期刊论文详细信息
BMC Evolutionary Biology
Reconstruction and in vivo analysis of the extinct tbx5 gene from ancient wingless moa (Aves: Dinornithiformes)
David M Lambert5  Sara Mirmoeini1  Craig Smith7  Michael Hofreiter6  Craig D Millar2  Yusuke Watanabe4  Toshihiko Ogura4  Takayuki Suzuki3  Leon Huynen5 
[1] Institute of Natural Sciences, Massey University, Auckland 0632, New Zealand;Allan Wilson Centre for Molecular Ecology and Evolution, School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland, New Zealand;Division of Biological Science, Nagoya University, Nagoya 464-8602, Japan;Institute of Development, Aging and Cancer (IDAC), Tohoku University, Sendai 980-8575, Japan;Environmental Futures Centre, Griffith University, 170 Kessels Road, Nathan Qld 4111, Australia;Faculty of Natural Sciences, University of Potsdam, 14476 Potsdam, Germany;Murdoch Children’s Research Institute, Royal Children’s Hospital, Flemington rd Parkville, Victoria 3052, Australia
关键词: Forelimb;    Development;    Ancient DNA;    Gene expression;    Moa;    tbx5;   
Others  :  856564
DOI  :  10.1186/1471-2148-14-75
 received in 2014-02-15, accepted in 2014-03-25,  发布年份 2014
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【 摘 要 】

Background

The forelimb-specific gene tbx5 is highly conserved and essential for the development of forelimbs in zebrafish, mice, and humans. Amongst birds, a single order, Dinornithiformes, comprising the extinct wingless moa of New Zealand, are unique in having no skeletal evidence of forelimb-like structures.

Results

To determine the sequence of tbx5 in moa, we used a range of PCR-based techniques on ancient DNA to retrieve all nine tbx5 exons and splice sites from the giant moa, Dinornis. Moa Tbx5 is identical to chicken Tbx5 in being able to activate the downstream promotors of fgf10 and ANF. In addition we show that missexpression of moa tbx5 in the hindlimb of chicken embryos results in the formation of forelimb features, suggesting that Tbx5 was fully functional in wingless moa. An alternatively spliced exon 1 for tbx5 that is expressed specifically in the forelimb region was shown to be almost identical between moa and ostrich, suggesting that, as well as being fully functional, tbx5 is likely to have been expressed normally in moa since divergence from their flighted ancestors, approximately 60 mya.

Conclusions

The results suggests that, as in mice, moa tbx5 is necessary for the induction of forelimbs, but is not sufficient for their outgrowth. Moa Tbx5 may have played an important role in the development of moa’s remnant forelimb girdle, and may be required for the formation of this structure. Our results further show that genetic changes affecting genes other than tbx5 must be responsible for the complete loss of forelimbs in moa.

【 授权许可】

   
2014 Huynen et al.; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Phillips MJ, Gibb GC, Crimp EA, Penny D: Tinamous and moa flock together: mitochondrial genome sequence analysis reveals independent losses of flight among ratites. Syst Biol 2009, 59:90-107.
  • [2]Zakany J, Duboule D: The role of Hox genes during vertebrate limb development. Curr Op Genet Dev 2009, 17:359-366.
  • [3]Moon AM, Capecchi MR: Fgf8 is required for outgrowth and patterning of the limbs. Nat Genet 2000, 26:455-459.
  • [4]Min H, Danilenko DM, Scully SA, Bolon B, Ring BD, Tarpley JE, DeRose M, Simonet S: Fgf-10 is required for both limb and lung development and exhibits striking functional similarity to Drosophila branchless. Genes Dev 1998, 12:3156-3161.
  • [5]Ng JK, Kawakami Y, Buscher D, Raya A, Itoh T, Koth CM, Rodriguez Esteban C, Rodriguez-Leon J, Garrity DM, Fishman MC, Izpisua Belmonte JC: The limb identity gene Tbx5 promotes limb initiation by interacting with Wnt2b and Fgf10. Development 2002, 129:5161-5170.
  • [6]Agarwal P, Wylie JN, Galceran J, Arkhitko O, Li C, Deng C, Grosschedl R, Bruneau BG: Tbx5 is essential for forelimb bud initiation following patterning of the limb field in the mouse embryo. Development 2003, 130:623-633.
  • [7]Argentin S, Ardati A, Tremblay S, Lihrmann I, Robitaille L, Drouin J, Nemer M: Developmental stage-specific regulation of atrial natruiretic factor gene transcription in cardiac cells. Mol Cell Biol 1994, 14:777-790.
  • [8]Koshiba-Takeuchi K, Takeuchi JK, Arruda EP, Kathiriya IS, Mo R, Hui CC, Srivastava D, Bruneau BG: Cooperative and antagonistic interactions between Sall4 and Tbx5 pattern the mouse limb and heart. Nat Genet 2006, 38:175-183.
  • [9]Ghosh TK, Packham EA, Bonser AJ, Robinson TE, Cross SJ, Brook JD: Characterization of the Tbx5 binding site and analysis of mutations that cause Holt-Oram syndrome. Hum Mol Genet 2001, 10:1983-1994.
  • [10]Takeuchi JK, Koshiba-Takeuchi K, Suzuki T, Kamimura M, Ogura K, Ogura T: Tbx5 and Tbx4 trigger limb initiation through activation of the Wnt/Fgf signalling cascade. Development 2003, 130:2729-2739.
  • [11]Bruneau BG, Nemer G, Schmidt JP, Charron F, Robitaille L, Caron F, Conner DA, Gessler M, Nemer M, Seidman CE, Seidman JG: A murine model of Holt-Oram syndrome defines roles of the T-Box transcription factor Tbx5 in cardiogenesis and disease. Cell 2001, 106:709-721.
  • [12]Ahn D, Kourakis MJ, Rohde LA, Silver LM, Ho RK: T-box gene tbx5 is essential for formation of the pectoral limb bud. Nature 2002, 417:754-758.
  • [13]Garrity DM, Childs S, Fishman MC: The heartstrings mutation in zebrafish causes heart/fin Tbx5 deficiency syndrome. Development 2002, 129:4635-4645.
  • [14]Brassington AME, Sung SS, Toydemir RM, Le T, Roeder AD, Rutherford AE, Whitby FG, Jorde LB, Bamshad MJ: Expressivity of Holt-Oram syndrome is not predicted by Tbx5 genotype. Am J Hum Genet 2003, 73:74-85.
  • [15]Borozdin W, Bravo Ferrer Acosta AM, Bamshad MJ, Botzenhart EM, Froster UG, Lemke J, Schinzel A, Spranger S, McGaughran J, Wand D, Chrzanowska KH, Kohlhase J: Expanding the spectrum of TBX5 mutations in Holt-Oram syndrome: detection of two intragenic deletions by quantitative real time PCR, and report of eight novel point mutations. Hum Mutat 2006, 27:975-976.
  • [16]Mori AD, Bruneau BG: Tbx5 mutations and congenital heart disease: Holt-Oram syndrome revealed. Curr Opin Cardiol 2004, 19:211-215.
  • [17]Basson CT, Huang T, Lin RC, Bachinsky DR, Weremowicz S, Vaglio A, Bruzzone R, Quadrelli R, Lerone M, Romeo G, Silengo M, Pereira A, Krieger J, Mesquita SF, Kamisago M, Morton CC, Pierpont ME, Müller CW, Seidman JG, Seidman CE: Different Tbx5 interactions in heart and limb defined by Holt-Oram syndrome mutations. Proc Natl Acad Sci U S A 1999, 96:2919-2924.
  • [18]Isphording D, Leylek AM, Yeung J, Mischel A, Simon H-G: T-box genes and congenital heart/limb malformations. Clin Genet 2004, 66:253-264.
  • [19]Margaglione M, Santacroce R, Colaizzo D, Seripa D, Vecchione G, Lupone MR, De Lucia D, Fortina P, Grandone E, Perricone C, Di Minno G: A G-to-A mutation in IVS-3 of the human gamma fibrogen gene causing afibrinogenemia due to abnormal RNA splicing. Blood 2000, 96:2501-2505.
  • [20]Asselta R, Duga S, Simonic T, Malcovati M, Santagostino E, Giagrande PL, Mannucci PM, Tenchini ML: A fibrinogenemia: first identification of a splicing mutation in the fibrogen gamma chain gene leading to a major gamma chain truncation. Blood 2000, 96:2496-2500.
  • [21]McCall RA, Nee S, Harvey PH: The role of wing length in the evolution of avian flightlessness. Evol Ecol 1998, 12:569-580.
  • [22]Slikas B, Olson SL, Fleischer RC: Rapid, independent evolution of flightlessness in four species of Pacific Island rails (Rallidae): an analysis based on mitochondrial sequence data. J Avian Biol 2002, 33:5-14.
  • [23]Cracraft J: Phylogeny and evolution of the ratite birds. Ibis 1974, 116:494-521.
  • [24]Worthy TH, Holdaway RN: The lost world of the moa: Canterbury University Press. New Zealand: Christchurch; 2002.
  • [25]Baker AJ, Huynen LJ, Haddrath O, Millar CD, Lambert DM: Reconstructing the tempo and mode of evolution in an extinct clade of birds with ancient DNA: the giant moas of New Zealand. Proc Natl Acad Sci U S A 2005, 102:8257-8262.
  • [26]Bunce M, Worthy TH, Phillips MJ, Holdaway RN, Willerslev E, Haile J, Shapiro B, Scofield RP, Drummond A, Kamp PJ, Cooper A: The evolutionary history of the extinct ratite moa and New Zealand Neogene paleogeography. Proc Natl Acad Sci U S A 2009, 106:20646-20651.
  • [27]Tennyson AJD, Worthy TH, Jones CM, Scofield RP, Hand SJ: Moa’s Ark: Miocene fossils reveal the great antiquity of moa (Aves: Dinornithiformes) in Zealandia. Rec Aust Mus 2010, 62:105-114.
  • [28]Scarlett RJ, Molnar : Terrestial bird or dinosaur phalanx from the New Zealand Cretaceous. NZ J of Zoology 1984, 11:271-275.
  • [29]Gans C: Tetrapod limblessness: evolution and functional corollaries. Am Zool 1975, 15:455-467.
  • [30]Greer AE: Limb reduction in squamates: identification of the lineages and discussion of the trends. J Herpetol 1991, 25:166-173.
  • [31]Whiting AS, Bauer AM, Sites JW: Phylogenetic relationships and limb loss in sub-Saharan African scincine lizards (Squamata: Scincidae). Mol Phylogen Evol 2003, 29:582-598.
  • [32]Collin R, Cipriani R: Dollo’s law and the re-evolution of shell coiling. Proc Royal Soc B 2003, 270:2551-2555.
  • [33]Skinner S, Lee MSY, Hutchinson MN: Rapid and repeated limb loss in a clade of scincid lizards. BMC Evol Biol 2008, 8:310. BioMed Central Full Text
  • [34]Brandley MC, Huelsenbeck JP, Wiens JJ: Rates and patterns in the evolution of snake-like body form in squamate reptiles: evidence for repeated re-evolution of lost digits and long-term persistence of intermediate body forms. Evolution 2008, 62:2042-2064.
  • [35]Kohlsdorf T, Wagner GP: Evidence for the reversibility of digit loss: a phylogenetic study of limb evolution in Bachia (Gymnophthalmidae: Squamata). Evolution 2006, 60:1896-1912.
  • [36]Lande R: Evolutionary mechanisms of limb loss in tetrapods. Evolution 1978, 32:73-92.
  • [37]Harris PH, Hasso SM, Ferguson MWJ, Fallon JF: The development of Archosaurian First-Generation teeth in a chicken mutant. Curr Biol 2006, 16:371-377.
  • [38]Borowsky R: Restoring sight in blind cavefish. Curr Biol 2008, 18:R23-24.
  • [39]Kohlsdorf T, Cummings MP, Lynch VJ, Stopper GF, Takahashi K, Wagner GP: A molecular footprint of limb loss: Sequence variation of the autopodial identity gene Hoxa-13. J Mol Evol 2008, 67:581-593.
  • [40]Hasson P, Del Buono J, Logan MPO: Tbx5 is dispensable for forelimb outgrowth. Development 2007, 134:85-92.
  • [41]Minguillon C, Nishimoto S, Wood S, Vendrell E, Gibson-Brown JJ, Logan MPO: Hox genes regulate the onset of Tbx5 expression in the forelimb. Development 2012, 139:3180-3188.
  • [42]Kohlhase J, Schubert L, Liebers M, Rauch A, Becker K, Mohammed SN, Newbury-Ecob R, Reardon W: Mutations at the SALL4 locus on chromosome 20 result in a range of clinically overlapping phenotypes, including Okihiro syndrome, Holt-Oram syndrome, and patients previously reported to represent thalidomide embryopathy. J Med Genet 2003, 40:473-478.
  • [43]Hamburger V, Hamilton HL: A series of normal stages in the development of the chick embryo. 1951. Dev Dyn 1992, 195:231-272.
  • [44]Nagai H, Mak SS, Weng W, Nakaya Y, Ladher R, Sheng G: Embryonic development of the emu, Dromaius novaehollandiae. Dev Dyn 2011, 240:162-175.
  • [45]Sambrook J, Russell DW: Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory. Vol 1 3rd edition. 2001, p 6.4. Chapter 6
  • [46]Huynen L, Millar CD, Scofield RP, Lambert DM: Nuclear DNA sequences detect species limits in ancient moa. Nature 2003, 425:175-178.
  • [47]Cooper A, Poinar HN: Ancient DNA: Do it right or not at all. Science 2000, 289:1139.
  • [48]Suzuki T, Ogura T: Congenic method in the chick limb buds by electroporation. Dev Growth Differ 2008, 50:459-465.
  • [49]Suzuki T, Hasso SM, Fallon JF: Unique SMAD1/5/8 activity at the phalanx-forming region determines digit identity. Proc Natl Acad Sci U S A 2008, 105:4185-4190.
  • [50]Murakami M, Nakagawa M, Olson EN, Nakagawa O: A WW domain protein TAZ is a critical coactivator for Tbx5, a transcription factor implicated in Holt-Oram syndrome. Proc Natl Acad Sci U S A 2005, 102:18034-18039.
  • [51]Kawakami Y, Capdevila J, Buscher D, Itoh T, Esteban CR, Izpisua-Belmonte JC: WNT signals control FGF-dependent limb initiation and AER induction in the chick embryo. Cell 2001, 104:891-900.
  • [52]Kulisz A, Simon HG: An evolutionarily conserved nuclear export signal facilitates cytoplasmic localization of the Tbx5 transcription factor. Mol and Cell Biol 2008, 28:1553-1564.
  • [53]Zaragoza MV, Lewis LE, Sun G, Wang E, Li L, Said-Salman I, Feucht L, Huang T: Identification of the TBX5 transactivating domain and the nuclear localization signal. Gene 2004, 330:9-18.
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