Phytochrome E Influences Internode Elongation and Flowering Time in Arabidopsis

Correspondence to: Garry C. Whitelam, GCW1{at}le.ac.uk (E-mail), 44-116-252-2791 (fax).

From a screen of M₂ seedlings derived from -mutagenesis of seeds doubly null for phytochromes phyA and phyB, we isolated a mutant lacking phyE. The PHYE gene of the selected mutant, phyE-1, was found to contain a 1-bp deletion at a position equivalent to codon 726, which is predicted to result in a premature stop at codon 739. Immunoblot analysis showed that the phyE protein was undetectable in the phyE-1 mutant. In the phyA- and phyB-deficient background, phyE deficiency led to early flowering, elongation of internodes between adjacent rosette leaves, and reduced petiole elongation. This is a phenocopy of the response of phyA phyB seedlings to end-of-day far-red light treatments. Furthermore, a phyE deficiency attenuated the responses of phyA phyB seedlings to end-of-day far-red light treatments. Monogenic phyE mutants were indistinguishable from wild-type seedlings. However, phyB phyE double mutants flowered earlier and had longer petioles than did phyB mutants. The elongation and flowering responses conferred by phyE deficiency are typical of shade avoidance responses to the low red/far-red ratio. We conclude that in conjunction with phyB and to a lesser extent with phyD, phyE functions in the regulation of the shade avoidance syndrome.

This article has been cited by other articles:

				K. A. Franklin and P. H. Quail Phytochrome functions in Arabidopsis development J. Exp. Bot., October 8, 2009; (2009) erp304v1. [Abstract] [Full Text] [PDF]

				S. Pouteau and C. Albertini The significance of bolting and floral transitions as indicators of reproductive phase change in Arabidopsis J. Exp. Bot., August 1, 2009; 60(12): 3367 - 3377. [Abstract] [Full Text] [PDF]

				C. C. Zheng, D. Potter, and S. D. O'Neill Phytochrome gene expression and phylogenetic analysis in the short-day plant Pharbitis nil (Convolvulaceae): Differential regulation by light and an endogenous clock Am. J. Botany, July 1, 2009; 96(7): 1319 - 1336. [Abstract] [Full Text] [PDF]

				H. Ikeda, N. Fujii, and H. Setoguchi Molecular Evolution of Phytochromes in Cardamine nipponica (Brassicaceae) Suggests the Involvement of PHYE in Local Adaptation Genetics, June 1, 2009; 182(2): 603 - 614. [Abstract] [Full Text] [PDF]

				T. Clack, A. Shokry, M. Moffet, P. Liu, M. Faul, and R. A. Sharrock Obligate Heterodimerization of Arabidopsis Phytochromes C and E and Interaction with the PIF3 Basic Helix-Loop-Helix Transcription Factor PLANT CELL, March 1, 2009; 21(3): 786 - 799. [Abstract] [Full Text] [PDF]

				W. Hu, Y.-S. Su, and J. C. Lagarias A Light-Independent Allele of Phytochrome B Faithfully Recapitulates Photomorphogenic Transcriptional Networks Mol Plant, January 1, 2009; 2(1): 166 - 182. [Abstract] [Full Text] [PDF]

				A. C. Wollenberg, B. Strasser, P. D. Cerdan, and R. M. Amasino Acceleration of Flowering during Shade Avoidance in Arabidopsis Alters the Balance between FLOWERING LOCUS C-Mediated Repression and Photoperiodic Induction of Flowering Plant Physiology, November 1, 2008; 148(3): 1681 - 1694. [Abstract] [Full Text] [PDF]

				L. Guo, J. Zhou, A. A. Elling, J.-B. F. Charron, and X. W. Deng Histone Modifications and Expression of Light-Regulated Genes in Arabidopsis Are Cooperatively Influenced by Changing Light Conditions Plant Physiology, August 1, 2008; 147(4): 2070 - 2083. [Abstract] [Full Text] [PDF]

				D. L. Filiault, C. A. Wessinger, J. R. Dinneny, J. Lutes, J. O. Borevitz, D. Weigel, J. Chory, and J. N. Maloof Amino acid polymorphisms in Arabidopsis phytochrome B cause differential responses to light PNAS, February 26, 2008; 105(8): 3157 - 3162. [Abstract] [Full Text] [PDF]

				P. Leivar, E. Monte, B. Al-Sady, C. Carle, A. Storer, J. M. Alonso, J. R. Ecker, and P. H. Quail The Arabidopsis Phytochrome-Interacting Factor PIF7, Together with PIF3 and PIF4, Regulates Responses to Prolonged Red Light by Modulating phyB Levels PLANT CELL, February 1, 2008; 20(2): 337 - 352. [Abstract] [Full Text] [PDF]

				J. Kneissl, T. Shinomura, M. Furuya, and C. Bolle A Rice Phytochrome A in Arabidopsis: The Role of the N-terminus under red and far-red light Mol Plant, January 1, 2008; 1(1): 84 - 102. [Abstract] [Full Text] [PDF]

				T. H. Kebrom and T. P. Brutnell The molecular analysis of the shade avoidance syndrome in the grasses has begun J. Exp. Bot., October 5, 2007; (2007) erm205v1. [Abstract] [Full Text] [PDF]

				E. Oh, S. Yamaguchi, J. Hu, J. Yusuke, B. Jung, I. Paik, H.-S. Lee, T.-p. Sun, Y. Kamiya, and G. Choi PIL5, a Phytochrome-Interacting bHLH Protein, Regulates Gibberellin Responsiveness by Binding Directly to the GAI and RGA Promoters in Arabidopsis Seeds PLANT CELL, April 1, 2007; 19(4): 1192 - 1208. [Abstract] [Full Text] [PDF]

				S. Pouteau, V. Ferret, and D. Lefebvre Comparison of environmental and mutational variation in flowering time in Arabidopsis J. Exp. Bot., December 1, 2006; 57(15): 4099 - 4109. [Abstract] [Full Text] [PDF]

				B. Thomas Light signals and flowering J. Exp. Bot., October 1, 2006; 57(13): 3387 - 3393. [Abstract] [Full Text] [PDF]

				A. Pareek, A. Singh, M. Kumar, H. R. Kushwaha, A. M. Lynn, and S. L. Singla-Pareek Whole-Genome Analysis of Oryza sativa Reveals Similar Architecture of Two-Component Signaling Machinery with Arabidopsis Plant Physiology, October 1, 2006; 142(2): 380 - 397. [Abstract] [Full Text] [PDF]

				R. Khanna, Y. Shen, G. Toledo-Ortiz, E. A. Kikis, H. Johannesson, Y.-S. Hwang, and P. H. Quail Functional Profiling Reveals That Only a Small Number of Phytochrome-Regulated Early-Response Genes in Arabidopsis Are Necessary for Optimal Deetiolation PLANT CELL, September 1, 2006; 18(9): 2157 - 2171. [Abstract] [Full Text] [PDF]

				I. Roig-Villanova, J. Bou, C. Sorin, P. F. Devlin, and J. F. Martinez-Garcia Identification of Primary Target Genes of Phytochrome Signaling. Early Transcriptional Control during Shade Avoidance Responses in Arabidopsis Plant Physiology, May 1, 2006; 141(1): 85 - 96. [Abstract] [Full Text] [PDF]

				G. C. Briggs, C. F. Mouchel, and C. S. Hardtke Characterization of the Plant-Specific BREVIS RADIX Gene Family Reveals Limited Genetic Redundancy Despite High Sequence Conservation Plant Physiology, April 1, 2006; 140(4): 1306 - 1316. [Abstract] [Full Text] [PDF]

				T. J. Emborg, J. M. Walker, B. Noh, and R. D. Vierstra Multiple Heme Oxygenase Family Members Contribute to the Biosynthesis of the Phytochrome Chromophore in Arabidopsis Plant Physiology, March 1, 2006; 140(3): 856 - 868. [Abstract] [Full Text] [PDF]

				M. Chen and M. Ni RED AND FAR-RED INSENSITIVE 2, a RING-Domain Zinc Finger Protein, Mediates Phytochrome-Controlled Seedling Deetiolation Responses Plant Physiology, February 1, 2006; 140(2): 457 - 465. [Abstract] [Full Text] [PDF]

				M. Takano, N. Inagaki, X. Xie, N. Yuzurihara, F. Hihara, T. Ishizuka, M. Yano, M. Nishimura, A. Miyao, H. Hirochika, et al. Distinct and Cooperative Functions of Phytochromes A, B, and C in the Control of Deetiolation and Flowering in Rice PLANT CELL, December 1, 2005; 17(12): 3311 - 3325. [Abstract] [Full Text] [PDF]

				K. A. FRANKLIN and G. C. WHITELAM Phytochromes and Shade-avoidance Responses in Plants Ann. Bot., August 1, 2005; 96(2): 169 - 175. [Abstract] [Full Text] [PDF]

				S. Mathews Phytochrome Evolution in Green and Nongreen Plants J. Hered., May 1, 2005; 96(3): 197 - 204. [Abstract] [Full Text] [PDF]

				A. P. Fernandez, P. Gil, I. Valkai, F. Nagy, and E. Schafer Analysis of the Function of the Photoreceptors Phytochrome B and Phytochrome D in Nicotiana plumbaginifolia and Arabidopsis thaliana Plant Cell Physiol., May 1, 2005; 46(5): 790 - 796. [Abstract] [Full Text] [PDF]

				T. Kozuka, G. Horiguchi, G.-T. Kim, M. Ohgishi, T. Sakai, and H. Tsukaya The Different Growth Responses of the Arabidopsis thaliana Leaf Blade and the Petiole during Shade Avoidance are Regulated by Photoreceptors and Sugar Plant Cell Physiol., January 15, 2005; 46(1): 213 - 223. [Abstract] [Full Text] [PDF]

				R. A. Sharrock and T. Clack Heterodimerization of type II phytochromes in Arabidopsis PNAS, August 3, 2004; 101(31): 11500 - 11505. [Abstract] [Full Text] [PDF]

				Y. Oka, T. Matsushita, N. Mochizuki, T. Suzuki, S. Tokutomi, and A. Nagatani Functional Analysis of a 450-Amino Acid N-Terminal Fragment of Phytochrome B in Arabidopsis PLANT CELL, August 1, 2004; 16(8): 2104 - 2116. [Abstract] [Full Text] [PDF]

				M. J. Sheehan, P. R. Farmer, and T. P. Brutnell Structure and Expression of Maize Phytochrome Family Homeologs Genetics, July 1, 2004; 167(3): 1395 - 1405. [Abstract] [Full Text] [PDF]

				P. K. Boss, R. M. Bastow, J. S. Mylne, and C. Dean Multiple Pathways in the Decision to Flower: Enabling, Promoting, and Resetting PLANT CELL, June 1, 2004; 16(suppl_1): S18 - S31. [Full Text] [PDF]

				K. A. Franklin and G. C. Whitelam Light signals, phytochromes and cross-talk with other environmental cues J. Exp. Bot., January 2, 2004; 55(395): 271 - 276. [Abstract] [Full Text] [PDF]

				B. M. Parks The Red Side of Photomorphogenesis Plant Physiology, December 1, 2003; 133(4): 1437 - 1444. [Full Text]

				S. El-Din El-Assal, C. Alonso-Blanco, A. J.M. Peeters, C. Wagemaker, J. L. Weller, and M. Koornneef The Role of Cryptochrome 2 in Flowering in Arabidopsis Plant Physiology, December 1, 2003; 133(4): 1504 - 1516. [Abstract] [Full Text] [PDF]

				N. H. Markelz, D. E. Costich, and T. P. Brutnell Photomorphogenic Responses in Maize Seedling Development Plant Physiology, December 1, 2003; 133(4): 1578 - 1591. [Abstract] [Full Text]

				P. F. Devlin, M. J. Yanovsky, and S. A. Kay A Genomic Analysis of the Shade Avoidance Response in Arabidopsis Plant Physiology, December 1, 2003; 133(4): 1617 - 1629. [Abstract] [Full Text]

				E. Monte, J. M. Alonso, J. R. Ecker, Y. Zhang, X. Li, J. Young, S. Austin-Phillips, and P. H. Quail Isolation and Characterization of phyC Mutants in Arabidopsis Reveals Complex Crosstalk between Phytochrome Signaling Pathways PLANT CELL, September 1, 2003; 15(9): 1962 - 1980. [Abstract] [Full Text] [PDF]

				K. A. Franklin, S. J. Davis, W. M. Stoddart, R. D. Vierstra, and G. C. Whitelam Mutant Analyses Define Multiple Roles for Phytochrome C in Arabidopsis Photomorphogenesis PLANT CELL, September 1, 2003; 15(9): 1981 - 1989. [Abstract] [Full Text] [PDF]

				D.-S. Cho, S.-H. Hong, H.-G. Nam, and M.-S. Soh FIN5 Positively Regulates Far-red Light Responses in Arabidopsis thaliana Plant Cell Physiol., June 15, 2003; 44(6): 565 - 572. [Abstract] [Full Text] [PDF]

				K. J. Halliday and G. C. Whitelam Changes in Photoperiod or Temperature Alter the Functional Relationships between Phytochromes and Reveal Roles for phyD and phyE Plant Physiology, April 1, 2003; 131(4): 1913 - 1920. [Abstract] [Full Text] [PDF]

				K. A. Franklin, U. Praekelt, W. M. Stoddart, O. E. Billingham, K. J. Halliday, and G. C. Whitelam Phytochromes B, D, and E Act Redundantly to Control Multiple Physiological Responses in Arabidopsis Plant Physiology, March 1, 2003; 131(3): 1340 - 1346. [Abstract] [Full Text] [PDF]

				T. Mockler, H. Yang, X. Yu, D. Parikh, Y.-c. Cheng, S. Dolan, and C. Lin Regulation of photoperiodic flowering by Arabidopsis photoreceptors PNAS, February 18, 2003; 100(4): 2140 - 2145. [Abstract] [Full Text] [PDF]

				D. M. Friedrichsen, J. Nemhauser, T. Muramitsu, J. N. Maloof, J. Alonso, J. R. Ecker, M. Furuya, and J. Chory Three Redundant Brassinosteroid Early Response Genes Encode Putative bHLH Transcription Factors Required for Normal Growth Genetics, November 1, 2002; 162(3): 1445 - 1456. [Abstract] [Full Text] [PDF]

				G. A. Maddonni, M. E. Otegui, B. Andrieu, M. Chelle, and J. J. Casal Maize Leaves Turn Away from Neighbors Plant Physiology, November 1, 2002; 130(3): 1181 - 1189. [Abstract] [Full Text] [PDF]

				S.-I. Tanaka, S. Nakamura, N. Mochizuki, and A. Nagatani Phytochrome in Cotyledons Regulates the Expression of Genes in the Hypocotyl through Auxin-Dependent and -Independent Pathways Plant Cell Physiol., October 15, 2002; 43(10): 1171 - 1181. [Abstract] [Full Text] [PDF]

				R. A. Sharrock and T. Clack Patterns of Expression and Normalized Levels of the Five Arabidopsis Phytochromes Plant Physiology, September 1, 2002; 130(1): 442 - 456. [Abstract] [Full Text] [PDF]

				T. Izawa, T. Oikawa, N. Sugiyama, T. Tanisaka, M. Yano, and K. Shimamoto Phytochrome mediates the external light signal to repress FT orthologs in photoperiodic flowering of rice Genes & Dev., August 1, 2002; 16(15): 2006 - 2020. [Abstract] [Full Text] [PDF]

				S. Kircher, P. Gil, L. Kozma-Bognar, E. Fejes, V. Speth, T. Husselstein-Muller, D. Bauer, E. Adam, E. Schafer, and F. Nagy Nucleocytoplasmic Partitioning of the Plant Photoreceptors Phytochrome A, B, C, D, and E Is Regulated Differentially by Light and Exhibits a Diurnal Rhythm PLANT CELL, July 1, 2002; 14(7): 1541 - 1555. [Abstract] [Full Text] [PDF]

				G. G. Simpson and C. Dean Arabidopsis, the Rosetta Stone of Flowering Time? Science, April 12, 2002; 296(5566): 285 - 289. [Abstract] [Full Text] [PDF]

				S.-i. Tanaka, N. Mochizuki, and A. Nagatani Expression of the AtGH3a Gene, an Arabidopsis Homologue of the Soybean GH3 Gene, is Regulated by Phytochrome B Plant Cell Physiol., March 1, 2002; 43(3): 281 - 289. [Abstract] [Full Text] [PDF]

				L. G. Luccioni, K. A. Oliverio, M. J. Yanovsky, H. E. Boccalandro, and J. J. Casal Brassinosteroid Mutants Uncover Fine Tuning of Phytochrome Signaling Plant Physiology, January 1, 2002; 128(1): 173 - 181. [Abstract] [Full Text] [PDF]

				L. Hennig, W. M. Stoddart, M. Dieterle, G. C. Whitelam, and E. Schafer Phytochrome E Controls Light-Induced Germination of Arabidopsis Plant Physiology, January 1, 2002; 128(1): 194 - 200. [Abstract] [Full Text] [PDF]

				M. J. Yanovsky, M. A. Mazzella, G. C. Whitelam, and J. J. Casal Resetting of the Circadian Clock by Phytochromes and Cryptochromes in Arabidopsis J Biol Rhythms, December 1, 2001; 16(6): 523 - 530. [Abstract] [PDF]

				E. R. Cober and H. D. Voldeng Low R:FR Light Quality Delays Flowering of E7E7 Soybean Lines Crop Sci., November 1, 2001; 41(6): 1823 - 1826. [Abstract] [Full Text] [PDF]

				J. M. Tepperman, T. Zhu, H.-S. Chang, X. Wang, and P. H. Quail Multiple transcription-factor genes are early targets of phytochrome A signaling PNAS, July 31, 2001; 98(16): 9437 - 9442. [Abstract] [Full Text] [PDF]

				M. A. Mazzella, P. D. Cerdan, R. J. Staneloni, and J. J. Casal Hierarchical coupling of phytochromes and cryptochromes reconciles stability and light modulation of Arabidopsis development Development, June 15, 2001; 128(12): 2291 - 2299. [Abstract] [Full Text] [PDF]

				X. L. Liu, M. F. Covington, C. Fankhauser, J. Chory, and D. R. Wagner ELF3 Encodes a Circadian Clock-Regulated Nuclear Protein That Functions in an Arabidopsis PHYB Signal Transduction Pathway PLANT CELL, June 1, 2001; 13(6): 1293 - 1304. [Abstract] [Full Text] [PDF]

				S. J. Davis, S. H. Bhoo, A. M. Durski, J. M. Walker, and R. D. Vierstra The Heme-Oxygenase Family Required for Phytochrome Chromophore Biosynthesis Is Necessary for Proper Photomorphogenesis in Higher Plants Plant Physiology, June 1, 2001; 126(2): 656 - 669. [Abstract] [Full Text] [PDF]

				L. Hennig, C. Poppe, U. Sweere, A. Martin, and E. Schäfer Negative Interference of Endogenous Phytochrome B with Phytochrome A Function in Arabidopsis Plant Physiology, February 1, 2001; 125(2): 1036 - 1044. [Abstract] [Full Text]

				B. L. Montgomery, K. A. Franklin, M. J. Terry, B. Thomas, S. D. Jackson, M. W. Crepeau, and J. C. Lagarias Biliverdin Reductase-Induced Phytochrome Chromophore Deficiency in Transgenic Tobacco Plant Physiology, January 1, 2001; 125(1): 266 - 277. [Abstract] [Full Text]

				P. F. Devlin and S. A. Kay Cryptochromes Are Required for Phytochrome Signaling to the Circadian Clock but Not for Rhythmicity PLANT CELL, December 1, 2000; 12(12): 2499 - 2510. [Abstract] [Full Text]

				C. Lin Photoreceptors and Regulation of Flowering Time Plant Physiology, May 1, 2000; 123(1): 39 - 50. [Full Text]

				J. W. Reed, P. Nagpal, R. M. Bastow, K. S. Solomon, M. J. Dowson-Day, R. P. Elumalai, and A. J. Millar Independent Action of ELF3 and phyB to Control Hypocotyl Elongation and Flowering Time Plant Physiology, April 1, 2000; 122(4): 1149 - 1160. [Abstract] [Full Text]

				G. Morelli and I. Ruberti Shade Avoidance Responses. Driving Auxin along Lateral Routes Plant Physiology, March 1, 2000; 122(3): 621 - 626. [Full Text] [PDF]

				M. M. Neff, C. Fankhauser, and J. Chory Light: an indicator of time and place Genes & Dev., February 1, 2000; 14(3): 257 - 271. [Full Text]

				M. A. Blázquez and D. Weigel Independent Regulation of Flowering by Phytochrome B and Gibberellins in Arabidopsis Plant Physiology, August 1, 1999; 120(4): 1025 - 1032. [Abstract] [Full Text]

				C. Fankhauser, K. Yeh, J. Clark, Lagarias, H. Zhang, T. D. Elich, and J. Chory PKS1, a Substrate Phosphorylated by Phytochrome That Modulates Light Signaling in Arabidopsis Science, May 28, 1999; 284(5419): 1539 - 1541. [Abstract] [Full Text]

				S. J. Davis, J. Kurepa, and R. D. Vierstra The Arabidopsis thaliana HY1 locus, required for phytochrome-chromophore biosynthesis, encodes a protein related to heme oxygenases PNAS, May 25, 1999; 96(11): 6541 - 6546. [Abstract] [Full Text] [PDF]

				K. J. Halliday, M. Hudson, M. Ni, M. Qin, and P. H. Quail poc1: An Arabidopsis mutant perturbed in phytochrome signaling because of a T DNA insertion in the promoter of PIF3, a gene encoding a phytochrome-interacting bHLH protein PNAS, May 11, 1999; 96(10): 5832 - 5837. [Abstract] [Full Text] [PDF]

				R. Yamaguchi, M. Nakamura, N. Mochizuki, S. A. Kay, and A. Nagatani Light-dependent Translocation of a Phytochrome B-GFP Fusion Protein to the Nucleus in Transgenic Arabidopsis J. Cell Biol., May 3, 1999; 145(3): 437 - 445. [Abstract] [Full Text] [PDF]

				P. F. Devlin, P. R.H. Robson, S. R. Patel, L. Goosey, R. A. Sharrock, and G. C. Whitelam Phytochrome D Acts in the Shade-Avoidance Syndrome in Arabidopsis by Controlling Elongation Growth and Flowering Time Plant Physiology, March 1, 1999; 119(3): 909 - 916. [Abstract] [Full Text]

				T. Mockler, H Guo, H Yang, H Duong, and C Lin Antagonistic actions of Arabidopsis cryptochromes and phytochrome B in the regulation of floral induction Development, January 5, 1999; 126(10): 2073 - 2082. [Abstract] [PDF]

				C. Fankhauser The Phytochromes, a Family of Red/Far-red Absorbing Photoreceptors J. Biol. Chem., April 6, 2001; 276(15): 11453 - 11456. [Full Text] [PDF]