Andrei Motchoulski, Emmanuel Liscum ^*

Phototropism of Arabidopsis thaliana seedlings in response to a blue light source is initiated by nonphototropic hypocotyl 1 (NPH1), a light-activated serine-threonine protein kinase. Mutations in three loci [NPH2, root phototropism 2 (RPT2), and NPH3] disrupt early signaling occurring downstream of the NPH1 photoreceptor. The NPH3 gene, now cloned, encodes a NPH1-interacting protein. NPH3 is a member of a large protein family, apparently specific to higher plants, and may function as an adapter or scaffold protein to bring together the enzymatic components of a NPH1-activated phosphorelay.

Division of Biological Sciences, University of Missouri, Columbia, MO 65211, USA.
^*   To whom correspondence should be addressed. E-mail: liscumm{at}missouri.edu

Phototropism: Translating light into directional growth.

T. Hohm, T. Preuten, and C. Fankhauser (2013)
Am. J. Botany 100, 47-59
 |  Abstract »  |  Full Text »  |  PDF »

Shoot phototropism in higher plants: New light through old concepts.

J. M. Christie and A. S. Murphy (2013)
Am. J. Botany 100, 35-46
 |  Abstract »  |  Full Text »  |  PDF »

A C-Terminal Membrane Association Domain of Phototropin 2 is Necessary for Chloroplast Movement.

S.-G. Kong, T. Kagawa, M. Wada, and A. Nagatani (2013)
Plant Cell Physiol. 54, 57-68
 |  Abstract »  |  Full Text »  |  PDF »

Antagonistic Regulation of Leaf Flattening by Phytochrome B and Phototropin in Arabidopsis thaliana.

T. Kozuka, N. Suetsugu, M. Wada, and A. Nagatani (2013)
Plant Cell Physiol. 54, 69-79
 |  Abstract »  |  Full Text »  |  PDF »

Role of RPT2 in Leaf Positioning and Flattening and a Possible Inhibition of phot2 Signaling by phot1.

A. Harada, A. Takemiya, S.-i. Inoue, T. Sakai, and K.-i. Shimazaki (2013)
Plant Cell Physiol. 54, 36-47
 |  Abstract »  |  Full Text »  |  PDF »

Photosensitivity of Kinase Activation by Blue Light Involves the Lifetime of a Cysteinyl-Flavin Adduct Intermediate, S390, in the Photoreaction Cycle of the LOV2 Domain in Phototropin, a Plant Blue Light Receptor.

K. Okajima, S. Kashojiya, and S. Tokutomi (2012)
J. Biol. Chem. 287, 40972-40981
 |  Abstract »  |  Full Text »  |  PDF »

PIN Auxin Efflux Carriers Are Necessary for Pulse-Induced But Not Continuous Light-Induced Phototropism in Arabidopsis.

K. Haga and T. Sakai (2012)
Plant Physiology 160, 763-776
 |  Abstract »  |  Full Text »  |  PDF »

The Light-Response BTB1 and BTB2 Proteins Assemble Nuclear Ubiquitin Ligases That Modify Phytochrome B and D Signaling in Arabidopsis.

M. J. Christians, D. J. Gingerich, Z. Hua, T. D. Lauer, and R. D. Vierstra (2012)
Plant Physiology 160, 118-134
 |  Abstract »  |  Full Text »  |  PDF »

The Role of a 14-3-3 Protein in Stomatal Opening Mediated by PHOT2 in Arabidopsis.

T.-S. Tseng, C. Whippo, R. P. Hangarter, and W. R. Briggs (2012)
PLANT CELL 24, 1114-1126
 |  Abstract »  |  Full Text »  |  PDF »

Nuclear Phytochrome A Signaling Promotes Phototropism in Arabidopsis.

C. Kami, M. Hersch, M. Trevisan, T. Genoud, A. Hiltbrunner, S. Bergmann, and C. Fankhauser (2012)
PLANT CELL 24, 566-576
 |  Abstract »  |  Full Text »  |  PDF »

The Signal Transducer NPH3 Integrates the Phototropin1 Photosensor with PIN2-Based Polar Auxin Transport in Arabidopsis Root Phototropism.

Y. Wan, J. Jasik, L. Wang, H. Hao, D. Volkmann, D. Menzel, S. Mancuso, F. Baluska, and J. Lin (2012)
PLANT CELL 24, 551-565
 |  Abstract »  |  Full Text »  |  PDF »

Tissue-Autonomous Promotion of Palisade Cell Development by Phototropin 2 in Arabidopsis.

T. Kozuka, S.-G. Kong, M. Doi, K.-i. Shimazaki, and A. Nagatani (2011)
PLANT CELL 23, 3684-3695
 |  Abstract »  |  Full Text »  |  PDF »

Modulation of Phototropic Responsiveness in Arabidopsis through Ubiquitination of Phototropin 1 by the CUL3-Ring E3 Ubiquitin Ligase CRL3NPH3.

D. Roberts, U. V. Pedmale, J. Morrow, S. Sachdev, E. Lechner, X. Tang, N. Zheng, M. Hannink, P. Genschik, and E. Liscum (2011)
PLANT CELL 23, 3627-3640
 |  Abstract »  |  Full Text »  |  PDF »

Rapid, Organ-Specific Transcriptional Responses to Light Regulate Photomorphogenic Development in Dicot Seedlings.

Y. Li, K. Swaminathan, and M. E. Hudson (2011)
Plant Physiology 156, 2124-2140
 |  Abstract »  |  Full Text »  |  PDF »

NPH3- and PGP-like genes are exclusively expressed in the apical tip region essential for blue-light perception and lateral auxin transport in maize coleoptiles.

S. Matsuda, T. Kajizuka, A. Kadota, T. Nishimura, and T. Koshiba (2011)
J. Exp. Bot. 62, 3459-3466
 |  Abstract »  |  Full Text »  |  PDF »

Polar-localized NPH3-like proteins regulate polarity and endocytosis of PIN-FORMED auxin efflux carriers.

M. Furutani, N. Sakamoto, S. Yoshida, T. Kajiwara, H. S. Robert, J. Friml, and M. Tasaka (2011)
Development 138, 2069-2078
 |  Abstract »  |  Full Text »  |  PDF »

Seven Things We Think We Know about Auxin Transport.

W. A. Peer, J. J. Blakeslee, H. Yang, and A. S. Murphy (2011)
Mol Plant 4, 487-504
 |  Abstract »  |  Full Text »  |  PDF »

A Negative Effector of Blue Light-Induced and Gravitropic Bending in Arabidopsis.

T. Knauer, M. Dummer, F. Landgraf, and C. Forreiter (2011)
Plant Physiology 156, 439-447
 |  Abstract »  |  Full Text »  |  PDF »

Functional Analyses of the Activation Loop of Phototropin2 in Arabidopsis.

S.-i. Inoue, T. Matsushita, Y. Tomokiyo, M. Matsumoto, K. I. Nakayama, T. Kinoshita, and K.-i. Shimazaki (2011)
Plant Physiology 156, 117-128
 |  Abstract »  |  Full Text »  |  PDF »

NPY Genes Play an Essential Role in Root Gravitropic Responses in Arabidopsis.

Y. Li, X. Dai, Y. Cheng, and Y. Zhao (2011)
Mol Plant 4, 171-179
 |  Abstract »  |  Full Text »  |  PDF »

The Arabidopsis PHYTOCHROME KINASE SUBSTRATE2 Protein Is a Phototropin Signaling Element That Regulates Leaf Flattening and Leaf Positioning.

M. de Carbonnel, P. Davis, M. R. G. Roelfsema, S.-i. Inoue, I. Schepens, P. Lariguet, M. Geisler, K.-i. Shimazaki, R. Hangarter, and C. Fankhauser (2010)
Plant Physiology 152, 1391-1405
 |  Abstract »  |  Full Text »  |  PDF »

Domain Swapping to Assess the Mechanistic Basis of Arabidopsis Phototropin 1 Receptor Kinase Activation and Endocytosis by Blue Light.

E. Kaiserli, S. Sullivan, M. A. Jones, K. A. Feeney, and J. M. Christie (2009)
PLANT CELL 21, 3226-3244
 |  Abstract »  |  Full Text »  |  PDF »

Understanding phototropism: from Darwin to today.

J. J. Holland, D. Roberts, and E. Liscum (2009)
J. Exp. Bot. 60, 1969-1978
 |  Abstract »  |  Full Text »  |  PDF »

The guard cell as a single-cell model towards understanding drought tolerance and abscisic acid action.

C. Sirichandra, A. Wasilewska, F. Vlad, C. Valon, and J. Leung (2009)
J. Exp. Bot. 60, 1439-1463
 |  Abstract »  |  Full Text »  |  PDF »

NPY genes and AGC kinases define two key steps in auxin-mediated organogenesis in Arabidopsis.

Y. Cheng, G. Qin, X. Dai, and Y. Zhao (2008)
PNAS 105, 21017-21022
 |  Abstract »  |  Full Text »  |  PDF »

Cell Polarity Signaling: Focus on Polar Auxin Transport.

X. Gao, S. Nagawa, G. Wang, and Z. Yang (2008)
Mol Plant
 |  Abstract »  |  Full Text »  |  PDF »

An Inositol Polyphosphate 5-Phosphatase Functions in PHOTOTROPIN1 Signaling in Arabidopis by Altering Cytosolic Ca2+.

X. Chen, W.-H. Lin, Y. Wang, S. Luan, and H.-W. Xue (2008)
PLANT CELL 20, 353-366
 |  Abstract »  |  Full Text »  |  PDF »

Leaf Positioning of Arabidopsis in Response to Blue Light.

S.-i. Inoue, T. Kinoshita, A. Takemiya, M. Doi, and K.-i. Shimazaki (2008)
Mol Plant 1, 15-26
 |  Abstract »  |  Full Text »  |  PDF »

The Subcellular Localization and Blue-Light-Induced Movement of Phototropin 1-GFP in Etiolated Seedlings of Arabidopsis thalianaw.

Y.-L. Wan, W. Eisinger, D. Ehrhardt, U. Kubitscheck, F. Baluska, and W. Briggs (2008)
Mol Plant 1, 103-117
 |  Abstract »  |  Full Text »  |  PDF »

Disruptions in AUX1-Dependent Auxin Influx Alter Hypocotyl Phototropism in Arabidopsis.

B. B. Stone, E. L. Stowe-Evans, R. M. Harper, R. B. Celaya, K. Ljung, G. Sandberg, and E. Liscum (2008)
Mol Plant 1, 129-144
 |  Abstract »  |  Full Text »  |  PDF »

PHYTOCHROME KINASE SUBSTRATE1 Regulates Root Phototropism and Gravitropism.

H. E. Boccalandro, S. N. De Simone, A. Bergmann-Honsberger, I. Schepens, C. Fankhauser, and J. J. Casal (2008)
Plant Physiology 146, 108-115
 |  Abstract »  |  Full Text »  |  PDF »

NPY1, a BTB-NPH3-like protein, plays a critical role in auxin-regulated organogenesis in Arabidopsis.

Y. Cheng, G. Qin, X. Dai, and Y. Zhao (2007)
PNAS 104, 18825-18829
 |  Abstract »  |  Full Text »  |  PDF »

The gene MACCHI-BOU 4/ENHANCER OF PINOID encodes a NPH3-like protein and reveals similarities between organogenesis and phototropism at the molecular level.

M. Furutani, T. Kajiwara, T. Kato, B. S. Treml, C. Stockum, R. A. Torres-Ruiz, and M. Tasaka (2007)
Development 134, 3849-3859
 |  Abstract »  |  Full Text »  |  PDF »

Large-Scale, Lineage-Specific Expansion of a Bric-a-Brac/Tramtrack/Broad Complex Ubiquitin-Ligase Gene Family in Rice.

D. J. Gingerich, K. Hanada, S.-H. Shiu, and R. D. Vierstra (2007)
PLANT CELL 19, 2329-2348
 |  Abstract »  |  Full Text »  |  PDF »

Regulation of Phototropic Signaling in Arabidopsis via Phosphorylation State Changes in the Phototropin 1-interacting Protein NPH3.

U. V. Pedmale and E. Liscum (2007)
J. Biol. Chem. 282, 19992-20001
 |  Abstract »  |  Full Text »  |  PDF »

A citrus abscission agent induces anoxia- and senescence-related gene expression in Arabidopsis.

F. Alferez, G. Y. Zhong, and J. K. Burns (2007)
J. Exp. Bot. 58, 2451-2462
 |  Abstract »  |  Full Text »  |  PDF »

Ubiquitin, Hormones and Biotic Stress in Plants.

K. Dreher and J. Callis (2007)
Ann. Bot. 99, 787-822
 |  Abstract »  |  Full Text »  |  PDF »

Protein phosphatase 1 positively regulates stomatal opening in response to blue light in Vicia faba.

A. Takemiya, T. Kinoshita, M. Asanuma, and K.-i. Shimazaki (2006)
PNAS 103, 13549-13554
 |  Abstract »  |  Full Text »  |  PDF »

Gene profiling of the red light signalling pathways in roots.

M. L. Molas, J. Z. Kiss, and M. J. Correll (2006)
J. Exp. Bot. 57, 3217-3229
 |  Abstract »  |  Full Text »  |  PDF »

PHYTOCHROME KINASE SUBSTRATE 1 is a phototropin 1 binding protein required for phototropism.

P. Lariguet, I. Schepens, D. Hodgson, U. V. Pedmale, M. Trevisan, C. Kami, M. de Carbonnel, J. M. Alonso, J. R. Ecker, E. Liscum, et al. (2006)
PNAS 103, 10134-10139
 |  Abstract »  |  Full Text »  |  PDF »

Phototropism: Bending towards Enlightenment.

C. W. Whippo and R. P. Hangarter (2006)
PLANT CELL 18, 1110-1119
 |  Full Text »  |  PDF »

An Auxilin-Like J-Domain Protein, JAC1, Regulates Phototropin-Mediated Chloroplast Movement in Arabidopsis.

N. Suetsugu, T. Kagawa, and M. Wada (2005)
Plant Physiology 139, 151-162
 |  Abstract »  |  Full Text »  |  PDF »

A Plant-Specific Protein Essential for Blue-Light-Induced Chloroplast Movements.

S. L. DeBlasio, D. L. Luesse, and R. P. Hangarter (2005)
Plant Physiology 139, 101-114
 |  Abstract »  |  Full Text »  |  PDF »

A Brassinosteroid-Hypersensitive Mutant of BAK1 Indicates That a Convergence of Photomorphogenic and Hormonal Signaling Modulates Phototropism.

C. W. Whippo and R. P. Hangarter (2005)
Plant Physiology 139, 448-457
 |  Abstract »  |  Full Text »  |  PDF »

Isolation of a Protein Interacting with Vfphot1a in Guard Cells of Vicia faba.

T. Emi, T. Kinoshita, K. Sakamoto, Y. Mineyuki, and K.-i. Shimazaki (2005)
Plant Physiology 138, 1615-1626
 |  Abstract »  |  Full Text »  |  PDF »

Cullins 3a and 3b Assemble with Members of the Broad Complex/Tramtrack/Bric-a-Brac (BTB) Protein Family to Form Essential Ubiquitin-Protein Ligases (E3s) in Arabidopsis.

D. J. Gingerich, J. M. Gagne, D. W. Salter, H. Hellmann, M. Estelle, L. Ma, and R. D. Vierstra (2005)
J. Biol. Chem. 280, 18810-18821
 |  Abstract »  |  Full Text »  |  PDF »

Arabidopsis Has Two Redundant Cullin3 Proteins That Are Essential for Embryo Development and That Interact with RBX1 and BTB Proteins to Form Multisubunit E3 Ubiquitin Ligase Complexes in Vivo.

P. Figueroa, G. Gusmaroli, G. Serino, J. Habashi, L. Ma, Y. Shen, S. Feng, M. Bostick, J. Callis, H. Hellmann, et al. (2005)
PLANT CELL 17, 1180-1195
 |  Abstract »  |  Full Text »  |  PDF »

The Rice COLEOPTILE PHOTOTROPISM1 Gene Encoding an Ortholog of Arabidopsis NPH3 Is Required for Phototropism of Coleoptiles and Lateral Translocation of Auxin.

K. Haga, M. Takano, R. Neumann, and M. Iino (2005)
PLANT CELL 17, 103-115
 |  Abstract »  |  Full Text »  |  PDF »

ARIA, an Arabidopsis Arm Repeat Protein Interacting with a Transcriptional Regulator of Abscisic Acid-Responsive Gene Expression, Is a Novel Abscisic Acid Signaling Component.

S. Kim, H.-i. Choi, H.-J. Ryu, J. H. Park, M. D. Kim, and S. Y. Kim (2004)
Plant Physiology 136, 3639-3648
 |  Abstract »  |  Full Text »  |  PDF »

Identification of ASK and clock-associated proteins as molecular partners of LKP2 (LOV kelch protein 2) in Arabidopsis.

M. Yasuhara, S. Mitsui, H. Hirano, R. Takanabe, Y. Tokioka, N. Ihara, A. Komatsu, M. Seki, K. Shinozaki, and T. Kiyosue (2004)
J. Exp. Bot. 55, 2015-2027
 |  Abstract »  |  Full Text »  |  PDF »

Analysis of Transposon Insertion Mutants Highlights the Diversity of Mechanisms Underlying Male Progamic Development in Arabidopsis.

E. Lalanne, C. Michaelidis, J. M. Moore, W. Gagliano, A. Johnson, R. Patel, R. Howden, J.-P. Vielle-Calzada, U. Grossniklaus, and D. Twell (2004)
Genetics 167, 1975-1986
 |  Abstract »  |  Full Text »  |  PDF »

Localization of the Blue-Light Receptor Phototropin to the Flagella of the Green Alga Chlamydomonas reinhardtii.

K. Huang, T. Kunkel, and C. F. Beck (2004)
Mol. Biol. Cell 15, 3605-3614
 |  Abstract »  |  Full Text »  |  PDF »

RPT2 Is a Signal Transducer Involved in Phototropic Response and Stomatal Opening by Association with Phototropin 1 in Arabidopsis thaliana.

S. Inada, M. Ohgishi, T. Mayama, K. Okada, and T. Sakai (2004)
PLANT CELL 16, 887-896
 |  Abstract »  |  Full Text »  |  PDF »

High Pigment1 Mutation Negatively Regulates Phototropic Signal Transduction in Tomato Seedlings.

A. Srinivas, R. K. Behera, T. Kagawa, M. Wada, and R. Sharma (2004)
Plant Physiology 134, 790-800
 |  Abstract »  |  Full Text »  |  PDF »

Relocalization of the PIN1 Auxin Efflux Facilitator Plays a Role in Phototropic Responses.

J. J. Blakeslee, A. Bandyopadhyay, W. A. Peer, S. N. Makam, and A. S. Murphy (2004)
Plant Physiology 134, 28-31
 |  Full Text »  |  PDF »

Blue Light Signaling through the Cryptochromes and Phototropins. So That's What the Blues Is All About.

E. Liscum, D. W. Hodgson, and T. J. Campbell (2003)
Plant Physiology 133, 1429-1436
 |  Full Text »

Blue-Light- and Phosphorylation-Dependent Binding of a 14-3-3 Protein to Phototropins in Stomatal Guard Cells of Broad Bean.

T. Kinoshita, T. Emi, M. Tominaga, K. Sakamoto, A. Shigenaga, M. Doi, and K.-i. Shimazaki (2003)
Plant Physiology 133, 1453-1463
 |  Abstract »  |  Full Text »

Primary Inhibition of Hypocotyl Growth and Phototropism Depend Differently on Phototropin-Mediated Increases in Cytoplasmic Calcium Induced by Blue Light.

K. M. Folta, E. J. Lieg, T. Durham, and E. P. Spalding (2003)
Plant Physiology 133, 1464-1470
 |  Abstract »  |  Full Text »

A Genomic Analysis of the Shade Avoidance Response in Arabidopsis.

P. F. Devlin, M. J. Yanovsky, and S. A. Kay (2003)
Plant Physiology 133, 1617-1629
 |  Abstract »  |  Full Text »

Summaries of National Science Foundation-Sponsored Arabidopsis 2010 Projects and National Science Foundation-Sponsored Plant Genome Projects That Are Generating Arabidopsis Resources for the Community.

F. M. Ausubel (2002)
Plant Physiology 129, 394-437
 |  Full Text »  |  PDF »

Photoexcited Structure of a Plant Photoreceptor Domain Reveals a Light-Driven Molecular Switch.

S. Crosson and K. Moffat (2002)
PLANT CELL 14, 1067-1075
 |  Abstract »  |  Full Text »  |  PDF »

Blue Light Receptors and Signal Transduction.

C. Lin (2002)
PLANT CELL 14, S207-S225
 |  Full Text »  |  PDF »

Plant Photobiology 2001: A Thousand Points of Enlightenment from Receptor Structures to Ecological Adaptation.

T. J. Campbell and E. Liscum (2001)
PLANT CELL 13, 1704-1710
 |  Full Text »  |  PDF »

The Enhancement of Phototropin-Induced Phototropic Curvature in Arabidopsis Occurs via a Photoreversible Phytochrome A-Dependent Modulation of Auxin Responsiveness.

E. L. Stowe-Evans, D. R. Luesse, and E. Liscum (2001)
Plant Physiology 126, 826-834
 |  Abstract »  |  Full Text »  |  PDF »

Blue Light Sensing in Higher Plants.

J. M. Christie and W. R. Briggs (2001)
J. Biol. Chem. 276, 11457-11460
 |  Full Text »  |  PDF »

Arabidopsis NPL1: A Phototropin Homolog Controlling the Chloroplast High-Light Avoidance Response.

T. Kagawa, T. Sakai, N. Suetsugu, K. Oikawa, S. Ishiguro, T. Kato, S. Tabata, K. Okada, and M. Wada (2001)
Science 291, 2138-2141
 |  Abstract »  |  Full Text »

Structure of a flavin-binding plant photoreceptor domain: Insights into light-mediated signal transduction.

S. Crosson and K. Moffat (2001)
PNAS 98, 2995-3000
 |  Abstract »  |  Full Text »  |  PDF »

Photoreceptors in Plant Photomorphogenesis to Date. Five Phytochromes, Two Cryptochromes, One Phototropin, and One Superchrome.

W. R. Briggs and M. A. Olney (2001)
Plant Physiology 125, 85-88
 |  Full Text »

Arabidopsis Research 2000.

S. Abel, M. Blazquez, J. Dangl, X. W. Deng, I. Graham, J. Harada, J. Jones, and O. Nilsson (2000)
PLANT CELL 12, 2302-2308
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RPT2: A Signal Transducer of the Phototropic Response in Arabidopsis.

T. Sakai, T. Wada, S. Ishiguro, and K. Okada (2000)
PLANT CELL 12, 225-236
 |  Abstract »  |  Full Text »  |  PDF »

Blue Light Sensing in Higher Plants.

J. M. Christie and W. R. Briggs (2001)
J. Biol. Chem. 276, 11457-11460
 |  Full Text »  |  PDF »

Structure of a flavin-binding plant photoreceptor domain: Insights into light-mediated signal transduction.

S. Crosson and K. Moffat (2001)
PNAS 98, 2995-3000
 |  Abstract »  |  Full Text »  |  PDF »