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Phylogenetic Analysis of Plant Basic Helix-Loop-Helix Proteins

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Abstract

The basic helix-loop-helix (bHLH) family of proteins is a group of functionally diverse transcription factors found in both plants and animals. These proteins evolved early in eukaryotic cells before the split of animals and plants, but appear to function in ‘plant-specific’ or ‘animal-specific’ processes. In animals bHLH proteins are involved in regulation of a wide variety of essential developmental processes. On the contrary, bHLH proteins have not been extensively studied in plants. Those that have been characterized function in anthocyanin biosynthesis, phytochrome signaling, globulin expression, fruit dehiscence, carpel and epidermal development. We have identified 118 different bHLH genes in the completely sequenced Arabidopsis thaliana genome and 131 bHLH genes in the rice genome. Here we report a phylogenetic analysis of these genes, including 46 genes from other plant species and a classification of these proteins into 15 distinct plant clades. Results imply a polyphyletic origin for the plant bHLH proteins related only by their bHLH DNA binding motif. We suggest that plant bHLH proteins are under weaker selective constraints than their animal counterparts and that lineage specific expansions and subfunctionalization have fashioned regulatory proteins for plant specific functions.

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References

  1. SF Altschul TL Madden AA Schaffer J Zhang Z Zhang W Miller DJ Lipman (1997) ArticleTitleGapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25 3389–3402 Occurrence Handle9254694

    PubMed  Google Scholar 

  2. WR Atchley WM Fitch (1997) ArticleTitleA natural classification of the basic helix-loop-helix class of transcription factors. Proc Natl Acad Sci USA 94 5172–5176 Occurrence Handle1:CAS:528:DyaK2sXjtlalurk%3D Occurrence Handle9144210

    CAS  PubMed  Google Scholar 

  3. WR Atchley W Terhalle A Dress (1999) ArticleTitlePositional dependence, cliques, and predictive motifs in the bHLH protein domain. J Mol Evol 48 501–516 Occurrence Handle1:CAS:528:DyaK1MXisFGisrc%3D Occurrence Handle10198117

    CAS  PubMed  Google Scholar 

  4. SG Bacsi O Hankinson (1996) ArticleTitleFunctional characterization of DNA-binding domains of the subunits of the heterodimeric aryl hydrocarbon receptor complex imputing novel and canonical basic helix-loop-helix protein-DNA interactions. J Biol Chem 271 8843–8850 Occurrence Handle1:CAS:528:DyaK28Xitlentrw%3D Occurrence Handle8621524

    CAS  PubMed  Google Scholar 

  5. S de Pater K Pham J Memelink J Kijne (1997) ArticleTitleRAP-1 is an Arabidopsis MYC-like R protein homologue, that binds to G-box sequence motifs. Plant Mol Biol 34 169–174 Occurrence Handle1:CAS:528:DyaK2sXjs1OnurY%3D Occurrence Handle9177323

    CAS  PubMed  Google Scholar 

  6. A Dommelen R De Mot J Vanderleyden (2001) ArticleTitleAmmonium transport: unifying concepts and unique aspects. Australian J Plant Physiol 28 959–967

    Google Scholar 

  7. P Elomaa M Mehto M Kotilainen Y Helariutta L Nevalainen TH Teeri (1998) ArticleTitleA bHLH transcription factor mediates organ, region and flower type specific signals on dihydroflavonol-4-reductase (dfr) gene expression in the inflorescence of Gerbera hybrida (Asteraceae). Plant J 16 93–99 Occurrence Handle1:CAS:528:DyaK1cXntFOnsb0%3D Occurrence Handle9807831

    CAS  PubMed  Google Scholar 

  8. Felsenstein J (1993) PHYLIP (Phytogeny Inference Package). Distributed by the author

  9. AR Ferre-D’Amare GC Prendergast EB Ziff SK Burley (1993) ArticleTitleRecognition by Max of its cognate DNA through a dimeric b/HLH/Z domain. Nature 363 38–45 Occurrence Handle8479534

    PubMed  Google Scholar 

  10. A Fisher M Caudy (1998) ArticleTitleThe function of hairy-related bHLH repressor proteins in cell fate decisions. Bioessays 20 298–306 Occurrence Handle10.1002/(SICI)1521-1878(199804)20:4<298::AID-BIES6>3.0.CO;2-M Occurrence Handle1:STN:280:DyaK1c3ot1ylsg%3D%3D Occurrence Handle9619101

    Article  CAS  PubMed  Google Scholar 

  11. R Foster T Izawa NH Chua (1994) ArticleTitlePlant bZIP proteins gather at ACGT elements. Faseb J 8 192–200 Occurrence Handle1:CAS:528:DyaK2cXitlOisLw%3D Occurrence Handle8119490

    CAS  PubMed  Google Scholar 

  12. J Garrell S Campuzano (1991) ArticleTitleThe helix-loop-helix domain: a common motif for bristles, muscles and sex. Bioessays 13 493–498 Occurrence Handle1:CAS:528:DyaK38Xht1egsLc%3D Occurrence Handle1755826

    CAS  PubMed  Google Scholar 

  13. SA Goff KC Cone VL Chandler (1992) ArticleTitleFunctional analysis of the transcriptional activator encoded by the maize B gene: evidence for a direct functional interaction between two classes of regulatory proteins. Genes Dev 6 864–875 Occurrence Handle1:CAS:528:DyaK38Xkt1Wns7s%3D Occurrence Handle1577278

    CAS  PubMed  Google Scholar 

  14. J Goodrich R Carpenter ES Coen (1992) ArticleTitleA common gene regulates pigmentation pattern in diverse plant species. Cell 68 955–964 Occurrence Handle1:CAS:528:DyaK3sXhvVCqtL8%3D Occurrence Handle1547495

    CAS  PubMed  Google Scholar 

  15. MG Heisler A Atkinson YH Bylstra R Walsh DR Smyth (2001) ArticleTitle SPATULA, a gene that controls development of carpel margin tissues in Arabidopsis, encodes a bHLH protein. Development 128 1089–1098 Occurrence Handle1:CAS:528:DC%2BD3MXjtFOlt7o%3D Occurrence Handle11245574

    CAS  PubMed  Google Scholar 

  16. S Henikoff JG Henikoff (1992) ArticleTitleAmino acid substitution matrices from protein blocks. PNAS 89 10915–10919 Occurrence Handle1:CAS:528:DyaK3sXjsFCgsQ%3D%3D Occurrence Handle1438297

    CAS  PubMed  Google Scholar 

  17. J Hu VS Reddy SR Wessler (2000) ArticleTitleThe rice R gene family: two distinct subfamilies containing several miniature inverted-repeat transposable elements. Plant Mol Biol 42 667–678 Occurrence Handle1:CAS:528:DC%2BD3cXjt1Grtr8%3D Occurrence Handle10809440

    CAS  PubMed  Google Scholar 

  18. BN Kaiser PM Finnegan SD Tyerman LF Whitehead FJ Bergersen DA Day MK Udvardi (1998) ArticleTitleCharacterization of an ammonium transport protein from the peribacteroid membrane of soybean nodules. Science 281 1202–1206 Occurrence Handle10.1126/science.281.5380.1202 Occurrence Handle1:CAS:528:DyaK1cXls1Gju78%3D Occurrence Handle9712587

    Article  CAS  PubMed  Google Scholar 

  19. R Kageyama M Ishibashi K Takebayashi K Tomita (1997) ArticleTitlebHLH transcription factors and mammalian neuronal differentiation. Int J Biochem Cell Biol 29 1389–1399 Occurrence Handle1:CAS:528:DyaK1cXitlOhu7c%3D Occurrence Handle9570134

    CAS  PubMed  Google Scholar 

  20. R Kageyama T Ohtsuka K Tomita (2000) ArticleTitleThe bHLH gene Hes1 regulates differentiation of multiple cell types. Mol Cells 10 1–7 Occurrence Handle1:CAS:528:DC%2BD3cXhvFSju7o%3D Occurrence Handle10774739

    CAS  PubMed  Google Scholar 

  21. Y Kawagoe N Murai (1996) ArticleTitleA novel basic region/helix-loop-helix protein binds to a G-box motif CACGTG of the bean seed storage protein B-phaseolin gene. Plant Science 116 47–57 Occurrence Handle1:CAS:528:DyaK28XitlGhsbc%3D

    CAS  Google Scholar 

  22. S Kosugi Y Ohashi (1997) ArticleTitlePCF1 and PCF2 specifically bind to cis elements in the rice proliferating cell nuclear antigen gene. Plant Cell 9 1607–1619 Occurrence Handle1:CAS:528:DyaK2sXmsFeltLs%3D Occurrence Handle9338963

    CAS  PubMed  Google Scholar 

  23. A Lawton-Rauh (2003) ArticleTitleEvolutionary dynamics of duplicated genes in plants. Mol Phylogen Evol

    Google Scholar 

  24. V Ledent O Paquet M Vervoort (2002) ArticleTitlePhylogenetic analysis of the human basic helix-loop-helix proteins. Genome Biol 3 research 0030.1–0030.18

    Google Scholar 

  25. V Ledent M Vervoort (2001) ArticleTitleThe basic helix-loop-helix protein family: comparative genomics and phylogenetic analysis. Genome Res 11 754–770 Occurrence Handle1:CAS:528:DC%2BD3MXjs1Wmuro%3D Occurrence Handle11337472

    CAS  PubMed  Google Scholar 

  26. O Lespinet YI Wolf EV Koonin L Aravind (2002) ArticleTitleThe role of lineage-specific gene family expansion in the evolution of eukaryotes. Genome Res 12 1048–1059 Occurrence Handle1:CAS:528:DC%2BD38XlsVWgsr4%3D Occurrence Handle12097341

    CAS  PubMed  Google Scholar 

  27. C Loulergue M Lebrun JF Briat (1998) ArticleTitleExpression cloning in Fe2+ transport defective yeast of a novel maize MYC transcription factor. Gene 225 47–57 Occurrence Handle1:CAS:528:DyaK1MXns1Gjtg%3D%3D Occurrence Handle9931428

    CAS  PubMed  Google Scholar 

  28. M Lynch A Force (2000) ArticleTitleThe probability of duplicate gene preservation by subfunctionalization. Genetics 154 459–473 Occurrence Handle1:CAS:528:DC%2BD3cXms1KhsA%3D%3D Occurrence Handle10629003

    CAS  PubMed  Google Scholar 

  29. C Martin J Paz-Ares (1997) ArticleTitleMYB transcription factors in plants. Trends Genet 13 67–73 Occurrence Handle1:CAS:528:DyaK2sXhtFOqs78%3D Occurrence Handle9055608

    CAS  PubMed  Google Scholar 

  30. JF Martinez-Garcia E Huq PH Quail (2000) ArticleTitleDirect targeting of light signals to a promoter element-bound transcription factor. Science 288 859–863

    Google Scholar 

  31. ME Massari C Murre (2000) ArticleTitleHelix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol Cell Biol 20 429–440 Occurrence Handle1:CAS:528:DC%2BD3cXjtVKnsg%3D%3D Occurrence Handle10611221

    CAS  PubMed  Google Scholar 

  32. J Mol E Grotewold R Koes (1998) ArticleTitleHow genes paint flowers and seeds. Trend Plant Sci 3 212–217

    Google Scholar 

  33. B Morgenstern (1999) ArticleTitleDIALIGN 2: improvement of the segment-to-segment approach to multiple sequence alignment. Bioinformatics 15 211–218 Occurrence Handle10.1093/bioinformatics/15.3.211 Occurrence Handle1:CAS:528:DyaK1MXjs1artrc%3D Occurrence Handle10222408

    Article  CAS  PubMed  Google Scholar 

  34. B Morgenstern WR Atchley (1999) ArticleTitleEvolution of bHLH transcription factors: modular evolution by domain shuffling? Mol Biol Evol 16 1654–1663 Occurrence Handle1:CAS:528:DyaK1MXnvF2nsr4%3D Occurrence Handle10605108

    CAS  PubMed  Google Scholar 

  35. CT Payne F Zhang AM Lloyd (2000) ArticleTitleGL3 encodes a bHLH protein that regulates trichome development in arabidopsis through interaction with GL1 and TTG1. Genetics 156 1349–1362

    Google Scholar 

  36. FB Pickett DR Meeks-Wagner (1995) ArticleTitleSeeing double: appreciating genetic redundancy. Plant Cell 7 1347–1356

    Google Scholar 

  37. MD Purugganan SR Wessler (1994) ArticleTitleMolecular evolution of the plant R regulatory gene family. Genetics 138 849–854 Occurrence Handle1:CAS:528:DyaK28XitlKhsg%3D%3D Occurrence Handle7851779

    CAS  PubMed  Google Scholar 

  38. PH Quail (2000) ArticleTitlePhytochrome-interacting factors. Semin Cell Dev Biol 11 457–466

    Google Scholar 

  39. S Rajani V Sundaresan (2001) ArticleTitleThe Arabidopsis myc/bHLH gene ALCATRAZ enables cell separation in fruit dehiscence. Curr Biol 11 1914–1922 Occurrence Handle1:CAS:528:DC%2BD38XisFCq Occurrence Handle11747817

    CAS  PubMed  Google Scholar 

  40. JA Rosinski WR Atchley (1998) ArticleTitleMolecular evolution of the Myb family of transcription factors: evidence for polyphyletic origin. J Mol Evol 46 74–83 Occurrence Handle1:CAS:528:DyaK1cXks1akuw%3D%3D Occurrence Handle9419227

    CAS  PubMed  Google Scholar 

  41. MB Sainz E Grotewold VL Chandler (1997) ArticleTitleEvidence for direct activation of an anthocyanin promoter by the maize C1 protein and comparison of DNA binding by related Myb domain proteins. Plant Cell 9 611–625 Occurrence Handle1:CAS:528:DyaK2sXivFCrsrY%3D Occurrence Handle9144964

    CAS  PubMed  Google Scholar 

  42. N Saitou M Nei (1987) ArticleTitleThe neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4 406–425 Occurrence Handle1:STN:280:BieC1cbgtVY%3D Occurrence Handle3447015

    CAS  PubMed  Google Scholar 

  43. MS Soh YM Kirn SJ Han PS Song (2000) ArticleTitleREP1, a basic helix-loop-helix protein, is required for a branch pathway of phytochrome A signaling in arabidopsis. Plant Cell 12 2061–2074 Occurrence Handle1:CAS:528:DC%2BD3MXos1Gm Occurrence Handle11090209

    CAS  PubMed  Google Scholar 

  44. C Spelt F Quattrocchio JN Mol R Koes (2000) ArticleTitleAnthocyanin1 of petunia encodes a basic helix-loop-helix protein that directly activates transcription of structural anthocyanin genes. Plant Cell 12 1619–1632 Occurrence Handle1:CAS:528:DC%2BD3cXnsVyltro%3D Occurrence Handle11006336

    CAS  PubMed  Google Scholar 

  45. D Srivastava (1999) ArticleTitleHAND proteins: molecular mediators of cardiac development and congenital heart disease. Trends Cardiovasc Med 9 11–18 Occurrence Handle1:CAS:528:DyaK1MXitFGksLk%3D Occurrence Handle10189962

    CAS  PubMed  Google Scholar 

  46. C Steidl C Leimeister B Klamt M Maier I Nanda M Dixon et al. (2000) ArticleTitleCharacterization of the human and mouse HEY1, HEY2, and HEYL genes: cloning, mapping, and mutation screening of a new bHLH gene family. Genomics 66 195–203 Occurrence Handle1:CAS:528:DC%2BD3cXktVKnu7k%3D Occurrence Handle10860664

    CAS  PubMed  Google Scholar 

  47. R Stracke M Werber B Weisshaar (2001) ArticleTitleThe R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol 4 447–456 Occurrence Handle10.1016/S1369-5266(00)00199-0 Occurrence Handle1:CAS:528:DC%2BD3MXmvFKgt74%3D Occurrence Handle11597504

    Article  CAS  PubMed  Google Scholar 

  48. K Strimmer Av Haeseler (1996) ArticleTitleQuatet puzzling: a quartet maximum likelihood method for reconstruction tree topologies. Mol Biol Evol 13 964–969 Occurrence Handle1:CAS:528:DyaK28XltlSmsLk%3D

    CAS  Google Scholar 

  49. AR Walker PA Davison AC Bolognesi-Winfield CM James N Srinivasan TL Blundell et al. (1999) ArticleTitleThe TRANSPARENT TESTA GLABRA1 locus, which regulates trichome differentiation and anthocyanin biosynthesis in Arabidopsis, encodes a WD40 repeat protein. Plant Cell 11 1337–1350

    Google Scholar 

  50. B Weisshaar GI Jenkins (1998) ArticleTitlePhenylpropanoid biosynthesis and its regulation. Curr Opin Plant Biol 1 251–257 Occurrence Handle1:CAS:528:DyaK1cXktFaku7k%3D Occurrence Handle10066590

    CAS  PubMed  Google Scholar 

  51. KH Wolfe DC Shields (1997) ArticleTitleMolecular evidence for an ancient duplication of the entire yeast genome. Nature 387 708–713 Occurrence Handle1:STN:280:ByiA3snhtVU%3D Occurrence Handle9192896

    CAS  PubMed  Google Scholar 

  52. WE Wright (1992) ArticleTitleMuscle basic helix-loop-helix proteins and the regulation of myogenesis. Curr Opin Genet Dev 2 243–248 Occurrence Handle1:CAS:528:DyaK38Xkt1elsb4%3D Occurrence Handle1638118

    CAS  PubMed  Google Scholar 

  53. J Yu S Hu J Wang GK Wong S Li B Liu et al. (2002) ArticleTitleA draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296 79–92

    Google Scholar 

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Acknowledgements

Thanks to Maria Tsompana, Michael Purugganan, and two anonymous reviewers for constructive comments. Supported by NIH grant GM45344.

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  1. Department of Genetics and The Center for Computational Biology, North Carolina State University, Campus Box 7614, Raleigh, NC 27695-7614, USA

    Michael J. Buck & William R. Atchley

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Buck, M.J., Atchley, W.R. Phylogenetic Analysis of Plant Basic Helix-Loop-Helix Proteins . J Mol Evol 56, 742–750 (2003). https://doi.org/10.1007/s00239-002-2449-3

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