Genomic and physiological studies of early cryptochrome 1 action demonstrate roles for auxin and gibberellin in the control of hypocotyl growth by blue light

Plant Journal

Volumn 36, Issue 2, 2003, Pages 203-214

  Folta, Kevin M ^a,d   Pontin, Mariela A ^b   Karlin Neumann, George ^c,e   Bottini, Rubén ^b,f   Spalding, Edgar P ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b National University of Rio Cuarto Laboratorio de Fisiologia Vegetal   (Argentina)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF FLORIDA   (United States)

^e ParAllele BioScience   (United States)

^f UNIVERSIDAD NACIONAL DE CUYO   (Argentina)

Author keywords

Auxin; Blue light; Cryptochrome; Gibberellin; Hypocotyl growth; Microarray

Indexed keywords

BIOSYNTHESIS; GENES; IRRADIATION; PHYSIOLOGY; RNA;

ARABIDOPSIS THALIANA; HYPOCOTYL GROWTH;

PLANTS (BOTANY);

NON-PROGRAMMATIC;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASE SEQUENCE; BIOLOGICAL CLOCKS; DNA PRIMERS; DROSOPHILA PROTEINS; EYE PROTEINS; FLAVOPROTEINS; GENE EXPRESSION REGULATION, PLANT; GENOME, PLANT; GIBBERELLINS; HYPOCOTYL; INDOLEACETIC ACIDS; LIGHT; PHOTORECEPTORS, INVERTEBRATE; RECEPTORS, G-PROTEIN-COUPLED; RNA, PLANT; TRANSCRIPTION, GENETIC;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 0142134233     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-313X.2003.01870.x     Document Type: Article

References (63)

1. Acton, G.J. and Murray, P.B. (1974) The roles of auxin and gibberellin in reversing radiation inhibition of hypocotyl lengthening. Planta, 36, 219-226.
2. Ahmad, M., Lin, C. and Cashmore, A.R. (1995) Mutations throughout an Arabidopsis blue-light photoreceptor impair blue-light-responsive anthocyanin accumulation and inhibition of hypocotyl elongation. Plant J. 8, 653-658.
3. Ahmad, M., Grancher, N., Heil, M., Black, R.C., Giovani, B., Galland, P. and Lardemer, D. (2002) Action spectrum for cryptochrome-dependent hypocotyl growth inhibition in Arabidopsis. Plant Physiol. 129, 774-785.
4. Ait-Ali, T., Frances, S., Weller, J.L., Reid, J.B., Kendrick, R.E. and Kamiya, Y. (1999) Regulation of gibberellin 20-oxidase and gibberellin 3-beta-hydroxylase transcript accumulation during de-etiolation of pea seedlings. Plant Physiol. 121, 783-791.
5. Anderson, M.B., Folta, K.M., Warpeha, K.M., Gibbons, J., Gao, J. and Kaufman, L.S. (1999) Blue light-directed destabilization of the pea Lhcb1*4 transcript depends on sequences within the 5′ untranslated region. Plant Cell, 11, 1579-1590.
6. Baraldi, R., Bertazza, M., Bogino, J., Luna, V. and Bottini, R. (1995) The effect of light quality in Prunus cerasus. Part II. Changes in hormone levels in light grown plants. Photochem. Photobiol. 62, 800-803.
7. Bender, J. and Fink, G.R. (1998) A Myb homologue, ATR1, activates tryptophan gene expression in Arabidopsis. Proc. Natl. Acad. Sci. USA, 95, 5655-5660.
8. Briggs, W.R. and Christie, J.M. (2002) Phototropins 1 and 2: versatile plant blue-light receptors. Trends Plant Sci. 7, 204-210.
9. Cashmore, A.R., Jarillo, J.A., Wu, Y.J. and Liu, D. (1999) Cryptochromes: blue light receptors for plants and animals. Science, 284, 760-765.
10. 3 levels. Physiol. Plant. 98, 381-388.
11. Coles, J.P., Phillips, A.L., Croker, S.J., García-Lepe, R., Lewis, M.J. and Hedden, P. (1999) Modification of gibberellin production and plant development in Arabidopsis by sense and antisense expression of gibberellin 20-oxidase genes. Plant J. 17, 547-556.
12. Collett, C.E., Harberd, N.P. and Leyser, O. (2000) Hormonal interactions in the control of Arabidopsis hypocotyl elongation. Plant Physiol. 124, 553-562.
13. Cosgrove, D.J. (1988) Mechanism of rapid suppression of cell expansion in cucumber hypocotyls after blue-light irradiation. Planta, 176, 109-116.
14. Cosgrove, D.J. (1994) Photomodulation of growth. In Photomorphogenesis in Plants, 2nd edn. (Kendrick, R.E. and Kronenberg, G.H.M., eds). Dordrecht, the Netherlands: Kluwer Academic Publishers, pp. 631-658.
15. Cosgrove, D.J. (1999) Enzymes and other agents that enhance cell wall extensibility. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 391-417.
16. Czernic, P., Visser, B., Sun, W., Savoure, A., Deslandes, L., Marco, Y., Van Montagu, M. and Verbruggen, N. (1999) Characterization of an Arabidopsis thaliana receptor-like protein kinase gene activated by oxidative stress and pathogen attack. Plant J. 18, 321-327.
17. Dale, S., Arro, M., Becerra, B., Morrice, N., Boronoat, A., Hardie, D.G. and Ferrer, A. (1995) Bacterial expression of the catalytic domain of (isoform HMGR1) from Arabidopsis thaliana, and its inactivation by phosphorylation at Ser577 by Brassica oleraceae 3-hydroxy-3-methylglutaryl-CoA reductase kinase. Eur. J. Biochem. 233, 506-513.
18. Devlin, P.F. and Kay, S.A. (2000) Cryptochromes are required for phytochrome signaling to the circadian clock but not for rhythmicity. Plant Cell, 12, 2499-2510.
19. Folta, K.M. and Kaufman, L.S. (2003) Phototropin 1 is required for high-fluence blue-light-mediated mRNA destabilization. Plant Mol. Biol. 51, 607-616.
20. Folta, K.M. and Spalding, E.P. (2001a) Unexpected roles for cryptochrome 2 and phototropin revealed by high-resolution analysis of blue light-mediated hypocotyl growth inhibition. Plant J. 26, 1-10.
21. Folta, K.M. and Spalding, E.P. (2001b) Opposing roles for phyA and phyB in cryptochrome-mediated suppression of hypocotyl elongation. Plant J. 28, 333-340.
22. Frachisse, J.M., Colcombet, J., Guern, J. and Barbier-Brygoo, H. (2000) Characterization of a nitrate-permeable channel able to mediate sustained anion efflux in hypocotyl cells from Arabidopsis thaliana. Plant J. 21, 361-371.
23. Gendreau, E., Traas, J., Desnos, T., Grandjean, O., Caboche, M. and Hofte, H. (1997) Cellular basis of hypocotyl growth in Arabidopsis thaliana. Plant Physiol. 114, 295-305.
24. Gendreau, E., Hofte, H., Grandjean, O., Brown, S. and Traas, J. (1998) Phytochrome controls the number of endoreduplication cycles in the Arabidopsis thaliana hypocotyl. Plant J. 13, 221-230.
25. Huala, E., Oeller, P.W., Liscum, E., Han, I.S., Larsen, E. and Briggs, W.R. (1997) Arabidopsis NPH1: a protein kinase with a putative redox-sensing domain. Science, 278, 2120-2123.
26. Imaizumi, T., Kadota, A., Hasebe, M. and Wada, M. (2002) Cryptochrome light signals control development to suppress auxin sensitivity in the moss Physcomitrella patens. Plant Cell, 14, 373-386.
27. Jackson, J.A. and Jenkins, G.I. (1995) Extension-growth responses and expression of flavonoid biosynthesis genes in the Arabidopsis hy4 mutant. Planta, 197, 233-239.
28. Jensen, P.J., Hangarter, R.P. and Estelle, M. (1998) Auxin transport is required for hypocotyl elongation in light-grown but not dark-grown Arabidopsis. Plant Physiol. 116, 455-462.
29. Kendrick, R.E. and Kronenberg, G.H.M. (1994) Photomorphogenesis in Plants, 2nd edn. Dordrecht, the Netherlands: Kluwer Academic Publishers.
30. Kleinow, T., Bhalerao, R., Breuer, F., Umeda, M., Salchert, K. and Koncz, C. (2000) Functional identification of an Arabidopsis snf4 ortholog by screening for heterologous multicopy suppressors of snf4 deficiency in yeast. Plant J. 23, 115-122.
31. Kranz, H.D., Denekamp, M., Greco, R. et al. (1998) Towards functional characterisation of the members of the R2R3-MYB gene family from Arabidopsis thaliana. Plant J. 16, 263-276.
32. Learned, R.M. (1996) Light suppresses 3-hydroxy-3-methylglutaryl coenzyme A reductase gene expression in Arabidopsis thaliana. Plant Physiol. 110, 645-655.
33. Lee, M.M. and Schiefelbein, J. (1999) WEREWOLF, a MYB-related protein in Arabidopsis, is a position-dependent regulator of epidermal cell patterning. Cell, 99, 473-483.
34. Li, J.X., Wang, X.Q., Watson, M.B. and Assmann, S.M. (2000) Regulation of abscisic acid-induced stomatal closure and anion channels by guard cell AAPK kinase. Science, 287, 300-303.
35. Lin, C. (2002) Blue light receptors and signal transduction. Plant Cell, 14 (Suppl.), 207-225.
36. Liscum, E. and Briggs, W.R. (1995) Mutations in the NPH1 locus of Arabidopsis disrupt the perception of phototropic stimuli. Plant Cell, 7, 473-485.
37. Lockhart, J.A. (1956) Reversal of the light inhibition of stem growth by the gibberellins. Proc. Natl. Acad. Sci. USA, 42, 841-848.
38. Ma, L., Li, J., Qu, L., Hager, J., Chen, Z., Zhao, H. and Deng, X.W. (2001) Light control of Arabidopsis development entails coordinated regulation of genome expression and cellular pathways. Plant Cell, 13, 2589-2607.
39. Noh, B. and Spalding, E.P. (1998) Anion channels and the stimulation of anthocyanin accumulation by blue light in Arabidopsis seedlings. Plant Physiol. 116, 503-509.
40. Parks, B.M. and Spalding, E.P. (1999) Sequential and coordinated action of phytochromes A and B during Arabidopsis stem growth revealed by kinetic analysis. Proc. Natl. Acad. Sci. USA, 96, 14142-14146.
41. Parks, B.M., Cho, M.H. and Spalding, E.P. (1998) Two genetically separable phases of growth inhibition induced by blue light in Arabidopsis seedlings. Plant Physiol. 118, 609-615.
42. Parks, B.M., Folta, K.M. and Spalding, E.P. (2001) Photocontrol of stem growth. Curr. Opin. Plant Biol. 4, 436-440.
43. Pei, Z.M., Kuchitsu, K., Ward, J.M., Schwarz, M. and Schroeder, J.I. (1997) Differential abscisic acid regulation of guard cell slow anion channels in Arabidopsis wild-type and abi1 and abi2 mutants. Plant Cell, 9, 409-423.
44. Peng, J. and Harberd, N.P. (1997) Gibberellin deficiency and response mutations suppress the stem elongation phenotype of phytochrome-deficient mutants of Arabidopsis. Plant Physiol. 113, 1051-1058.
45. Quail, P.H., Boylan, M.T., Parks, B.M., Short, T.W., Xu, Y. and Wagner, D. (1995) Phytochromes: photosensory perception and signal transduction. Science, 268, 675-680.
46. Rademacher, W. (1991) Inhibitors of gibberellin biosynthesis: applications in agriculture and horticulture. In Gibberellins (Takahashi, N., Phinney, B.O. and McMillan, J., eds). New York: Springer-Verlag, pp. 296-310.
47. Reed, J.W. (2001) Roles and activities of Aux/IAA proteins in Arabidopsis. Trends Plant Sci. 6, 420-425.
48. Reed, J.W., Foster, K.R., Morgan, P.W. and Chory, J. (1996) Phytochrome B affects responsiveness to gibberellins in Arabidopsis. Plant Physiol. 112, 337-342.
49. Reid, J.B., Botwright, N.A., Smith, J.J., O'Neill, D.P. and Kerckhoffs, L.H. (2002) Control of gibberellin levels and gene expression during de-etiolation in pea. Plant Physiol. 128, 734-741.
50. Salchert, K., Bhalerao, R., Koncz-Kalman, Z. and Koncz, C. (1998) Control of cell elongation and stress responses by steroid hormones and carbon catabolic repression in plants. Philos. Trans. R. Soc. Lond. B Biol. Sci. 353, 1517-1520.
51. Schmidt, C., Schelle, I., Liao, Y.J. and Schroeder, J.I. (1995) Strong regulation of slow anion channels and abscisic-acid signaling in guard cells by phosphorylation and dephosphorylation events. Proc. Natl. Acad. Sci. USA, 92, 9535-9539.
52. Shalitin, D., Yang, H., Mockler, T.C., Maymon, M., Guo, H., Whitelam, G.C. and Lin, C. (2002) Regulation of Arabidopsis cryptochrome 2 by blue-light-dependent phosphorylation. Nature, 417, 763-767.
53. Spalding, E.P. (2000) Ion channels and the transduction of light signals. Plant Cell Environ. 23, 665-674.
54. Stowe-Evans, E.L., Luesse, D.R. and Liscum, E. (2001) The enhancement of phototropin-induced phototropic curvature in Arabidopsis occurs via a photoreversible phytochrome A-dependent modulation of auxin responsiveness. Plant Physiol. 26, 826-834.
55. Stracke, R., Werber, M. and Weisshaar, B. (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr. Opin. Plant Biol. 4, 447-456.
56. Tepperman, J.M., Zhu, T., Chang, H.S., Wang, X. and Quail, P.H. (2001) Multiple transcription-factor genes are early targets of phytochrome A signaling. Proc. Natl. Acad. Sci. USA, 98, 9437-9442.
57. Thomine, S., Lelievre, F., Boufflet, M., Guern, J. and Barbier-Brygoo, H. (1997) Anion-Channel blockers interfere with auxin responses in dark-grown Arabidopsis hypocotyls. Plant Physiol. 115, 533-542.
58. 3 and abscisic acid. Plant Growth Reg. 26, 165-173.
59. Wang, H., Ma, L., Habashi, J., Li, J., Zhao, H. and Deng, X.W. (2002) Analysis of far-red light-regulated genome expression profiles of phytochrome A pathway mutants in Arabidopsis. Plant J. 32, 723-733.
60. Whitelam, G.C., Patel, S. and Devlin, P.F. (1998) Phytochromes and photomorphogenesis in Arabidopsis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 353, 1445-1453.
61. Yamaguchi, S. and Kamiya, Y. (2000) Gibberellin biosynthesis: its regulation by endogenous and environmental signals. Plant Cell Physiol. 41, 251-257.
62. Zhao, Y. and Chory, J. (2001) A link between the light and gibberellin signaling cascades. Dev. Cell, 1, 315-316.
63. Zhong, H.H., Resnick, A.S., Straume, M. and McClung, C.R. (1997) Effects of synergistic signaling by phytochrome A and cryptochrome1 on circadian clock-regulated catalase expression. Plant Cell, 9, 947-955.