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Repetitive Dna Sequence from Whooping Cranes (Grus Americana)

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Repetitive Dna Sequence from Whooping Cranes (Grus Americana) The Auk 109(1):73-79, 1992 CHARACTERIZATION AND PHYLOGENETIC SIGNIFICANCE OF A REPETITIVE DNA SEQUENCE FROM WHOOPING CRANES (GRUS AMERICANA) JAMIE LOVE1'3 AND PRESCOTTDEININGER 1'2 •Departmentof Biochemistryand Molecular Biology, Louisiana State University Medical Center, New Orleans, Louisiana 70112, USA; and 2Departmentof MolecularGenetics, Alton OschnerResearch Foundation, New Orleans, Louisiana70212, USA Downloaded from https://academic.oup.com/auk/article/109/1/73/5172808 by guest on 29 September 2021 ABSTR•CT.--Wesurveyed a WhoopingCrane (Grus americana) genomic library enrichedfor repetitiveclones, and isolateda clonewhose insert hybridized stringently to a repeated-DNA family in the genomesof Whooping Cranes,but not Sandhill Cranes(G. canadensis).This tandemsequence, repeated approximately 500 times in theWhooping Crane genome, displays taxon-specificproperties suggesting that the CommonCrane (G. grus) is the Whooping Crane's nearestliving relative. Low-stringencyhybridizations with this repeatproduced conserved patternsin all cranesexcept crowned-cranes (Balearica), which indicatesan earlydivergence of the crowned-cranesand the remainingcranes. Sequence and DNA-hybridization analyses imply that this repeatis a satellitesequence of similarcomplexity and organizationto the primatealphold DNA-sequencefamily, which alsohas chromosome and speciesspecificity. Received13 December1990, accepted 30 April 1991. A SUBSTANTIALportion of the eukaryotic ge- throughout the genome. The large, complex nome consistsof sequencesrepeated thousands, tandem repeats,which are lessstudied in birds, to hundreds of thousands, of times. Because most are the subjectof this paper. We isolated from repetitive sequencesdo not codefor genes,they a Whooping Crane (Grusamericana) an autoso~ often escapeselection and may accumulatemu- mal, complex tandem repeat with taxon speci- tationsrapidly. Consequently,repeats are good ficity and suggestthat it may contribute to the candidatesfor the study of closely related spe- isolating mechanism in cranes. cies. Repeats may be interspersed throughout the genomeor arrangedin long, tandem arrays. MATERIALS AND METHODS Arthur and Straus (1977) found that repeated Constructionof WhoopingCrane library.--We extract- sequenceswere not extensively interspersedin ed high-molecular-weightDNA from female Whoop- the chicken (Gallusgallus) genome, and estab- ing Cranered bloodcells by standardmethods (Mani- lished that avian-genome sequence organiza- atiset al. 1982).It wassheared by sonicationto greater tion is most similar to that of Drosophila.The Cot than 1-kilobase (kb) average fragment length, and curves they produced from DNA samples purified by NACS columnchromatography (Bethesda shearedto differentlengths, indicating that both Research Laboratories, Gaithersburg, Maryland). the fold-back component and the moderately Fragmentswere end-repairedusing the Klenow frag- repeated component of chicken genomes are ment of DNA polymeraseI, and blunt-ligated into primarily tandem repeats. the Sinaisite of pUCl18 following the proceduresof Tandem repeatsare divided into severaltypes King and Blakesley(1986). CompetentXL-1 Blues(a strain of Escherichiacoli from Stratagene,La Jolla, Cal- (families) basedupon length and complexityof ifornia) were transformed with aliquots of the liga- the repeating units. The variable-number tan- tion mix, and recombinantswere selectedby growth dem repeatsthat yield "DNA fingerprints" in on ampicillin plates.The library of 20,000indepen- Southern blot analysisare familiar (for exam- dent clonescontained an averageinsert size of 0.5 kb, ples of their use, see Wetton et al. 1987, Burke representinga total of 10,000kb, or approximately and Bruford 1987).These simple repeatscontain 1%, of the crane's genome, assuming a genome the short sequences,tandemly repeateda moderate same size as the chicken's (1 x 106 kb; Shields 1983). number of times and mostly interspersed Isolationof the whooperrepeat.--The specific clone for the Whooping Crane (whooper repeat) was iso- lated fortuitouslyduring an unsuccessfulsurvey for 3 Present address:AFRC, Edinburgh ResearchSta- sex-specificrepetitive sequences(data not shown). tion, Roslin, Midlothian EH25 9PS, United Kingdom. Clones were tested individually for their ability to 73 74 LOVEAND DEININGER [Auk, Vol. 109 hybridize to dot blots of male and female craneDNA Corp.) was used. Productsof the four forward and of both Whooping Cranes and Sandhill Cranes (G. four reversereactions were electrophoresedthrough canadensis)under high-stringencyconditions. We in- an 8% polyacrylamide,7 M urea gel, after which the vestigateda clone that produceda strong signal with gel was dried under vacuum and autoradiographed. Whooping Crane DNA from both sexes,but not with Sandhill Crane DNA of either sex. This was the RESULTS whooper repeat or clone. Preparationof the whooper-repeatfragment.--The Dot blots.--A one-day autoradiograph dem- whooper clone was double digested with EcoRI and onstrated hybridization of the DNAs of the BamHIto releasethe recombinantinsert. The digested DNA was electrophoresedthrough a 2% agarosegel Whooping Crane and the Common Crane (G. Downloaded from https://academic.oup.com/auk/article/109/1/73/5172808 by guest on 29 September 2021 and the 0.2 kb clone fragment collected. This frag- grus)with intensities equivalent to the control ment was used to make quantified standardsfor dot- Hela sample(2.5 •g) that was spikedwith 250 pg blot experiments and as probe in all hybridization (picograms)of whooper fragment(Fig. 1). This experiments. suggestsapproximately 10 -4 (250 pg/2.5 •g) of Dot-blotanalysis.--DNA from two male Whooping the genomesof these two speciescontain this Cranes,two male Sandhill Cranes,a male hybrid of repeat. The DNA of the Whooping Crane x the two species,and a female of each member of the Sandhill Crane hybrid displayed an intensity genusGrus (as well as a female chicken) were tested. approximatelyhalf that of the Whooping Crane We sonicated2.5 •g of DNA in 10 x SSC(!.5 M sodium chloride, 0.15 M sodium citrate) to approximately 0.5 DNA. No other craneDNA produceda hybrid- kb, boiled for 5 min, and quick-chilled.For quanti- ization signal after a one-day exposure.In fol- tation, 2.5 •g aliquotsof Hela DNA were spikedwith low-up experiments, DNA from all eight different amountsof the whooper fragment and treat- Whooping Cranes testedwere positive, and all ed in the same manner. The solution was vacuum dot sevenSandhill Cranestested were negative(data blotted onto nitrocellulose membrane, then vacuum- not shown). baked at 80øC for 2 h. A six-day exposureof the sameblot revealed The whooper-repeatfragment was radiolabeled with weak hybridizationwith someother speciesof c•2PdATP by nick-translation(Maniatis et al. 1982). crane, which indicatesthe presenceof similar The probe was separatedfrom unincorporated ma- sequence(s).Note that this experiment cannot terials by $ephadexG-50 chromatography. differentiatebetween copynumbers and degree After prehybridization (in 25mM KPO4, 5 x SSC, 5 x Denhardt's solution, 50 •g/ml sonicatedsalmon of sequencesimilarity. The low signalsfrom the milt DNA, 50%formamide), the dot blot was hybrid- longer exposeddot blot may be due to small ized at 42øCovernight in 10 ml of the same solution numbersof sequencesidentical to the whooper containing 6 x 106cpm (0.25 •g) of the boiled probe. sequences,or due to a large number of sequenc- The blot was washed twice in 2x SSC, 0.1% SDS at es that are similar enough to the whooper se- 37øC followed by a wash in 0.1 x SSC at 68øC,and quenceto causea fraction of them to hybridize autoradiographed. with the probe. DNA from the Black-necked Southernblot analysis.--Fivemicrograms of HaeIII- Crane (G. nigricollis)and the Hooded Crane (G. digestedDNA from a female member of eachspecies monachus)produced signals equivalent to ap- of Gruidae, a chicken, a parrot Amazonaochrocephela, and a hawk Parabuteo unicinctus (as well as male proximately 15 pg of the sequencein the 2.5 •g WhoopingCranes, Sandhill Cranes,and a hybrid of dotsof DNA, and that from the JapaneseCrane the two species)were electrophoresedthrough a I% (G. japonensis)contained slightly less. The re- agarosegel and transferred to nitrocellulose mem- maining membersof the Gruidae did not hy- brane (Maniatis et al. 1982). bridize with the whooper probe (at high strin- After prehybridization, the blot was hybridized gency),nor did the chickenor Hela DNAs, even overnight at 42øCin 10 ml of hybridizationsolution after six days of exposure. (asbefore) containing 14 x 106cpm (0.25•g) of probe. Southernblot analysis.--We utilized Southern The blot was washed twice in 2x SSC, 0.1% SDS at blot analysisto determine the pattern of restric- 37øCfollowed by a wash in 0.1x SSC at 60øC.This tion fragments containing this repeated se- low-stringency blot was autoradiographedfor 24 h, after which it was rewashed in 1 L of 0.1 x SSC at quence(Fig. 2). At low stringency,we observed 68øC. This high-stringency blot was autoradio- doubletpatterns of fragmentsin digestsof DNAs graphedfor a similar length of time. of most gruids, including the Wattled Crane Sequencing.--TheDNA of the whooper repeat was (Bugeranuscarunculatus). High-molecular-weight sequencedin both directionsby the methodof Kraft bandswere missingor were very light in some et al. (I 988).$equenase Version 2.0 (U.S. Biochemical species,such as the JapaneseCrane. The pattern January1992] WhoopingCrane Repetitive DNA 75 Six-day One-day Birds Fragment exposure exposure
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