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PMID: 19503786 Published · epublish English Journal Article Research Support, Non-U.S. Gov't

Evolution of the B3 DNA binding superfamily: new insights into REM family gene diversification.

PloS one ·Vol. 4 ·No. 6 ·2009-06-08 ·Pages e5791

Romanel EA, Schrago CG, Couñago RM, Russo CA, Alves-Ferreira M

Abstract

The B3 DNA binding domain includes five families: auxin response factor (ARF), abscisic acid-insensitive3 (ABI3), high level expression of sugar inducible (HSI), related to ABI3/VP1 (RAV) and reproductive meristem (REM). The release of the complete genomes of the angiosperm eudicots Arabidopsis thaliana and Populus trichocarpa, the monocot Orysa sativa, the bryophyte Physcomitrella patens,the green algae Chlamydomonas reinhardtii and Volvox carteri and the red algae Cyanidioschyzon melorae provided an exceptional opportunity to study the evolution of this superfamily. In order to better understand the origin and the diversification of B3 domains in plants, we combined comparative phylogenetic analysis with exon/intron structure and duplication events. In addition, we investigated the conservation and divergence of the B3 domain during the origin and evolution of each family. Our data indicate that showed that the B3 containing genes have undergone extensive duplication events, and that the REM family B3 domain has a highly diverged DNA binding. Our results also indicate that the founding member of the B3 gene family is likely to be similar to the ABI3/HSI genes found in C. reinhardtii and V. carteri. Among the B3 families, ABI3, HSI, RAV and ARF are most structurally conserved, whereas the REM family has experienced a rapid divergence. These results are discussed in light of their functional and evolutionary roles in plant development.

MeSH Terms
Arabidopsis/chemistry,genetics Arabidopsis Proteins/chemistry,genetics Biological Evolution Eukaryota/genetics Evolution, Molecular Gene Duplication Genes, Plant Molecular Sequence Data Multigene Family Phylogeny Plant Physiological Phenomena Plant Proteins Protein Conformation Protein Structure, Tertiary Zea mays/chemistry,genetics
Chemicals
Arabidopsis Proteins Plant Proteins
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Romanel Elisson A C
Department of Genetics, Federal University of Rio de Janeiro, Rio de Janeiro, Brazil.
Schrago Carlos G
Couñago Rafael M
Russo Claudia A M
Alves-Ferreira Márcio
References (84)
84 references, click to expand
  1. The balance between CONSTANS and TEMPRANILLO activities determines FT expression to trigger flowering.
    Curr Biol. 2008 Sep 9;18(17):1338-43 PMID: 18718758
  2. The conserved B3 domain of VIVIPAROUS1 has a cooperative DNA binding activity.
    Plant Cell. 1997 May;9(5):799-807 PMID: 9165754
  3. The neighbor-joining method: a new method for reconstructing phylogenetic trees.
    Mol Biol Evol. 1987 Jul;4(4):406-25 PMID: 3447015
  4. Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements.
    Plant Cell. 1997 Nov;9(11):1963-71 PMID: 9401121
  5. Regulation of AUXIN RESPONSE FACTOR3 by TAS3 ta-siRNA affects developmental timing and patterning in Arabidopsis.
    Curr Biol. 2006 May 9;16(9):939-44 PMID: 16682356
  6. EST data suggest that poplar is an ancient polyploid.
    New Phytol. 2005 Jul;167(1):165-70 PMID: 15948839
  7. Chlamydomonas reinhardtii genome project. A guide to the generation and use of the cDNA information.
    Plant Physiol. 2003 Feb;131(2):401-8 PMID: 12586865
  8. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions.
    Acta Crystallogr D Biol Crystallogr. 2004 Dec;60(Pt 12 Pt 1):2256-68 PMID: 15572779
  9. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana.
    Nature. 2000 Dec 14;408(6814):796-815 PMID: 11130711
  10. Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D.
    Nature. 2004 Apr 8;428(6983):653-7 PMID: 15071595
  11. Auxin response factors.
    Curr Opin Plant Biol. 2007 Oct;10(5):453-60 PMID: 17900969
  12. AtREM1, a member of a new family of B3 domain-containing genes, is preferentially expressed in reproductive meristems.
    Plant Physiol. 2002 Feb;128(2):418-27 PMID: 11842146
  13. Searching tRNA sequences for relatedness to aminoacyl-tRNA synthetase families.
    J Mol Evol. 1995 May;40(5):482-6 PMID: 7783223
  14. Characterization and functional analysis of ABSCISIC ACID INSENSITIVE3-like genes from Physcomitrella patens.
    Plant J. 2006 Jun;46(6):1032-44 PMID: 16805735
  15. The Pfam protein families database.
    Nucleic Acids Res. 2002 Jan 1;30(1):276-80 PMID: 11752314
  16. Protein secondary structure prediction based on position-specific scoring matrices.
    J Mol Biol. 1999 Sep 17;292(2):195-202 PMID: 10493868
  17. The PSIPRED protein structure prediction server.
    Bioinformatics. 2000 Apr;16(4):404-5 PMID: 10869041
  18. The plant B3 superfamily.
    Trends Plant Sci. 2008 Dec;13(12):647-55 PMID: 18986826
  19. A gene expression map of Arabidopsis thaliana development.
    Nat Genet. 2005 May;37(5):501-6 PMID: 15806101
  20. MIPS Arabidopsis thaliana Database (MAtDB): an integrated biological knowledge resource based on the first complete plant genome.
    Nucleic Acids Res. 2002 Jan 1;30(1):91-3 PMID: 11752263
  21. An ancient genome duplication contributed to the abundance of metabolic genes in the moss Physcomitrella patens.
    BMC Evol Biol. 2007 Aug 02;7:130 PMID: 17683536
  22. A draft sequence of the rice genome (Oryza sativa L. ssp. japonica).
    Science. 2002 Apr 5;296(5565):92-100 PMID: 11935018
  23. Global expression profiling applied to the analysis of Arabidopsis stamen development.
    Plant Physiol. 2007 Nov;145(3):747-62 PMID: 17905860
  24. The Chlamydomonas genome reveals the evolution of key animal and plant functions.
    Science. 2007 Oct 12;318(5848):245-50 PMID: 17932292
  25. Protein structure prediction servers at University College London.
    Nucleic Acids Res. 2005 Jul 1;33(Web Server issue):W36-8 PMID: 15980489
  26. ETTIN patterns the Arabidopsis floral meristem and reproductive organs.
    Development. 1997 Nov;124(22):4481-91 PMID: 9409666
  27. The closest living relatives of land plants.
    Science. 2001 Dec 14;294(5550):2351-3 PMID: 11743201
  28. Transcriptional program controlled by the floral homeotic gene AGAMOUS during early organogenesis.
    Development. 2005 Feb;132(3):429-38 PMID: 15634696
  29. Arabidopsis RAV1 is down-regulated by brassinosteroid and may act as a negative regulator during plant development.
    Cell Res. 2004 Feb;14(1):8-15 PMID: 15040885
  30. Expansion of protein domain repeats.
    PLoS Comput Biol. 2006 Aug 25;2(8):e114 PMID: 16933986
  31. ProtTest: selection of best-fit models of protein evolution.
    Bioinformatics. 2005 May 1;21(9):2104-5 PMID: 15647292
  32. MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes.
    Plant Cell. 2005 May;17(5):1360-75 PMID: 15829600
  33. A genomic perspective on protein families.
    Science. 1997 Oct 24;278(5338):631-7 PMID: 9381173
  34. Assessing protein structures with a non-local atomic interaction energy.
    J Mol Biol. 1998 Apr 17;277(5):1141-52 PMID: 9571028
  35. Expresso: automatic incorporation of structural information in multiple sequence alignments using 3D-Coffee.
    Nucleic Acids Res. 2006 Jul 1;34(Web Server issue):W604-8 PMID: 16845081
  36. Solution structure of the B3 DNA binding domain of the Arabidopsis cold-responsive transcription factor RAV1.
    Plant Cell. 2004 Dec;16(12):3448-59 PMID: 15548737
  37. Gene regulation during late embryogenesis: the RY motif of maturation-specific gene promoters is a direct target of the FUS3 gene product.
    Plant J. 2000 Mar;21(5):401-8 PMID: 10758492
  38. Expression pattern shifts following duplication indicative of subfunctionalization and neofunctionalization in regulatory genes of Arabidopsis.
    Mol Biol Evol. 2006 Feb;23(2):469-78 PMID: 16280546
  39. Endogenous and synthetic microRNAs stimulate simultaneous, efficient, and localized regulation of multiple targets in diverse species.
    Plant Cell. 2006 May;18(5):1134-51 PMID: 16603651
  40. Isolation of the Arabidopsis ABI3 gene by positional cloning.
    Plant Cell. 1992 Oct;4(10):1251-61 PMID: 1359917
  41. Comparative genomics of Physcomitrella patens gametophytic transcriptome and Arabidopsis thaliana: implication for land plant evolution.
    Proc Natl Acad Sci U S A. 2003 Jun 24;100(13):8007-12 PMID: 12808149
  42. Distance-scaled, finite ideal-gas reference state improves structure-derived potentials of mean force for structure selection and stability prediction.
    Protein Sci. 2002 Nov;11(11):2714-26 PMID: 12381853
  43. Differential activation of ABI3 and LEA genes upon plant parasitic nematode infection.
    Mol Plant Pathol. 2005 May 1;6(3):321-5 PMID: 20565660
  44. Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes.
    Plant Cell. 2004 Jul;16(7):1667-78 PMID: 15208399
  45. The POU domain: versatility in transcriptional regulation by a flexible two-in-one DNA-binding domain.
    Genes Dev. 1995 Jul 15;9(14):1679-93 PMID: 7622033
  46. Structures and evolutionary origins of plant-specific transcription factor DNA-binding domains.
    Plant Physiol Biochem. 2008 Mar;46(3):394-401 PMID: 18272381
  47. Interaction of PvALF and VP1 B3 domains with the beta -phaseolin promoter.
    Plant Mol Biol. 2004 May;55(2):221-37 PMID: 15604677
  48. Seven newly discovered intron positions in the triose-phosphate isomerase gene: evidence for the introns-late theory.
    Proc Natl Acad Sci U S A. 1995 Aug 29;92(18):8507-11 PMID: 7667320
  49. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling.
    Bioinformatics. 2006 Jan 15;22(2):195-201 PMID: 16301204
  50. Widespread genome duplications throughout the history of flowering plants.
    Genome Res. 2006 Jun;16(6):738-49 PMID: 16702410
  51. From endonucleases to transcription factors: evolution of the AP2 DNA binding domain in plants.
    Plant Cell. 2004 Sep;16(9):2265-77 PMID: 15319480
  52. Identification of correct regions in protein models using structural, alignment, and consensus information.
    Protein Sci. 2006 Apr;15(4):900-13 PMID: 16522791
  53. Multiple roles of Arabidopsis VRN1 in vernalization and flowering time control.
    Science. 2002 Jul 12;297(5579):243-6 PMID: 12114624
  54. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray).
    Science. 2006 Sep 15;313(5793):1596-604 PMID: 16973872
  55. LHP1, the Arabidopsis homologue of HETEROCHROMATIN PROTEIN1, is required for epigenetic silencing of FLC.
    Proc Natl Acad Sci U S A. 2006 Mar 28;103(13):5012-7 PMID: 16549797
  56. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0.
    Mol Biol Evol. 2007 Aug;24(8):1596-9 PMID: 17488738
  57. Structure of the B3 domain from Arabidopsis thaliana protein At1g16640.
    Protein Sci. 2005 Sep;14(9):2478-83 PMID: 16081658
  58. Repression of the LEAFY COTYLEDON 1/B3 regulatory network in plant embryo development by VP1/ABSCISIC ACID INSENSITIVE 3-LIKE B3 genes.
    Plant Physiol. 2007 Feb;143(2):902-11 PMID: 17158584
  59. Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3.
    Nature. 2004 Jan 8;427(6970):159-64 PMID: 14712276
  60. Seed-specific transcription factors ABI3 and FUS3: molecular interaction with DNA.
    Planta. 2004 May;219(1):158-66 PMID: 14767767
  61. A recent polyploidy superimposed on older large-scale duplications in the Arabidopsis genome.
    Genome Res. 2003 Feb;13(2):137-44 PMID: 12566392
  62. The transcription factor FUSCA3 controls developmental timing in Arabidopsis through the hormones gibberellin and abscisic acid.
    Dev Cell. 2004 Sep;7(3):373-85 PMID: 15363412
  63. Protein structure homology modeling using SWISS-MODEL workspace.
    Nat Protoc. 2009;4(1):1-13 PMID: 19131951
  64. The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants.
    Science. 2008 Jan 4;319(5859):64-9 PMID: 18079367
  65. AtGA3ox2, a key gene responsible for bioactive gibberellin biosynthesis, is regulated during embryogenesis by LEAFY COTYLEDON2 and FUSCA3 in Arabidopsis.
    Plant Physiol. 2004 Nov;136(3):3660-9 PMID: 15516508
  66. Analysis of a sugar response mutant of Arabidopsis identified a novel B3 domain protein that functions as an active transcriptional repressor.
    Plant Physiol. 2005 Jun;138(2):675-85 PMID: 15894743
  67. Activation and repression of transcription by auxin-response factors.
    Proc Natl Acad Sci U S A. 1999 May 11;96(10):5844-9 PMID: 10318972
  68. LEAFY COTYLEDON2 encodes a B3 domain transcription factor that induces embryo development.
    Proc Natl Acad Sci U S A. 2001 Sep 25;98(20):11806-11 PMID: 11573014
  69. Knowing when to grow: signals regulating bud dormancy.
    Trends Plant Sci. 2003 Nov;8(11):534-40 PMID: 14607098
  70. Knowledge-based protein secondary structure assignment.
    Proteins. 1995 Dec;23(4):566-79 PMID: 8749853
  71. Expression of the gene encoding transcription factor PaVP1 differs in Picea abies embryogenic lines depending on their ability to develop somatic embryos.
    Plant Cell Rep. 2008 Mar;27(3):435-41 PMID: 17968553
  72. Embedding strategies for effective use of information from multiple sequence alignments.
    Protein Sci. 1997 Mar;6(3):698-705 PMID: 9070452
  73. Genome duplication and the origin of angiosperms.
    Trends Ecol Evol. 2005 Nov;20(11):591-7 PMID: 16701441
  74. RAV1, a novel DNA-binding protein, binds to bipartite recognition sequence through two distinct DNA-binding domains uniquely found in higher plants.
    Nucleic Acids Res. 1999 Jan 15;27(2):470-8 PMID: 9862967
  75. Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics.
    Proc Natl Acad Sci U S A. 2004 Jun 29;101(26):9903-8 PMID: 15161969
  76. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
    Nucleic Acids Res. 1994 Nov 11;22(22):4673-80 PMID: 7984417
  77. Deciphering gene regulatory networks that control seed development and maturation in Arabidopsis.
    Plant J. 2008 May;54(4):608-20 PMID: 18476867
  78. Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae).
    Mol Biol Evol. 2000 Oct;17(10):1483-98 PMID: 11018155
  79. Genome-wide analysis of gene expression during early Arabidopsis flower development.
    PLoS Genet. 2006 Jul;2(7):e117 PMID: 16789830
  80. Substitution rate comparisons between grasses and palms: synonymous rate differences at the nuclear gene Adh parallel rate differences at the plastid gene rbcL.
    Proc Natl Acad Sci U S A. 1996 Sep 17;93(19):10274-9 PMID: 8816790
  81. The rapid generation of mutation data matrices from protein sequences.
    Comput Appl Biosci. 1992 Jun;8(3):275-82 PMID: 1633570
  82. Epigenetic maintenance of the vernalized state in Arabidopsis thaliana requires LIKE HETEROCHROMATIN PROTEIN 1.
    Nat Genet. 2006 Jun;38(6):706-10 PMID: 16682972
  83. The map-based sequence of the rice genome.
    Nature. 2005 Aug 11;436(7052):793-800 PMID: 16100779
  84. New Drosophila introns originate by duplication.
    Proc Natl Acad Sci U S A. 1998 Feb 17;95(4):1658-62 PMID: 9465072
Article Info
Journal
PloS one
Abbr.
PLoS One
ISSN
1932-6203
Published
2009-06-08
Epub
2009-00-08
Pages
e5791
Language
English
Region
United States
NLM ID
101285081
PMCID
PMC2688026
Subset
IM
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