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PCR to Study Mammalian Phylogeny A Russian Journal of Genetics, Vol. 38, No. 6, 2002, pp. 714–724. Translated from Genetika, Vol. 38, No. 6, 2002, pp. 853–864. Original Russian Text Copyright © 2002 by Bannikova, Matveev, Kramerov. Using Inter-SINE–PCR to Study Mammalian Phylogeny A. A. Bannikova1, V. A. Matveev1, and D. A. Kramerov2 1 Department of Vertebrate Zoology, Moscow State University, Moscow, 119899 Russia; e-mail: [email protected] 2 Engelhardt Institute of Molecular Biology, Russian Academy of Sciences, Moscow, 119991 Russia Received October 31, 2001 Abstract—Results of the use of the fingerprinting method related to short interspersed elements (SINEs), inter- SINE–PCR, in the study of phylogenetic and taxonomic relationship in mammals from orders Chiroptera (fam- ily Vespertilionidae) and Lipotyphla (family Erinaceidae) are reported. The inter-SINE–PCR method is based on the amplification of fragments situated between copies of SINEs, which are short retroposons spaced 100 to 1000 bp apart. Specifically selected primers were used, which are complementary to consensus sequences of two short retroposons: the mammalian interspersed repeat (MIR), which is typical of all mammals and some other vertebrates, was used in the cases of bats and Erinaceidae, and the ERI-1 element recently isolated from the genome of the Daurian hedgehog was used in the case of Erinaceidae. The results support the current view on phylogenetic relationship between hedgehogs belonging to genera Erinaceus, Hemiechinus, and Paraechi- nus (but not the genus Atelerix). In bats, the phylogenetic reconstruction revealed a statistically valid topology only at lower taxonomic levels, whereas the topology for the genus and supragenus ranks was unresolved and fan-shaped. The benefits and limitations of the inter-SINE–PCR method are discussed. INTRODUCTION SINE families. The presence or absence of a SINE fam- ily in a genome is a perfect synapomorphy, because, In modern studies on the phylogeny and taxonomy once appeared, the SINE family is preserved in all later of the intraorder level, the role of PCR-based molecular separated branches of the given stem of the evolution- markers has significantly enhanced. The examples are ary tree [7, 8]. Another perfect synapomorphy is the molecular markers obtained using the following meth- presence or absence of some SINE copies in certain loci ods: RAPD, which detects randomly amplified poly- of the genome. These traits were successfully used in morphic DNA fragments in PCR with a single arbitrary phylogenetic studies of mammals and fish [9, 10]. primer [1]; SSR–PCR, which enables one to amplify However, this approach is labor-consuming and expen- DNA fragments situated between microsatellites [2]; sive. and AFLP, which represents the results of selective amplification of restriction fragments of genomic DNA Another approach to phylogenetic studies that is also and combines the potentialities of RFLP and PCR [3]. based on using SINEs is considerably easier and less The search for universal markers that are applicable for expensive. This method, inter-SINE–PCR, consists in the both diagnostic and phylogenetic purposes is continued. amplification of fragments situated between SINE copies In this work, we report the results of using one more situated at a relatively small (100 to 1000 bp) distance variety of fingerprinting, which is related to short inter- apart (Fig. 1). For the first time, restriction polymor- spersed elements (SINEs). We used this method, inter- phism of DNA fragments flanked by short interspersed SINE–PCR, in the studies of taxonomic relationship in repeats was investigated in the study of Alu-polymor- mammals. SINEs (short interspersed elements, short ret- phism in the human genome (so-called Alu–PCR or roposons) are repeated 80- to 400-bp DNA sequences, IRS–PCR [11]). Later, polymorphism of other short tens and even hundreds of thousands copies of which interspersed repeats was studied in the mammalian are dispersed throughout the genome [4–6]. SINEs are order Artiodactyla [12] transcribed by RNA polymerase III, and the reverse Our attention was drawn by a SINE family named transcription of the newly formed low-molecular- the mammalian interspersed repeat (MIR), which is weight RNA can result in the formation of new SINE represented by 105 copies probably in all mammalian copies. The overwhelming majority of SINE families genomes [13–15]. The MIR elements represent one of originate from tRNA molecules, which was established the most ancient of known SINE families, which is from the similarity between the nucleotide sequences indicated by their wide distribution and an extremely of tRNA and the head part of SINEs. The tail part of high (up to 50%) divergence of their copies. The latter SINEs is usually formed by an A-rich sequence, fact also indicates that, in contrast to other known whereas the central part is quite different in different SINEs, MIR stopped multiplying long ago. Apparently, 1022-7954/02/3806-0714 $27.00 © 2002 MAIK “Nauka /Interperiodica” USING INTER-SINE–PCR TO STUDY MAMMALIAN PHYLOGENY 715 MIL17 MIR17 MIL17 Genomic locus 1 locus 2 locus 3 DNA MIR MIR MIR MIR MIL17 MIR17 MIL17 PCR products Fig. 1. Scheme of SINE–PCR. Four MIR element copies are shown, of which three are oriented in one direction and one in the other. Thin arrows indicate primers MIL17 and MIR17, which are complementary to different DNA strands. Taken separately, each of the primers ensures the amplification of the regions situated between tail-to-tail- or head-to-head-oriented MIR element copies (locus 1 or locus 2, respectively). Simultaneous presence of both primers in the reaction mixture ensures the amplification of the fragment flanked by equally (tail-to-head) oriented MIR element copies (locus 3). because of the ancient origin, full-sized MIR copies Hylomyinae); in Chiroptera, 40 vespertilionid bats (260 bp in length) occur relatively seldom. As a rule, (family Vespertilionidae), 2 bats of different horseshoe the copies are lacking one or both termini, and the bat species (family Rhinolophidae), and 2 bulldog bats majority of these copies are represented by the only (family Molossidae). The description of samples is central region (core sequence), 70 bp in length, for given in Table 1. which the reasons are not clearly understood. Differ- DNA isolation. DNA was isolated from ethanol- ences in the patterns of inter-SINE–PCR products are fixed tissues (muscles, testes, kidneys, and liver) by caused by both mutations in the copies of these repeats phenol–chloroform extraction following the treatment per se and deletions and insertions in DNA regions sit- of tissue homogenates with pronase [21]. uated between the copies. To date, the inter-SINE–PCR method was used only Conditions of inter-SINE–PCR. Inter-MIR–PCR for the studies of phylogeny in Artiodactyla [16]. The (hereafter, MIR–PCR) was conducted using one or two objects of our study were mammals belonging to two primers that were complementary to the most con- orders: Lipotyphla and Chiroptera. In addition to the served region of the central core sequence of the MIR MIR elements, we studied a short retroposon ERI1 element [14]: MIR17, 5'-AGTGACTTGCTCAAGGT-3', and MIL17, 5'-GCCTCAGTTTCCTCATC-3' (Fig. 1). (158 bp in length), which is specific of only the family γ32 Erinaceidae and has recently been isolated from the Primers (100 pmole each) were labeled with [ P]-ATP (1 MBq) by polynucleotide kinase [22]. PCR was con- genome of the Daurian hedgehog Hemiechinus dauuri- µ cus [17]. Note that such SINEs, which are characterized ducted in 20 l of a reaction mixture containing 10 mM of by a narrow distribution range and a relatively low a Tris–HCl buffer, pH 8.3; 50 mM KCl; 2.5 mM MgCl2; divergence of copies, were never used in phylogenetic 0.001% gelatin; dNTPs, 0.2 mM each; 4 pmole of each studies conducted by the inter-SINE–PCR method primer; 1 EU of Taq polymerase (Sileks); and 25 ng of before our work. DNA template. The conditions of MIR-specific PCR corresponded to an earlier described schedule [14]: According to recent data of molecular macrotaxon- denaturation, 30 s at 94°C; annealing, 45 s at 56°C; and omy [18, 19], true insectivorous mammals Eulipo- elongation, 2 min at 72°C. The number of cycles was 27. typhla and bats Microchiroptera represent a monophyl- The initial denaturation and final synthesis lasted for 3 etic group, whereas they greatly differ in the direction min at 94°C and 5 min at 72°C, respectively. of radiation. Ancient insectivorous mammals were a very generalized group, which allowed them to become In ERI–PCR, we used the primer that was comple- ancestral forms for most of latest placental animals. mentary to the fore end of the ERI1 element (5'-CCAC- From their origin till the present, Chiroptera have been CTCCC(G/A)GGACCAC-3') [17] and initiated DNA related to the most specialized mammals, while some synthesis in the direction upstream of the SINE. The of them, e.g., bats, preserved some particular morpho- primer was labeled as described above. In the experi- logical features that bring these bats closer to insectiv- ments with ERI1, a consistently reproducible pattern was obtained upon increasing the annealing tempera- orous mammals [20]. Among Lipotyphla, the most ° ancient family is Erinaceidae. So far, no consensus ture by 5 C as against the calculated temperature. As a exist on the number of genera and species of this fam- result, PCR was conducted under the following condi- tions: denaturation, 30 s at 94°C; annealing, 45 s at ily. The largest bat family, Vespertilionidae, is also the ° ° most taxonomically confused. All of the above has 65 C; and elongation, 2 min at 72 C. The number of motivated a comparative study of these two taxa. cycles was 27. The initial denaturation and final synthe- sis lasted for 3 min at 94°C and 5 min at 72°C, respec- tively.
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