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PMID: 18813954 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Systematic sequence analysis and identification of tissue-specific or stress-responsive genes of NAC transcription factor family in rice.

Molecular genetics and genomics : MGG ·Vol. 280 ·No. 6 ·2008-12-00 ·Pages 547-63

Fang Y, You J, Xie K, Xie W, Xiong L

Abstract

NAM, ATAF, and CUC (NAC) transcription factors comprise a large plant-specific gene family and a few members of this family have been characterized for their roles in plant growth, development, and stress tolerance. In this study, systematic sequence analysis revealed 140 putative NAC or NAC-like genes (ONAC) in rice. Phylogenetic analysis suggested that NAC family can be divided into five groups (I-V). Among them, all the published development-related genes fell into group I, and all the published stress-related NAC genes fell into the group III (namely stress-responsive NAC genes, SNAC). Distinct compositions of the putative motifs were revealed on the basis of NAC protein sequences in rice. Most members contained a complete NAC DNA-binding domain and a variable transcriptional regulation domain. Sequence analysis, together with the organization of putative motifs, indicated distinct structures and potential diverse functions of NAC family in rice. Yeast one-hybrid analysis confirmed that 12 NAC proteins representing different motif compositions can bind the NAC core DNA-binding site. Real-time polymerase chain reaction (PCR) analysis revealed 12 genes with different tissue-specific (such as callus, root, stamen, or immature endosperm) expression patterns, suggesting that these genes may play crucial regulatory roles during growth and development of rice. The expression levels of this family were also checked under various abiotic stresses including drought, salinity, and low temperature. A preliminary check based on our microarray data suggested that more than 40 genes of this family were responsive to drought and/or salt stresses. Among them, 20 genes were further investigated for their stress responsiveness in detail by real-time PCR analysis. Most of these stress-responsive genes belonged to the group III (SNAC). Considering the fact that a very limited number of genes of the NAC family have been characterized, our data provide a very useful reference for functional analysis of this family in rice.

MeSH Terms
Amino Acid Motifs Amino Acid Sequence Base Sequence Computational Biology Gene Expression Profiling Gene Expression Regulation, Plant Genes, Plant Molecular Sequence Data Organ Specificity/genetics Oryza/genetics Phylogeny Plant Proteins/chemistry,genetics,metabolism Regulatory Sequences, Nucleic Acid/genetics Reverse Transcriptase Polymerase Chain Reaction Sequence Analysis, DNA Stress, Physiological/genetics Transcription Factors/genetics,metabolism Two-Hybrid System Techniques
Chemicals
Plant Proteins Transcription Factors
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Fang Yujie
National Center of Plant Gene Research, Huazhong Agricultural University, 430070, Wuhan, China.
You Jun
Xie Kabin
Xie Weibo
Xiong Lizhong
References (61)
61 references, click to expand
  1. Interactions between plant RING-H2 and plant-specific NAC (NAM/ATAF1/2/CUC2) proteins: RING-H2 molecular specificity and cellular localization.
    Biochem J. 2003 Apr 1;371(Pt 1):97-108 PMID: 12646039
  2. Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor.
    Nat Biotechnol. 1999 Mar;17(3):287-91 PMID: 10096298
  3. Transcription factors in rice: a genome-wide comparative analysis between monocots and eudicots.
    Plant Mol Biol. 2005 Sep;59(1):191-203 PMID: 16217612
  4. GRAB proteins, novel members of the NAC domain family, isolated by their interaction with a geminivirus protein.
    Plant Mol Biol. 1999 Mar;39(4):647-56 PMID: 10350080
  5. Structure of the conserved domain of ANAC, a member of the NAC family of transcription factors.
    EMBO Rep. 2004 Mar;5(3):297-303 PMID: 15083810
  6. A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway.
    Plant J. 2004 Sep;39(6):863-76 PMID: 15341629
  7. InterPro, progress and status in 2005.
    Nucleic Acids Res. 2005 Jan 1;33(Database issue):D201-5 PMID: 15608177
  8. Molecular analysis of the NAC gene family in rice.
    Mol Gen Genet. 2000 Jan;262(6):1047-51 PMID: 10660065
  9. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method.
    Methods. 2001 Dec;25(4):402-8 PMID: 11846609
  10. Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses.
    Plant J. 2003 Apr;34(2):137-48 PMID: 12694590
  11. MrBayes 3: Bayesian phylogenetic inference under mixed models.
    Bioinformatics. 2003 Aug 12;19(12):1572-4 PMID: 12912839
  12. AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development.
    Plant J. 2005 Dec;44(6):903-16 PMID: 16359384
  13. NAC transcription factors, NST1 and NST3, are key regulators of the formation of secondary walls in woody tissues of Arabidopsis.
    Plant Cell. 2007 Jan;19(1):270-80 PMID: 17237351
  14. CUPULIFORMIS establishes lateral organ boundaries in Antirrhinum.
    Development. 2004 Feb;131(4):915-22 PMID: 14757643
  15. Genome-wide gene expression profiling in Arabidopsis thaliana reveals new targets of abscisic acid and largely impaired gene regulation in the abi1-1 mutant.
    J Cell Sci. 2002 Dec 15;115(Pt 24):4891-900 PMID: 12432076
  16. Cloning and characterization of tomato leaf senescence-related cDNAs.
    Plant Mol Biol. 1997 Mar;33(4):641-51 PMID: 9132056
  17. The CUP-SHAPED COTYLEDON1 gene of Arabidopsis regulates shoot apical meristem formation.
    Development. 2001 Apr;128(7):1127-35 PMID: 11245578
  18. The no apical meristem gene of Petunia is required for pattern formation in embryos and flowers and is expressed at meristem and primordia boundaries.
    Cell. 1996 Apr 19;85(2):159-70 PMID: 8612269
  19. Transcriptional regulation in wood formation.
    Trends Plant Sci. 2007 Feb;12(2):64-70 PMID: 17224301
  20. GenBank.
    Nucleic Acids Res. 1997 Jan 1;25(1):1-6 PMID: 9016491
  21. Global genome expression analysis of rice in response to drought and high-salinity stresses in shoot, flag leaf, and panicle.
    Plant Mol Biol. 2007 Mar;63(5):591-608 PMID: 17225073
  22. Interdependency of brassinosteroid and auxin signaling in Arabidopsis.
    PLoS Biol. 2004 Sep;2(9):E258 PMID: 15328536
  23. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.
    Nucleic Acids Res. 1997 Dec 15;25(24):4876-82 PMID: 9396791
  24. A membrane-associated NAC transcription factor regulates salt-responsive flowering via FLOWERING LOCUS T in Arabidopsis.
    Planta. 2007 Aug;226(3):647-54 PMID: 17410378
  25. Involvement of CUP-SHAPED COTYLEDON genes in gynoecium and ovule development in Arabidopsis thaliana.
    Plant Cell Physiol. 2000 Jan;41(1):60-7 PMID: 10750709
  26. Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana.
    DNA Res. 2003 Dec 31;10(6):239-47 PMID: 15029955
  27. SINAT5 promotes ubiquitin-related degradation of NAC1 to attenuate auxin signals.
    Nature. 2002 Sep 12;419(6903):167-70 PMID: 12226665
  28. Overexpression of a zinc-finger protein gene from rice confers tolerance to cold, dehydration, and salt stress in transgenic tobacco.
    Proc Natl Acad Sci U S A. 2004 Apr 20;101(16):6309-14 PMID: 15079051
  29. Profile hidden Markov models.
    Bioinformatics. 1998;14(9):755-63 PMID: 9918945
  30. Control of flowering time and cold response by a NAC-domain protein in Arabidopsis.
    PLoS One. 2007 Jul 25;2(7):e642 PMID: 17653269
  31. Role of arabidopsis MYC and MYB homologs in drought- and abscisic acid-regulated gene expression.
    Plant Cell. 1997 Oct;9(10):1859-68 PMID: 9368419
  32. A membrane-bound NAC transcription factor regulates cell division in Arabidopsis.
    Plant Cell. 2006 Nov;18(11):3132-44 PMID: 17098812
  33. A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress.
    Plant Cell. 1994 Feb;6(2):251-64 PMID: 8148648
  34. SND1, a NAC domain transcription factor, is a key regulator of secondary wall synthesis in fibers of Arabidopsis.
    Plant Cell. 2006 Nov;18(11):3158-70 PMID: 17114348
  35. Molecular characterization of Brassica napus NAC domain transcriptional activators induced in response to biotic and abiotic stress.
    Plant Mol Biol. 2003 Oct;53(3):383-97 PMID: 14750526
  36. Fitting a mixture model by expectation maximization to discover motifs in biopolymers.
    Proc Int Conf Intell Syst Mol Biol. 1994;2:28-36 PMID: 7584402
  37. NAC transcription factors: structurally distinct, functionally diverse.
    Trends Plant Sci. 2005 Feb;10(2):79-87 PMID: 15708345
  38. Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter.
    Plant Cell. 2004 Sep;16(9):2481-98 PMID: 15319476
  39. Transcription switches for protoxylem and metaxylem vessel formation.
    Genes Dev. 2005 Aug 15;19(16):1855-60 PMID: 16103214
  40. Differential induction of two potato genes, Stprx2 and StNAC, in response to infection by Phytophthora infestans and to wounding.
    Plant Mol Biol. 2001 Jul;46(5):521-9 PMID: 11516145
  41. PlnTFDB: an integrative plant transcription factor database.
    BMC Bioinformatics. 2007 Feb 07;8:42 PMID: 17286856
  42. Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development.
    Genes Dev. 2000 Dec 1;14 (23 ):3024-36 PMID: 11114891
  43. A NAC Gene regulating senescence improves grain protein, zinc, and iron content in wheat.
    Science. 2006 Nov 24;314(5803):1298-301 PMID: 17124321
  44. HRT gene function requires interaction between a NAC protein and viral capsid protein to confer resistance to turnip crinkle virus.
    Plant Cell. 2000 Oct;12(10):1917-26 PMID: 11041886
  45. Molecular characterization of AtNAM: a member of the Arabidopsis NAC domain superfamily.
    Plant Mol Biol. 2002 Sep;50(2):237-48 PMID: 12175016
  46. Improving plant drought, salt and freezing tolerance by gene transfer of a single stress-inducible transcription factor.
    Novartis Found Symp. 2001;236:176-86; discussion 186-9 PMID: 11387979
  47. Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice.
    Proc Natl Acad Sci U S A. 2006 Aug 29;103(35):12987-92 PMID: 16924117
  48. ANAC012, a member of the plant-specific NAC transcription factor family, negatively regulates xylary fiber development in Arabidopsis thaliana.
    Plant J. 2007 Jun;50(6):1035-48 PMID: 17565617
  49. The CUP-SHAPED COTYLEDON3 gene is required for boundary and shoot meristem formation in Arabidopsis.
    Plant Cell. 2003 Jul;15(7):1563-77 PMID: 12837947
  50. A homolog of NO APICAL MERISTEM is an immediate target of the floral homeotic genes APETALA3/PISTILLATA.
    Cell. 1998 Jan 9;92(1):93-103 PMID: 9489703
  51. Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis.
    Plant Cell. 1998 Aug;10(8):1391-406 PMID: 9707537
  52. Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions.
    Proc Natl Acad Sci U S A. 2000 Oct 10;97(21):11632-7 PMID: 11005831
  53. OsNAC6, a member of the NAC gene family, is induced by various stresses in rice.
    Genes Genet Syst. 2005 Apr;80(2):135-9 PMID: 16172526
  54. The MYB46 transcription factor is a direct target of SND1 and regulates secondary wall biosynthesis in Arabidopsis.
    Plant Cell. 2007 Sep;19(9):2776-92 PMID: 17890373
  55. Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice.
    Plant J. 2007 Aug;51(4):617-30 PMID: 17587305
  56. Plant cis-acting regulatory DNA elements (PLACE) database: 1999.
    Nucleic Acids Res. 1999 Jan 1;27(1):297-300 PMID: 9847208
  57. Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis.
    Plant Physiol. 2002 Oct;130(2):639-48 PMID: 12376631
  58. An Arabidopsis gene family encoding DRE/CRT binding proteins involved in low-temperature-responsive gene expression.
    Biochem Biophys Res Commun. 1998 Sep 8;250(1):161-70 PMID: 9735350
  59. Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant.
    Plant Cell. 1997 Jun;9(6):841-57 PMID: 9212461
  60. Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes.
    Science. 2000 Dec 15;290(5499):2105-10 PMID: 11118137
  61. Characterization of transcription factor gene SNAC2 conferring cold and salt tolerance in rice.
    Plant Mol Biol. 2008 May;67(1-2):169-81 PMID: 18273684
Article Info
Journal
Molecular genetics and genomics : MGG
Abbr.
Mol Genet Genomics
ISSN
1617-4615
DOI
10.1007/s00438-008-0386-6
Published
2008-12-00
Epub
2008-00-24
Pages
547-63
Language
English
Region
Germany
NLM ID
101093320
Subset
IM
External Links
PubMed source DOI: 10.1007/s00438-008-0386-6 View journal details
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