in the common ancestor of these genera. We found that the Cestrum species investigated had particularly large mean chromosome sizes. We discuss whether this is a consequence of alternative telomere end maintenance systems. Keywords: absence of TTTAGGG telomere, dicot, chromosome, FISH. Introduction The ends of eukaryotic chromosomes frequently, but not of chromosome ends degraded by incomplete lagging ubiquitously, have TnGn rich minisatellite sequences occur- strand synthesis during the S phase of the cell cycle. ring in tandem arrays of many hundreds or thousands of However, the highly conserved minisatellite telomeric repeats. In higher plants, the consensus sequence cloned sequence is not universally found. Sahara et al. (1999) used from Arabidopsis thaliana is (TTTAGGG)n (Richards and Southern hybridization to show that the species in four Ausubel, 1988). Similar minisatellite sequences are con- orders of insects (Diptera, Coleoptera, Heteroptera, and served in vertebrates, as in human, in which the consensus Dermaptera) and a spider lacked the insect consensus sequence is (TTAGGG)n (Moyzis et al., 1988), whereas in sequence (TTAGG)n. Of the nine species of Coleoptera many insects it is (TTAGG)n (Okazaki et al., 1993). Telo- investigated, four lacked (TTAGG)n. If these numbers are meres distinguish the natural chromosome ends from in any way representative of Coleoptera, it could be pre- unrepaired chromosome breaks and are thought to per- dicted that there may be millions of beetle species without form the following functions: (i) prevention of end-to-end the insect consensus sequence. In Drosophila melanoga- fusions of chromosomes; (ii) binding of speci®c telomere- ster (Diptera), the telomeres contain Het-A and TART that associated proteins involved in DNA folding producing a preferentially retrotranspose to the chromosome termini, stable structure that may interact with the nuclear envel- whereas in D. virilis and other species in the virilis group, ope, be involved in chromosome disposition, and per- as well as in the genus Chironomus (Diptera), complex haps prevent chromosome fusions; and (iii) re-synthesis satellite DNA sequences, presumed to be elongated by a ß 2003 Blackwell Publishing Ltd 283 284 Eva Sykorova et al. homologous recombination mechanism, are located at the appear to be absent from the chromosome termini and telomeres (Biessmann et al., 2000). therefore are not telomere sequences. Thus, this paper In plants too, there is evidence that the plant consensus provides evidence of an absence of Arabidopsis-type telo- sequence (TTTAGGG)n is lacking in some groups. Fuchs meres in eudicot plants. et al. (1995) showed that it was absent in Allium, Nothos- cordum, and Tulbaghia of the monocotyledonous family Results Alliaceae. Further analysis showed that the sequence was most likely replaced by rDNA, a satellite sequence or retro- Pich and Schubert (1998) and Adams et al. (2000) demon- transposable element(s) at the end of the chromosome strated an absence of Arabidopsis-type telomeric (Pich and Schubert, 1998; Pich et al., 1996a,b). Adams et al. sequences in the monocot genera Aloe and Allium using (2000) showed that Aloe in Asphodelaceae also lacked several methods: (i) ¯uorescent in situ hybridization (FISH) (TTTAGGG)n.AsAllium and Aloe are distantly related using a PCR-generated concatemer of the Arabidopsis con- members of the order Asparagales, this led to an investiga- sensus sequence (TTTAGGG)5 as a probe; (ii) Southern/ tion of other related genera. Many other species were found slot-blot hybridization analysis using the TTTAGGG con- to lack the sequence suggesting that an absence of the catemer probe; and (iii) elongation or asymmetric PCR Arabidopsis-type repeat was common in Asparagales using the forward primer only of the oligonucleotide (Adams et al., 2000) although the human-type of telomere sequence (TTTAGGG)4. Variations on these approaches (TTAGGG)n occurs in some of the species in its place (Weiss were used on Cestrum. and Scherthan, 2002). For the purpose of this paper, it is important to clarify the Absence of Arabidopsis-type telomeres using FISH terms Arabidopsis-type telomeric sequence, which de®nes the minisatellite (TTTAGGG)n sequence, as distinct from Fluorescent in situ hybridization experiments using a bio- the Arabidopsis-type telomere, which describes a telomere tin-labelled concatemer of the Arabidopsis-type telomeric formed by this sequence. Here we provide evidence that sequence (TTTAGGG)5 (Cox et al., 1993; Ijdo et al., 1991), whereas short lengths of the Arabidopsis-type sequence detected by avidin-Cy3, revealed that there was an absence are dispersed in some species of the closely related genera of probe labelling to the ends of chromosomes in Cestrum Cestrum, Vestia and Sessea (Solanaceae), these sequences parqui (Figure 1a,b) and Vestia foetida (Figure 1d,e) Figure 1. FISH to metaphase spreads of Cestrum parqui (a±c), Vestia foetida (d±f) and Nicotiana sylvestris (g,h), stained with DAPI for DNA (blue (a,d,g)) and probed with avidin-labelled Arabidopsis-type telomere probe detected with Cy3 (red (b,e,h)). Note only N. sylvestris shows strong labelling at the ends of the chromosomes. For a positive control, the metaphases of C. parqui and V. foetida are probed with digoxigenin-labelled 18±26S rDNA (c) and 5S rDNA (f), respectively (yellow-green). The intensity of the FITC signal for 18±26S rDNA in C. parqui (c) has resulted in some light coming through the Cy3 ®lter block and is thus visible in (b). Scale bar 10 mm. ß Blackwell Publishing Ltd, The Plant Journal, (2003), 34, 283±291 Loss of TTTAGGGn-type telomeres in a eudicot group 285 metaphase cell spreads. Ribosomal DNA (18±26S or 5S rDNA) was used as a positive control for the ef®cacy of the in situ methods (Figure 1c,e). Clear signals were observed using the Arabidopsis-type telomeric sequence on control metaphase spreads of Nicotiana sylvestris as expected (Figure 1g,h). FISH may be a low-sensitivity method for detecting sequences, as less than 1 kb of con- tiguous sequence may not be detectable (Gill and Friebe, 1998). For this reason, the results were complemented by slot-blot and PCR approaches. Slot-blot analysis of genomic DNA Using slot-blot hybridization and the labelled ATSB probe, we analysed genomic DNAs from eight Cestrum species and a hybrid (Table 1) for the presence of Arabidopsis-type Figure 2. Slot-blot hybridization with radioactive-labelled telomere primer telomeric sequences (Figure 2a). The negative control used (a) ATSB or (b) HUSB as the probe. in the experiment was genomic DNAs of Allium cepa, and Control DNAs are Nicotiana sylvestris (S), Silene latifolia (R), Homo sapiens the positive controls were genomic DNAs of N. sylvestris (Q), Allium cepa (V) and N. otophora (Y). Species investigated in the Sola- naceae are Cestrum aurantiacum (A), C. elegans (B), C. fasciculatum (C), and Silene latifolia, the latter having relatively short telo- C. nocturnum (D), C. psittacinum (E), C. purpureum (F), C. roseum (G), mere repeats with approximately 2.5±4.5 kb of Arabidopsis- C. parqui (T), C. parqui  C. aurantiacum (U), Streptosolen jamesonii (H), type telomeric sequence per chromosome terminus (Riha Solanum betaceum (I), Physalis alkekengi (J), Iochroma australe (K), Lycium barbarum (L), L. cestroides (M), Withania coagulans (N), Vestia foetida (O), et al., 1998). All membranes were re-probed with 18S rDNA Nicandra physaloides (P), and Sessea stipulata (X). to ensure transfer of genomic DNA (data not shown). Greater sensitivity may be obtained using Southern hybri- dization because the method can potentially separate telo- and control DNA from S. latifolia were analysed by this mere repeat sequences from the bulk of genomic DNA. technique for the presence of Arabidopsis-type telomeric Therefore, genomic DNAs of Cestrum parqui, C. elegans sequences. No signal was obtained in Cestrum DNAs, but Table 1 The species used Species Herbarium voucher specimen Seed/plant source Allium cepa L. cv. Ailsa Craig RBG, Kew Arabidopsis thaliana L. cv. Columbia Queen Mary, London Cestrum aurantiacum Lindl. Chase 12216 (K) RBG, Kew Cestrum elegans (Brongn.) Schltdl. Lim 002 (BM) Ginkgo Nursery, London, UK Cestrum fasciculatum (Schltdl.) Miers Chase 12218 (K) RBG, Kew Cestrum nocturnum L. Chase 12219 (K) RBG, Kew Cestrum parqui L'Her. Chelsea Physic Garden, London, UK Cestrum parqui  Cestrum aurantiacum Saikia 001 (BM) Ginkgo Nursery, London, UK Cestrum psittacinum Stapf.
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