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A membrane-associated NAC transcription factor regulates salt-responsive flowering via FLOWERING LOCUS T in Arabidopsis

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Abstract

The plant-specific NAC (NAM, ATAF1/2, CUC2) transcription factors play regulatory roles in diverse developmental processes and stress responses. Notably, a subset of the NAC members, collectively designated NTLs, is membrane-associated, suggesting that membrane-mediated regulation would be an important molecular scheme functioning in rapid transcriptional responses to external stimuli. Here, we examined the physiological role of a salt-responsive NTL, NTL8, by molecular genetic and transgenic approaches. NTL8 is expressed as a membrane-associated, dormant form and subsequently processed into a transcriptionally active, nuclear form. Transgenic plants overproducing an active NTL8 form exhibited delayed flowering as well as reduced growth with small curled leaves. Accordingly, expression of FLOWERING LOCUS T (FT) and its downstream genes was significantly reduced in the transgenic plants. Furthermore, FT was significantly repressed by high salt. We therefore propose that NTL8 mediates salt-responsive flowering via FT in Arabidopsis.

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Abbreviations

ABA:

Abscisic acid

FT:

FLOWERING LOCUS T

GA:

Gibberellic acid

GFP:

Green fluorescence protein

GUS:

β-Glucuronidase

JA:

Jasmonic acid

LD:

Long day

MTF:

Membrane-associated transcription factor

NAC:

NAM, ATAF1/2, CUC2

NTL:

NTM1-Like

RUP:

Ubiquitin/proteasome-dependent processing

SD:

Short day

TM:

Transmembrane domain

References

  • Achard P, Cheng H, De Grauwe L, Decat J, Schoutteten H, Moritz T, Van Der Straeten D, Peng J, Harberd NP (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science 311:91–94

    Article  PubMed  CAS  Google Scholar 

  • Amasino RM (2005) Vernalization and flowering time. Curr Opin Biotechnol 16:154–158

    Article  PubMed  CAS  Google Scholar 

  • Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ Antiport in Arabidopsis. Science 285:1256–1258

    Article  PubMed  CAS  Google Scholar 

  • Ausin I, Alonso-Blanco C, Martinez-Zapater JM (2005) Environmental regulation of flowering. Int J Dev Biol 49:689–705

    Article  PubMed  CAS  Google Scholar 

  • Balasubramanian S, Sureshkumar S, Lempe J, Weigel D (2006) Potent induction of Arabidopsis thaliana flowering by elevated growth temperature PLoS Genet 2:e106

    Article  PubMed  CAS  Google Scholar 

  • Bohnert HJ, Nelson DE, Jensen RG (1995) Adaptations to environmental stresses. Plant Cell 7:1099–1111

    Article  PubMed  CAS  Google Scholar 

  • Brown MS, Ye J, Rawson RB, Goldstein JL (2000) Regulated intramembrane proteolysis: a control mechanism conserved from bacteria to humans. Cell 100:391–398

    Article  PubMed  CAS  Google Scholar 

  • Christmann A, Moes D, Himmelbach A, Yang Y, Tang Y, Grill E (2006) Integration of abscisic acid signalling into plant responses. Plant Biol 8:314–325

    Article  PubMed  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  PubMed  CAS  Google Scholar 

  • Denby K, Gehring C (2005) Engineering drought and salinity tolerance in plants: lessons from genome-wide expression profiling in Arabidopsis. Trends Biotechnol 23:547–552

    Article  PubMed  CAS  Google Scholar 

  • Duval M, Hsieh TF, Kim SY, Thomas TL (2002) Molecular characterization of AtNAM: a member of the Arabidopsis NAC domain superfamily. Plant Mol Biol 50:237–248

    Article  PubMed  CAS  Google Scholar 

  • Fujita M, Fujita Y, Maruyama K, Seki M, Hiratsu K, Ohme-Takagi M, Tran LSP, Yamaguchi-Shinozaki K, Shinozaki K (2004) A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. Plant J 39:863–876

    Article  PubMed  CAS  Google Scholar 

  • He XJ, Mu RL, Cao WH, Zhang ZG, Zhang JS, Chen SY (2005) AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. Plant J 44:903–916

    Article  PubMed  CAS  Google Scholar 

  • Hegedus D, Yu M, Baldwin D, Gruber M, Sharpe A, Parkin I, Whitwill S, Lydiate D (2003) Molecular characterization of Brassica napus NAC domain transcriptional activators induced in response to biotic and abiotic stress. Plant Mol Biol 53:383–397

    Article  PubMed  CAS  Google Scholar 

  • Hibara K, Takada S, Tasaka M (2003) CUC1 gene activates the expression of SAM-related genes to induce adventitious shoot formation. Plant J 36:687–696

    Article  PubMed  CAS  Google Scholar 

  • Hoppe T, Matuschewski K, Rape M, Schlenker S, Ulrich HD, Jentsch S (2000) Activation of a membrane-bound transcription factor by regulated ubiquitin/proteasome-dependent processing. Cell 102:577–586

    Article  PubMed  CAS  Google Scholar 

  • Hoppe T, Rape M, Jentsch S (2001) Membrane-bound transcription factors: regulated release by RIP or RUP. Curr Opin Cell Biol 13:344–348

    Article  PubMed  CAS  Google Scholar 

  • Inan G, Zhang Q, Li P, Wang Z, Cao Z, Zhang H, Zhang C, Quist TM, Goodwin SM, Zhu J, Shi H, Damsz B, Charbaji T, Gong Q, Ma S, Fredricksen M, Galbraith DW, Jenks MA, Rhodes D, Hasegawa PM, Bohnert HJ, Joly RJ, Bressan RA, Zhu JK (2004) Salt cress. A halophyte and cryophyte Arabidopsis relative model system and its applicability to molecular genetic analyses of growth and development of extremophiles. Plant Physiol 135:1718–37

    Article  PubMed  CAS  Google Scholar 

  • Iwata Y, Koizumi N (2005) An Arabidopsis transcription factor, AtbZIP60, regulates the endoplasmic reticulum stress response in a manner unique to plants. Proc Natl Acad Sci USA 102:5280–5285

    Article  PubMed  CAS  Google Scholar 

  • Jiang Y, Deyholos MK (2006) Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes. BMC Plant Biol 6:25. doi:10.1186/1471–2229–6-25

  • Kaffman A, O’Shea EK (1999) Regulation of nuclear localization: a key to a door. Annu Rev Cell Dev Biol 15:291–339

    Article  PubMed  CAS  Google Scholar 

  • Kardailsky I, Shukla VK, Ahn JH, Dagenais N, Christensen SK, Nguyen JT, Chory J, Harrison MJ, Weigel D (1999) Activation tagging of the floral inducer FT. Science 286:1962–1965

    Article  PubMed  CAS  Google Scholar 

  • Kim YS, Kim SG, Park JE, Park HY, Lim MH, Chua NH, Park CM (2006) A membrane-bound NAC transcription factor regulates cell division in Arabidopsis. Plant Cell 18:3132–3144

    Article  PubMed  CAS  Google Scholar 

  • Kim SY, Kim SG, Kim YS, Seo PJ, Bae M, Yoon HK, Park CM (2007) Exploring membrane-associated NAC transcription factors in Arabidopsis: implications for membrane biology in genome regulation. Nucleic Acids Res 35:203–213

    Article  PubMed  CAS  Google Scholar 

  • Koiwa H, Bressan RA, Hasegawa PM (2006) Identification of plant stress-responsive determinants in Arabidopsis by large-scale forward genetic screens. J Exp Bot 57:1119–1128

    Article  PubMed  CAS  Google Scholar 

  • Mouradov A, Cremer F, Coupland G (2002) Control of flowering time: interacting pathways as a basis for diversity. Plant Cell 14:S111–S130

    PubMed  CAS  Google Scholar 

  • Ooka H, Satoh K, Doi K, Nagata T, Otomo Y, Murakami K, Matsubara K, Osato N, Kawai J, Carninci P, Hayashizaki Y, Suzuki K, Kojima K, Takahara Y, Yamamoto K, Kikuchi S (2003) Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Res 10:239–247

    Article  PubMed  CAS  Google Scholar 

  • Sablowski RW, Meyerowitz EM (1998) A homolog of NO APICAL MERISTEM is an immediate target of the floral homeotic genes APETALA3/PISTILLATA. Cell 92:93–103

    Article  PubMed  CAS  Google Scholar 

  • Schwacke R, Schneider A, van der Graaff E, Fischer K, Catoni E, Desimone M, Frommer WB, Flügge UI, Kunze R (2003) ARAMEMNON, a novel database for Arabidopsis integral membrane proteins. Plant Physiol 131:16–26

    Article  PubMed  CAS  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (1996) Molecular responses to drought and cold stress. Curr Opin Biotechnol 7:161–167

    Article  PubMed  CAS  Google Scholar 

  • Suárez-López P, Wheatley K, Robson F, Onouchi H, Valverde F, Coupland G (2001) CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410:1116–1120

    Article  PubMed  Google Scholar 

  • Tran LS, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, Maruyama K, Fujita M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2004) 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 16:2481–2498

    Article  PubMed  CAS  Google Scholar 

  • Vik Å, Rine J (2000) Membrane biology: membrane-regulated transcription. Curr Biol 10:R869–R871

    Article  PubMed  CAS  Google Scholar 

  • Xie Q, Frugis G, Colgan D, Chua NH (2000) Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes Dev 14:3024–3036

    Article  PubMed  CAS  Google Scholar 

  • Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14:S165–S183

    Article  PubMed  CAS  Google Scholar 

  • Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis tool box. Plant Physiol 136:2621–2632

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We would like to thank Y.-S. Kim and H.-K. Yun for their technical supports. This work was supported by the Brain Korea 21, Biogreen 21 (20050301034456), National Research Laboratory (2005-01039) Programs, and by grants from the Plant Signaling Network Research Center and from KOSEF and KRF (2005-070-C00129).

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  1. Molecular Signaling Laboratory, Department of Chemistry, Seoul National University, Seoul, 151-742, Korea

    Sang-Gyu Kim, Sun-Young Kim & Chung-Mo Park

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  1. Sang-Gyu Kim
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  2. Sun-Young Kim
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Correspondence to Chung-Mo Park.

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Kim, SG., Kim, SY. & Park, CM. A membrane-associated NAC transcription factor regulates salt-responsive flowering via FLOWERING LOCUS T in Arabidopsis . Planta 226, 647–654 (2007). https://doi.org/10.1007/s00425-007-0513-3

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