Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
권호 표지

A Basic Helix-Loop-Helix Transcription Factor Regulates Cell Elongation and Seed Germination

  • Kim, Jin-A (Graduate School of Chemistry and Molecular Engineering, Seoul National University) ;
  • Yun, Ju (Graduate School of Chemistry and Molecular Engineering, Seoul National University) ;
  • Lee, Minsun (Graduate School of Chemistry and Molecular Engineering, Seoul National University) ;
  • Kim, Youn-Sung (Graduate School of Chemistry and Molecular Engineering, Seoul National University) ;
  • Woo, Jae-Chang (Department of Biology, Mokpo National University) ;
  • Park, Chung-Mo (Graduate School of Chemistry and Molecular Engineering, Seoul National University)
  • Received : 2004.11.25
  • Accepted : 2005.01.24
  • Published : 2005.06.30
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Abstract

Plants are sessile and rely on a wide variety of growth hormones to adjust growth and development in response to internal and external stimuli. We have identified a gene, designated NAN, encoding a basic helix-loop-helix (bHLH) transcription factor that regulates cell elongation and seed germination in plants. NAN has an HLH motif in its C-terminal region but does not have any other discernible homologies to bHLH proteins. A bipartite nuclear localization signal is located close to the HLH motif. An Arabidopsis mutant, nan-1D, in which NAN is activated by the insertion of the 35S enhancer, exhibits growth retardation with short hypocotyls and curled leaves. It is also characterized by reduced seed germination and apical hook formation, symptomatic of GA deficiency or disrupted GA signaling. The phenotypic effects of nan-1D were increased by treatment with paclobutrazol (PAC), an inhibitor of gibberellic acid (GA) biosynthesis. NAN is constitutively expressed throughout the life cycle. Our observations indicate that NAN has a housekeeping role in plant growth and development, particularly in seed germination and cell elongation, and that it may modulate GA signaling.

Keywords

Acknowledgement

Supported by : Korea Science and Engineering Foundation, Korea Institute of Science and Technology Evaluation and Planning

References

  1. Achard, P., Vriezen, W. H., Van Der Straeten, D., and Harberd, N. P. (2003) Ethylene regulates Arabidopsis development via the modulation of DELLA protein growth repressor function. Plant Cell 15, 2816-2825 https://doi.org/10.1105/tpc.015685
  2. Atchley, W. R., Therhalle, W., and Dress, A. (1999) Positional dependence, cliques and predictive motifs in the bHLH protein domain. J. Mol. Evol. 48, 501–516 https://doi.org/10.1007/PL00006494
  3. Bereterbide, A., Hernould, M., Castera, S., and Mouras, A. (2001) Inhibition of cell proliferation, cell expansion and differentiation by the Arabidopsis SUPERMAN gene in transgenic tobacco plants. Planta 214, 22–29 https://doi.org/10.1007/s004250100584
  4. Bethke, P. C. and Jones, R. L. (1998) Gibberellin signaling. Curr. Opin. Plant Biol. 1, 440–446 https://doi.org/10.1016/S1369-5266(98)80270-7
  5. Bewley, J. D. (1997) Seed germination and dormancy. Plant Cell 9, 1055–1066 https://doi.org/10.1105/tpc.9.7.1055
  6. Borner, R., Kampmann, G., Chandler, J., Gleissner, R., Wisman, E., et al. (2000) A MADS domain gene involved in the transition to flowering in Arabidopsis. Plant J. 24, 591–599 https://doi.org/10.1046/j.1365-313x.2000.00906.x
  7. Chandler, P. M., Marion-Poll, A., Ellis, M., and Gubler, F. (2002) Mutants at the Slender1 locus of barley cv Himalaya. Molecular and physiological characterization. Plant Physiol. 129, 181–190 https://doi.org/10.1104/pp.010917
  8. Clough, S. J. and Bent, A. F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743 https://doi.org/10.1046/j.1365-313x.1998.00343.x
  9. Dill, A. and Sun, T. (2001) Synergistic derepression of gibberellin signaling by removing RGA and GAI function in Arabidopsis thaliana. Genetics 159, 777–785
  10. Fairchild, C. D., Schumaker, M. A., and Quail, P. H. (2000) HFR1 encodes an atypical bHLH protein that acts in phytochrome A signal transduction. Genes Dev. 14, 2377-2391
  11. Gilroy, S. and Jones, R. L. (1994) Perception of gibberellin and abscisic acid at the external face of the plasma membrane of barley (Hordeum vulgare L.) aleurone protoplasts. Plant Physiol. 104, 1185–1192
  12. Grandori, C., Cowley, S. M., James, L. P., and Eisenman, R. N. (2000) The Myc/Max/Mad network and the transcriptional control of cell behavior. Annu. Rev. Cell Dev. Biol. 16, 653– 699 https://doi.org/10.1146/annurev.cellbio.16.1.653
  13. Hedden, P. and Phillips A. L. (2000) Gibberellin metabolism: new insights revealed by the genes. Trends Plant Sci. 5, 523– 530 https://doi.org/10.1016/S1360-1385(00)01790-8
  14. Hooley, R., Beale, M. H., and Smith, S. J. (1991) Gibberellin perception at the plasma membrane of Avena fatua aleurone protoplasts. Planta 183, 274–280
  15. Huq, E. and Quail, P. H. (2002) PIF4, a phytochrome-interacting bHLH factor, functions as a negative regulator of phytochrome B signaling in Arabidopsis. EMBO J. 21, 2441–2450 https://doi.org/10.1093/emboj/21.10.2441
  16. Jacobsen, S. E., Binkowski, K. A., and Olszewski, N. E. (1996) SPINDLY, a tetratricopeptide repeat protein involved in gibberellin signal transduction in Arabidopsis. Proc. Natl. Acad. Sci. USA 93, 9292–9296
  17. King, K. E., Moritz, T., and Harberd, N. P. (2001) Gibberellins are not required for normal stem growth in Arabidopsis thaliana in the absence of GAI and RGA. Genetics 159, 767– 776
  18. Koornneef, M., Bentsink, L., and Hilhost, H. (2002) Seed dormancy and germination. Curr. Opin. Plant Biol. 5, 33–36 https://doi.org/10.1016/S1369-5266(01)00219-9
  19. Kurosawa, E. (1926) Experimental studies on the nature of the substance secreted by the 'bakanae' fungus. Nat. Hist. Soc. Formosa 16, 213-227
  20. Ledent, V. and Vervoort, M. (2001) The basic helix-loop-helix protein family: comparative genomics and phylogenetic analysis. Genome Res. 11, 754–770 https://doi.org/10.1101/gr.177001
  21. Lee, S., Cheng, H., King, K. E., Wang, W., He, Y., et al. (2002) Gibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose expression is up-regulated following imbibition. Genes Dev. 16, 646–658 https://doi.org/10.1101/gad.969002
  22. Lee, Y. J., Kim, J. H., Bae, S., Rho, S.-K., and Choe, S. Y. (2004) Mechanisms of transcriptional repression by TEL/ RUNX1 fusion protein. Mol. Cells 17, 217-222 https://doi.org/10.4313/JKEM.2004.17.2.217
  23. Lehman, A., Black, R., and Ecker, J. R. (1996) HOOKLESS1, an ethylene-response gene, is required for differential cell elongation in the Arabidopsis hypocotyl. Cell 85, 183-194 https://doi.org/10.1016/S0092-8674(00)81095-8
  24. Lim, M.-H., Kim, J., Kim, Y.-S., Chung, K.-S., Seo, Y.-H., et al. (2004) A new Arabidopsis gene, FLK, encodes an RNA binding protein with K homology motifs and regulates flowering time via FLOWERING LOCUS C. Plant Cell 16, 731-740 https://doi.org/10.1105/tpc.019331
  25. Liu, Y. G., Mitsukawa, N., Oosumi, T., and Whittier, R. F. (1995) Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J. 8, 457-463 https://doi.org/10.1046/j.1365-313X.1995.08030457.x
  26. Lovegrove, A. and Hooley, R. (2000) Gibberellin and abscisic acid signalling in aleurone. Trends Plant Sci. 5, 102-110 https://doi.org/10.1016/S1360-1385(00)01571-5
  27. Massari, M. E. and Murre, C. (2000) Helix-loop-helix proteins: Regulators of transcription in eukaryotic organisms. Mol. Cell. Biol. 20, 429–440 https://doi.org/10.1128/MCB.20.2.429-440.2000
  28. Mitsunaga, S., Tashiro, T., and Yamaguchi, J. (1994) Identification and characterization of gibberellin-insensitive mutants selected from among dwarf mutants of rice. Theor. Appl. Genet. 87, 705–712
  29. Ogas, J., Cheng, J.-C., Sung, Z. R., and Somerville, C. (1997) Cellular differentiation regulated by gibberellin in the Arabidopsis thaliana pickle mutant. Science 277, 91–94 https://doi.org/10.1126/science.277.5322.91
  30. Olszewski, N., Sun, T., and Gubler, F. (2002) Gibberellin signaling: biosynthesis, catabolism, and response pathways. Plant Cell 14 (Suppl.), S61–S80
  31. Peng, J. and Harberd, N. P. (2002) The role of GA-mediated signalling in the control of seed germination. Curr. Opin. Plant Biol. 5, 376-381 https://doi.org/10.1016/S1369-5266(02)00279-0
  32. Peng, J., Carol, P., Richards, D. E., King, K. E., Cowling, R. J., et al. (1997) The Arabidopsis GAI gene defines a signalling pathway that negatively regulates gibberellin responses. Genes Dev. 11, 3194–3205 https://doi.org/10.1101/gad.11.23.3194
  33. Raz, V. and Ecker, J. R. (1999) Regulation of differential growth in the apical hook of Arabidopsis. Development 126, 3661- 3668
  34. Richards, D. E., King, K. E., Ait-ali, T., and Harberd, N. P. (2001) How gibberellin regulates plant growth and development: a molecular genetic analysis of gibberellin signaling. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 67–88 https://doi.org/10.1146/annurev.arplant.52.1.67
  35. Sakamoto, T., Kamiya, N., Ueguchi-Tanaka, M., Iwahori, S., and Matsuoka, M. (2001) KNOX homeodomain protein directly suppresses the expression of a gibberellin biosynthetic gene in the tobacco shoot apical meristem. Genes Dev. 15, 581–590 https://doi.org/10.1101/gad.867901
  36. Silverstone, A. L., Mak, P. Y., Martinez, E. C., and Sun, T. P. (1997) The new RGA locus encodes a negative regulator of gibberellin response in Arabidopsis thaliana. Genetics 146, 1087–1099
  37. Silverstone, A. L., Jung, H.-S., Dill, A., Kawaide, H., Kamiya, Y., et al. (2001) Repressing a repressor: Gibberellin-induced rapid reduction of the RGA protein in Arabidopsis. Plant Cell 13, 1555-1565 https://doi.org/10.1105/tpc.13.7.1555
  38. Sun, T. (2000) Gibberellin signal transduction. Curr. Opin. Plant Biol. 3, 374-380 https://doi.org/10.1016/S1369-5266(00)00099-6
  39. Thomas, S. G. and Sun, T. (2004) Update on gibberellin signaling. A tale of the tall and the short. Plant Physiol. 135, 668-676 https://doi.org/10.1104/pp.104.040279
  40. Thornton, T. M., Swain, S. M., and Olszewski, N. E. (1999) Gibberellin signal transduction presents ellipsisthe SPY who O-GlcNAc'd me. Trends Plant Sci. 4, 424–428 https://doi.org/10.1016/S1360-1385(99)01485-5
  41. Toledo-Ortiz, G., Huq, E., and Quail, P. H. (2003) The Arabidopsis basic/helix-loop-helix transcription factor family. Plant Cell 15, 1749-1770 https://doi.org/10.1105/tpc.013839
  42. Vriezen, W. H., Achard, P., Harberd, N. P., and Van Der Straeten, D. (2004) Ethylene-mediated enhancement of apical hook formation in etiolated Arabidopsis thaliana seedlings is gibberellin dependent. Plant J. 37, 505-516 https://doi.org/10.1046/j.1365-313X.2003.01975.x
  43. Weigel, D., Ahn, J. H., Blazquez, M. A., Borevitz, J. O., Christensen, S. K., et al. (2000) Activation tagging in Arabidopsis. Plant Physiol. 122, 1003-1013 https://doi.org/10.1104/pp.122.4.1003
  44. Wen, C. K. and Chang, C. (2002) Arabidopsis RGL1 encodes a negative regulator of gibberellin responses. Plant Cell 14, 87–100 https://doi.org/10.1105/tpc.010325