Interstitial Telomerelike Repeats in the Monocot Family Araceae

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Interstitial Telomerelike Repeats in the Monocot Family Araceae bs_bs_banner Botanical Journal of the Linnean Society, 2015, 177, 15–26. With 3 figures Interstitial telomere-like repeats in the monocot family Araceae ARETUZA SOUSA* and SUSANNE S. RENNER Department of Biology, University of Munich (LMU), 80638 Munich, Germany Received 6 May 2014; revised 26 September 2014; accepted for publication 4 October 2014 Combining molecular cytogenetics and phylogenetic modelling of chromosome number change can shed light on the types of evolutionary changes that may explain the haploid numbers observed today. Applied to the monocot family Araceae, with chromosome numbers of 2n = 8 to 2n = 160, this type of approach has suggested that descending dysploidy has played a larger role than polyploidy in the evolution of the current chromosome numbers. To test this, we carried out molecular cytogenetic analyses in 14 species from 11 genera, using probes for telomere repeats, 5S rDNA and 45S rDNA and a plastid phylogenetic tree covering the 118 genera of the family, many with multiple species. We obtained new chromosome counts for six species, modelled chromosome number evolution using all available counts for the family and carried out fluorescence in situ hybridization with three probes (5S rDNA, 45S rDNA and Arabidopsis-like telomeres) on 14 species with 2n =14to2n = 60. The ancestral state reconstruction provides support for a large role of descending dysploidy in Araceae, and interstitial telomere repeats (ITRs) were detected in Anthurium leuconerum, A. wendlingeri and Spathyphyllum tenerum, all with 2n = 30. The number of ITR signals in Anthurium (up to 12) is the highest so far reported in angiosperms, and the large repeats located in the pericentromeric regions of A. wendlingeri are of a type previously reported only from the gymnosperms Cycas and Pinus. © 2014 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 177, 15–26. ADDITIONAL KEYWORDS: 5S and 45S rDNA – ancestral trait reconstruction – Araceae, gymnosperms – Bayesian and maximum-likelihood inference – dysploidy – FISH – interstitial telomeric signals. INTRODUCTION which n = 8 is ancestral to n = 5 through inversions, fusions and translocations (Lysak et al., 2006). A phylogenetic analysis establishes the direction of Descending dysploidy in Arabidopsis could be inferred evolution and allows reconstruction of the likely time- only by combining phylogenetic trees for the relevant frame and sequence of events that may have led to the species with fluorescence in situ hybridization (FISH). character states seen in the included species. With the Work on chromosome evolution in the large monocot availability of DNA-based phylogenetic trees, cytoge- family Araceae, with 3790 species in 118 genera (Boyce neticists have increasingly turned to ‘trait reconstruc- & Croat, 2011), revealed that in this family dysploidy tion’ to infer the direction of change in chromosome may also have played a greater role than polyploidy numbers. Among the insights coming from these (Cusimano, Sousa & Renner, 2012: table S1 lists all efforts is that over the course of evolution descending counts for Araceae; Sousa, Cusimano & Renner, 2014). chromosome numbers (dysploidy) may be a more This inference, however, was based on a relatively common phenomenon than traditionally thought, for sparse sample of species representing the family example in Brassicaceae (Yogeeswaran et al., 2005; (Cusimano et al., 2012) and a follow-up study on one Lysak et al., 2006; Mandakova & Lysak, 2008; Cheng derived tribe, Areae (Sousa et al., 2014). The hypoth- et al., 2013), Rosaceae (Vilanova et al., 2008; Illa et al., esis of frequent chromosome losses due to descending 2011; Jung et al., 2012), Poaceae (Luo et al., 2009) and dysploidy in Araceae is therefore in need of further Melanthiaceae (Pellicer et al., 2014). Probably the best cytogenetic testing. studied case of chromosome rearrangements leading to A cytogenetic test for a possible reduction in chro- descending dysploidy is Arabidopsis (DC.) Heynh., in mosome number by chromosome fusion is the pres- ence of interstitial telomere repeats (ITRs), which can *Corresponding author. E-mail: [email protected] be visualized using standard probes for plant © 2014 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 177, 15–26 15 16 A. SOUSA and S. S. RENNER telomere repeats (Ijdo et al., 1991; Fuchs, Brandes & GenBank accession numbers, are listed in Supporting Schubert, 1995; Weiss-Schneeweiss et al., 2004). Information Table S1. For voucher information on the Thus, ITRs have been used as indicators of chromo- previously sequenced Araceae, see Nauheimer et al. some fusion in Vicia faba L., Sideritis montana L. and (2012; table S1). The final alignment included 160 of Typhonium laoticum Gagnep. (Schubert et al., 1992; the 3790 species from each of the 118 genera of Raskina et al., 2008; Sousa et al., 2014), and telomere Araceae and 11 outgroups representing the remaining signals near a centromere may indicate the fusion of families of Alismatales. two telocentric chromosomes (Schubert et al., 1992). The absence of ITRs, however, does not exclude the possibility of chromosome number reduction via chro- PHYLOGENETIC ANALYSES mosome rearrangements (see Lysak et al., 2006). Alignments were generated in MAFFT (Katoh & Thus far, Pinus L. is the genus with the most con- Standley, 2013; http://mafft.cbrc.jp/alignment/server/) spicuous interstitial telomere FISH signals, with and checked visually using MEGA5 (Tamura et al., often up to four signals near the centromere and in 2011). We removed 249 poorly aligned positions and interstitial positions (Fuchs et al., 1995; Lubaretz the combined plastid matrix was then used for et al., 1996; Schmidt et al., 2000; Hizume et al., 2002; maximum-likelihood (ML) tree searches in RAxML Islam-Faridi, Nelson & Kubisiak, 2007). Based on the (Stamatakis, 2006; Stamatakis, Hoover & inferred large role of descending dysploidy in Araceae Rougemont, 2008), under the GTR + G substitution (Cusimano et al., 2012; Sousa et al., 2014), we decided model with four rate categories because this model to carry out cytogenetic analyses of the distribution of fits the data best, as assessed with Modeltest (Posada telomere repeats in 14 species from 11 genera, & Crandall, 1998). selected to represent lineages of Araceae not previ- Bootstrapping under ML used 1000 replicates. We ously well studied. The enlarged Araceae phylogenetic also generated ultrametric trees in BEAST v. 1.7.5 via analysis and new cytogenetic data on which we report the portal CIPRES science gateway (Drummond & here reveal an unexpected frequency of conspicuous Rambaut, 2007; Miller, Pfeiffer & Schwartz, 2010), ITRs in this family. using the same substitution model for the entire concatenated alignment and a pure-birth Yule model as the tree prior. The analysis was run for 100 million generations, sampling every 1000th step. The burn-in MATERIAL AND METHODS fraction, i.e. the number of trees to be discarded PLANT MATERIAL AND DNA SEQUENCING before reconstructing a consensus tree (the maximum We augmented the DNA data matrix of Nauheimer, clade credibility tree) from the remaining trees, was Metzler & Renner (2012) by adding sequences for 29 assessed using Tracer v. 1.4.1, which is part of the further species from GenBank and by sequencing 14 BEAST package. additional species (on which cytogenetic studies were performed) for the same gene loci used by Nauheimer et al. (the plastid trnL intron and trnL-F spacer, the INFERENCE OF CHROMOSOME NUMBER CHANGE matK gene and partial trnK intron and the rbcL For ML and Bayesian phylogenetic inferences of gene). We used standard primers (Cabrera et al., ancestral haploid chromosome numbers we used 2008), except for matK for which we used the primers ChromEvol v. 1.4 with eight models (Mayrose, Barker listed in Cusimano et al. (2010). Total DNA from & Otto, 2010; http://www.tau.ac.il/~itaymay/cp/ silica-dried leaves was extracted with the NucleoSpin chromEvol/index.html), the fit of which was assessed plant II kit according to the manufacturer’s protocol via likelihood ratio testing, using the Akaike informa- (Macherey-Nagel). Polymerase chain reactions (PCRs) tion criterion (AIC). ChromEvol models have the fol- were performed using 1.25 units of Taq DNA poly- lowing parameters: polyploidization (chromosome merase (New England Biolabs). Each PCR was com- number duplication) with constant rate ρ, demi- posed of 17.55 μLH2O (Sigma), 2.5 μL 10× PCR duplication (fusion of gametes of different ploidy) with buffer, 1 μL10mM dNTPs, 0.75 μL25mM MgCl2, constant rate μ and dysploidization with either con- 0.2 μL Taq polymerase, 1 μL forward primer and 1 μL stant or linearly changing rates (ascending: chromo- reverse primer (Taberlet et al., 1991). The PCR prod- some gain rates λ or λ1; descending: chromosome loss ucts were purified with Exo I and FastAP (Fermen- rates δ or δ1). We fitted all models to a phylogram (in tas). Sequencing was done on an ABI 3130 four- which branch lengths are proportional to numbers of capillary sequencer and sequences were assembled substitutions) and an ultrametric depiction of the and edited with Sequencher 4.2 (Gene Codes Corp.). phylogenetic tree (in which branch lengths are pro- The newly studied and sequenced species, with their portional to time). The phylogram was the RAxML taxonomic authorities, herbarium vouchers and tree, and the ultrametric tree was the BEAST © 2014 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 177, 15–26 CHROMOSOME EVOLUTION IN THE ARACEAE 17 maximum clade credibility tree. For each model, we (w/v), 2× SSC, 10% (w/v) dextran sulfate and 100– ran 10 000 simulated repetitions to compute the 200 ng of labelled probe. The hybridization mix was expected number of changes along each branch of the denatured at 75 °C for 10 min and immediately cooled phylogenetic tree and the ancestral haploid chromo- on ice for 10 min; 10–15 μL of the mix was then added some numbers at nodes. The maximum possible to each slide and the slides plus the hybridization mix ancestral number of chromosomes was set to ten were denatured at 75 ºC for 5 min.
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