Phototropism in land plants: Molecules and mechanism from light perception to response

Abstract

BACKGROUND: Phototropism is the response a plant exhibits when it is faced with a directional blue light stimulus. Though a seemingly simple differential cell elongation response within a responding tissue that results in organ curvature, phototropism is regulated through a complex set of signal perception and transduction events that move from the plasma membrane to the nucleus. In nature phototropism is one of several plant responses that have evolved to optimize photosynthesis and growth.

OBJECTIVE: In the present work we will review the state of the field with respect to the molecules and mechanisms associated with phototropism in land plants.

METHODS: A systematic literature search was done to identify relevant advances in the field. Though we tried to focus on literature within the past decade (1998-present), we have discussed and cited older literature where appropriate because of context or its significant impact to the present field. Several previous review articles are also cited where appropriate and readers should seek those out.

RESULTS: A total of 199 articles are cited that fulfill the criteria listed above.

CONCLUSIONS: Though important numerous and significant advances have been made in our understanding of the molecular, biochemical, cell biological and physiologic mechanisms underlying phototropism in land plants over the past decade, there are many remaining unanswered questions. The future is indeed bright for researchers in the field and we look forward to the next decade worth of discoveries.

Keywords

phototropism / phototropin / phytochrome / crytochrome / auxin / auxin response factor / phosphorylation / ubiquitination / transcriptional control / cell elongation / growth / non-phototropic hypocotyl 3 / NPH3/RPT2-like / protein kinase / calcium

References

[1] Aggarwal C, Banaś A K, Kasprowicz-Maluśki A, Borghetti C, Łabuz J, Dobrucki J, Gabryś H (2014). Blue-light-activated phototropin2 trafficking from the cytoplasm to Golgi/post-Golgi vesicles. J Exp Bot, 65(12): 3263–3276

[2] Ahmad M, Cashmore A R (1993). HY4 gene of A. thaliana encodes a protein with characteristics of a blue-light photoreceptor. Nature, 366(6451): 162–166

[3] Ahmad M, Jarillo J A, Cashmore A R, Ahmad M, Jarillo J A, Cashmore A R (1998). Chimeric proteins between cry1 and cry2 Arabidopsis blue light photoreceptors indicate overlapping functions and varying protein stability. Plant Cell, 10(2): 197–207

[4] Askinosie S (2016). Blue light- and ubiquitin-dependent influence on phototropin 1 abundance and movement at the plasma membrane. PhD Dissertation, University of Missouri-Columbia, pp. 161

[5] Babourina O, Godfrey L, Voltchanskii K (2004). Changes in ion fluxes during phototropic bending of etiolated oat coleoptiles. Ann Bot, 94(1): 187–194

[6] Baum G, Long J C, Jenkins G I, Trewavas A J (1999). Stimulation of the blue light phototropic receptor NPH1 causes a transient increase in cytosolic Ca²⁺. Proc Natl Acad Sci USA, 96(23): 13554–13559

[7] Benjamins R, Ampudia C S, Hooykaas P J, Offringa R (2003). PINOID-mediated signaling involves calcium-binding proteins. Plant Physiol, 132(3): 1623–1630

[8] Bennett M J, Marchant A, Green H G, May S T, Sally P, Millner P A, Walker A R, Schulz B, Feldmann K A (1996). Arabidopsis AUX1 gene: A permease-like regulator of root gravitropism. Science, 273(5277), 948–950.

[9] Bennett S R M, Alvarez J, Bossinger G, Smyth D R (1995). Morphogenesis in pinoid mutants of Arabidopsis thaliana. Plant J, 8(4): 505–520

[10] Bennett T (2015). PIN proteins and the evolution of plant development. Trends Plant Sci, 20(8): 498–507

[11] Blakeslee J J, Bandyopadhyay A, Peer W A, Makam S N, Murphy A S (2004). Relocalization of the PIN1 auxin efflux facilitator plays a role in phototropic responses. Plant Physiol, 134(1): 28–31

[12] Boer D R, Freire-Rios A, van den Berg W A M, Saaki T, Manfield I W, Kepinski S, López-Vidrieo I, Franco-Zorrilla J M, de Vries S C, Solano R, Weijers D, Coll M (2014). Structural basis for DNA binding specificity by the auxin-dependent ARF transcription factors. Cell, 156(3): 577–589

[13] Bögre L, Okrész L, Henriques R, Anthony R G (2003). Growth signalling pathways in Arabidopsis and the AGC protein kinases. Trends Plant Sci, 8(9): 424–431

[14] Borner G H H, Lilley K S, Stevens T J, Dupree P (2003). Identification of glycosylphosphatidylinositol-anchored proteins in Arabidopsis. A proteomic and genomic analysis. Plant Physiol, 132(2): 568–577

[15] Briggs W R, Huala E (1999). Blue-light photoreceptors in higher plants. Annu Rev Cell Dev Biol, 15(1): 33–62

[16] Carretero-Paulet L, Galstyan A, Roig-Villanova I, Martínez-García J F, Bilbao-Castro J R, Robertson D L (2010). Genome-wide classification and evolutionary analysis of the bHLH family of transcription factors in Arabidopsis, poplar, rice, moss, and algae. Plant Physiol, 153(3): 1398–1412

[17] Chaves I, Pokorny R, Byrdin M, Hoang N, Ritz T, Brettel K, Essen L O, van der Horst G T, Batschauer A, Ahmad M (2011). The cryptochromes: blue light photoreceptors in plants and animals. Annu Rev Plant Biol, 62(1): 335–364

[18] Chen L, Hellmann H (2013). Plant E3 ligases: flexible enzymes in a sessile world. Mol Plant, 6(5): 1388–1404

[19] Cheng Y, Qin G, Dai X, Zhao Y (2007). NPY1, a BTB-NPH3-like protein, plays a critical role in auxin-regulated organogenesis in Arabidopsis. Proc Natl Acad Sci USA, 104(47): 18825–18829

[20] Cheng Y, Qin G, Dai X, Zhao Y (2008). NPY genes and AGC kinases define two key steps in auxin-mediated organogenesis in Arabidopsis. Proc Natl Acad Sci USA, 105(52): 21017–21022

[21] Cho M, Lee S H, Cho H T (2007). P-glycoprotein4 displays auxin efflux transporter-like action in Arabidopsis root hair cells and tobacco cells. Plant Cell, 19(12): 3930–3943

[22] Christensen S K, Dagenais N, Chory J, Weigel D (2000). Regulation of auxin response by the protein kinase PINOID. Cell, 100(4): 469–478

[23] Christie J M, Reymond P, Powell G K, Bernasconi P, Raibekas A A, Liscum E, Briggs W R (1998). Arabidopsis NPH1: a flavoprotein with the properties of a photoreceptor for phototropism. Science, 282(5394): 1698–1701

[24] Christie J M, Salomon M, Nozue K, Wada M, Briggs W R (1999). LOV (light, oxygen, or voltage) domains of the blue-light photoreceptor phototropin (nph1): binding sites for the chromophore flavin mononucleotide. Proc Natl Acad Sci USA, 96(15): 8779–8783

[25] Christie J M, Suetsugu N, Sullivan S, Wada M (2018). Shining light on the function of NPH3/RPT2-Like proteins in phototropin signalling. Plant Physiol, 176(2): 1015–1024

[26] Christie J M, Yang H, Richter G L, Sullivan S, Thomson C E, Lin J, Titapiwatanakun B, Ennis M, Kaiserli E, Lee O R, Adamec J, Peer W A, Murphy A S (2011). phot1 inhibition of ABCB19 primes lateral auxin fluxes in the shoot apex required for phototropism. PLoS Biol, 9(6): e1001076

[27] Clack T, Mathews S, Sharrock R A (1994). The phytochrome apoprotein family in Arabidopsis is encoded by five genes: the sequences and expression of PHYD and PHYE. Plant Mol Biol, 25(3): 413–427

[28] Crosson S, Rajagopal S, Moffat K (2003). The LOV domain family: photoresponsive signaling modules coupled to diverse output domains. Biochemistry, 42(1): 2–10

[29] Darwin C (1880). The Power of Movement in Plants. (London: John Murray Publishers).

[30] de Carbonnel M, Davis P, Roelfsema M R G, Inoue S, Schepens I, Lariguet P, Geisler M, Shimazaki K, Hangarter R, Fankhauser C (2010). The Arabidopsis PHYTOCHROME KINASE SUBSTRATE2 protein is a phototropin signaling element that regulates leaf flattening and leaf positioning. Plant Physiol, 152(3): 1391–1405

[31] DeBlasio S L, Mullen J L, Luesse D R, Hangarter R P (2003). Phytochrome modulation of blue light-induced chloroplast movements in Arabidopsis. Plant Physiol, 133(4): 1471–1479

[32] Demarsy E, Schepens I, Okajima K, Hersch M, Bergmann S, Christie J, Shimazaki K, Tokutomi S, Fankhauser C (2012). Phytochrome Kinase Substrate 4 is phosphorylated by the phototropin 1 photoreceptor. EMBO J, 31(16): 3457–3467

[33] Deshaies R J, Joazeiro C A (2009). RING domain E3 ubiquitin ligases. Annu Rev Biochem, 78(1): 399–434

[34] Dezfulian M H, Jalili E, Roberto D K A, Moss B L, Khoo K, Nemhauser J L, Crosby W L (2016). Oligomerization of SCF^TIR1 is essential for Aux/IAA degradation and auxin signaling in Arabidopsis. PLoS Genet, 12(9): e1006301

[35] Ding Z, Galván-Ampudia C S, Demarsy E, Łangowski Ł, Kleine-Vehn J, Fan Y, Morita M T, Tasaka M, Fankhauser C, Offringa R, Friml J (2011). Light-mediated polarization of the PIN3 auxin transporter for the phototropic response in Arabidopsis. Nat Cell Biol, 13(4): 447–452

[36] Doherty G J, McMahon H T (2009). Mechanisms of endocytosis. Annu Rev Biochem, 78(1): 857–902

[37] Dümmer M, Michalski C, Essen L O, Rath M, Galland P, Forreiter C (2016). EHB1 and AGD12, two calcium-dependent proteins affect gravitropism antagonistically in Arabidopsis thaliana. J Plant Physiol, 206: 114–124

[38] Esmon C A, Tinsley A G, Ljung K, Sandberg G, Hearne L B, Liscum E (2006). A gradient of auxin and auxin-dependent transcription precedes tropic growth responses. Proc Natl Acad Sci USA, 103(1): 236–241

[39] Fankhauser C (2001). The phytochromes, a family of red/far-red absorbing photoreceptors. J Biol Chem, 276(15): 11453–11456

[40] Fankhauser C, Yeh K C, Lagarias J C, Zhang H, Elich T D, Chory J (1999). PKS1, a substrate phosphorylated by phytochrome that modulates light signaling in Arabidopsis. Science, 284(5419): 1539–1541

[41] Felle H (1988). Auxin causes oscillations of cytosolic free calcium and pH in Zea mays coleoptiles. Planta, 174(4): 495–499

[42] Figueroa P, Gusmaroli G, Serino G, Habashi J, Ma L, Shen Y, Feng S, Bostick M, Callis J, Hellmann H, Deng X W (2005). 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. Plant Cell, 17(4): 1180–1195

[43] Folta K M, Lieg E J, Durham T, Spalding E P (2003). Primary inhibition of hypocotyl growth and phototropism depend differently on phototropin-mediated increases in cytoplasmic calcium induced by blue light. Plant Physiol, 133(4): 1464–1470

[44] Franklin K A, Quail P H (2010). Phytochrome functions in Arabidopsis development. J Exp Bot, 61(1): 11–24

[45] Friml J, Wiśniewska J, Benková E, Mendgen K, Palme K (2002). Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature, 415(6873): 806–809

[46] Friml J, Yang X, Michniewicz M, Weijers D, Quint A, Tietz O, Benjamins R, Ouwerkerk P B, Ljung K, Sandberg G, Hooykaas P J, Palme K, Offringa R (2004). A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science, 306(5697): 862–865

[47] Furutani M, Kajiwara T, Kato T, Treml B S, Stockum C, Torres-Ruiz R A, Tasaka M (2007). The gene MACCHI-BOU 4/ENHANCER OF PINOID encodes a NPH3-like protein and reveals similarities between organogenesis and phototropism at the molecular level. Development, 134(21): 3849–3859

[48] Gehring C A, Williams D A, Cody S H, Parish R W (1990). Phototropism and geotropism in maize coleoptiles are spatially correlated with increases in cytosolic free calcium. Nature, 345(6275): 528–530

[49] Geldner N, Anders N, Wolters H, Keicher J, Kornberger W, Muller P, Delbarre A, Ueda T, Nakano A, Jürgens G (2003b). The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell, 112(2): 219–230

[50] Geldner N, Richter S, Vieten A, Marquardt S, Torres-Ruiz R A, Mayer U, Jürgens G (2004a). Partial loss-of-function alleles reveal a role for GNOM in auxin transport-related, post-embryonic development of Arabidopsis. Development, 131(2): 389–400

[51] Genschik P, Sumara I, Lechner E (2013). The emerging family of CULLIN3-RING ubiquitin ligases (CRL3s): cellular functions and disease implications. EMBO J, 32(17): 2307–2320

[52] Grones P, Friml J (2015). Auxin transporters and binding proteins at a glance. J Cell Sci, 128(1): 1–7

[53] Grunewald W, Friml J (2010). The march of the PINs: developmental plasticity by dynamic polar targeting in plant cells. EMBO J, 29(16): 2700–2714

[54] Guilfoyle T J (2015). The PB1 domain in auxin response factor and Aux/IAA proteins: a versatile protein interaction module in the auxin response. Plant Cell, 27(1): 33–43

[55] Ha C M, Jun J H, Fletcher J C (2010). Shoot apical meristem form and function. Curr Top Dev Biol, 91(C): 103–140

[56] Haga K, Frank L, Kimura T, Schwechheimer C, Sakai T (2018). Roles of AGCVIII kinases in the hypocotyl phototropism of Arabidopsis seedlings. Plant Cell Physiol, 59(5): 1060–1071

[57] Haga K, Takano M, Neumann R, Iino M (2005). The Rice COLEOPTILE PHOTOTROPISM1 gene encoding an ortholog of Arabidopsis NPH3 is required for phototropism of coleoptiles and lateral translocation of auxin. Plant Cell, 17(1): 103–115

[58] Haga K, Tsuchida-Mayama T, Yamada M, Sakai T (2015). Arabidopsis ROOT PHOTOTROPISM2 contributes to the adaptation to high-intensity light in phototropic responses. Plant Cell, 27(4): 1098–1112

[59] Haglund K, Dikic I (2005). Ubiquitylation and cell signaling. EMBO J, 24(19): 3353–3359

[60] Han I S, Cho H Y, Moni A, Lee A Y, Briggs W R (2013). Investigations on the photoregulation of chloroplast movement and leaf positioning in Arabidopsis. Plant Cell Physiol, 54(1): 48–56

[61] Han I S, Tseng T S, Eisinger W, Briggs W R (2008). Phytochrome A regulates the intracellular distribution of phototropin 1-green fluorescent protein in Arabidopsis thaliana. Plant Cell, 20(10): 2835–2847

[62] Han M, Park Y, Kim I, Kim E H, Yu T K, Rhee S, Suh J Y (2014). Structural basis for the auxin-induced transcriptional regulation by Aux/IAA17. Proc Natl Acad Sci USA, 111(52): 18613–18618

[63] Harada A, Sakai T, Okada K (2003). Phot1 and phot2 mediate blue light-induced transient increases in cytosolic Ca²⁺ differently in Arabidopsis leaves. Proc Natl Acad Sci USA, 100(14): 8583–8588

[64] Harada A, Shimazaki K (2007). Phototropins and blue light-dependent calcium signaling in higher plants. Photochem Photobiol, 83(1): 102–111

[65] Harada A, Takemiya A, Inoue S, Sakai T, Shimazaki K (2013). Role of RPT2 in leaf positioning and flattening and a possible inhibition of phot2 signaling by phot1. Plant Cell Physiol, 54(1): 36–47

[66] Harper R M, Stowe-Evans E L, Luesse D R, Muto H, Tatematsu K, Watahiki M K, Yamamoto K, Liscum E (2000). The NPH4 locus encodes the auxin response factor ARF7, a conditional regulator of differential growth in aerial Arabidopsis tissue. Plant Cell, 12(5): 757–770

[67] Harper S M, Christie J M, Gardner K H (2004). Disruption of the LOV-Jalpha helix interaction activates phototropin kinase activity. Biochemistry, 43(51): 16184–16192

[68] Holland J J, Roberts D, Liscum E (2009). Understanding phototropism: from Darwin to today. J Exp Bot, 60(7): 1969–1978

[69] Hotton S K, Callis J (2008). Regulation of cullin RING ligases. Annu Rev Plant Biol, 59(1): 467–489

[70] Huala E, Oeller P W, Liscum E, Han I S, Larsen E, Briggs W R (1997). Arabidopsis NPH1: a protein kinase with a putative redox-sensing domain. Science, 278(5346): 2120–2123

[71] Huang F, Zago M K, Abas L, van Marion A, Galván-Ampudia C S, Offringa R (2010). Phosphorylation of conserved PIN motifs directs Arabidopsis PIN1 polarity and auxin transport. Plant Cell, 22(4): 1129–1142

[72] Hughes J (2013). Phytochrome cytoplasmic signaling. Annu Rev Plant Biol, 64(1): 377–402

[73] Inada S, Ohgishi M, Mayama T, Okada K, Sakai T (2004). RPT2 is a signal transducer involved in phototropic response and stomatal opening by association with phototropin 1 in Arabidopsis thaliana. Plant Cell, 16(4): 887–896

[74] Inoue S, Kinoshita T, Matsumoto M, Nakayama K I, Doi M, Shimazaki K (2008). Blue light-induced autophosphorylation of phototropin is a primary step for signaling. Proc Natl Acad Sci USA, 105(14): 5626–5631

[75] Inoue S, Kinoshita T, Takemiya A, Doi M, Shimazaki K (2008). Leaf positioning of Arabidopsis in response to blue light. Mol Plant, 1(1): 15–26

[76] Inoue S, Matsushita T, Tomokiyo Y, Matsumoto M, Nakayama K I, Kinoshita T, Shimazaki K (2011). Functional analyses of the activation loop of phototropin2 in Arabidopsis. Plant Physiol, 156(1): 117–128

[77] Jaedicke K, Lichtenthäler A L, Meyberg R, Zeidler M, Hughes J (2012). A phytochrome-phototropin light signaling complex at the plasma membrane. Proc Natl Acad Sci USA, 109(30): 12231–12236

[78] Janoudi A K, Gordon W R, Wagner D, Quail P, Poff K L (1997). Multiple phytochromes are involved in red-light-induced enhancement of first-positive phototropism in Arabidopsis thaliana. Plant Physiol, 113(3): 975–979

[79] Janoudi A K, Poff K L (1993). Desensitization and recovery of phototropic responsiveness in Arabidopsis thaliana. Plant Physiol, 101(101): 1175–1180

[80] Janoudi A-K, Konjevic R, Apel P, Poff K L (1992). Time threshold for second positive phototropism is decreased by a preirradiation with red light. Plant Physiol, 99(4): 1422–1425

[81] Jarillo J A, Gabrys H, Capel J, Alonso J M, Ecker J R, Cashmore A R (2001). Phototropin-related NPL1 controls chloroplast relocation induced by blue light. Nature, 410(6831): 952–954

[82] Jones M A, Feeney K A, Kelly S M, Christie J M (2007). Mutational analysis of phototropin 1 provides insights into the mechanism underlying LOV2 signal transmission. J Biol Chem, 282(9): 6405–6414

[83] Kagawa T, Sakai T, Suetsugu N, Oikawa K, Ishiguro S, Kato T, Tabata S, Okada K, Wada M (2001). Arabidopsis NPL1: a phototropin homolog controlling the chloroplast high-light avoidance response. Science, 291(5511): 2138–2141

[84] Kaiserli E, Sullivan S, Jones M A, Feeney K A, Christie J M (2009). Domain swapping to assess the mechanistic basis of Arabidopsis phototropin 1 receptor kinase activation and endocytosis by blue light. Plant Cell, 21(10): 3226–3244

[85] Kami C, Allenbach L, Zourelidou M, Ljung K, Schütz F, Isono E, Watahiki M K, Yamamoto K T, Schwechheimer C, Fankhauser C (2014). Reduced phototropism in pks mutants may be due to altered auxin-regulated gene expression or reduced lateral auxin transport. Plant J, 77(3): 393–403

[86] Kami C, Hersch M, Trevisan M, Genoud T, Hiltbrunner A, Bergmann S, Fankhauser C (2012). Nuclear phytochrome A signaling promotes phototropism in Arabidopsis. Plant Cell, 24(2): 566–576

[87] Kami C, Lorrain S, Hornitschek P, Fankhauser C (2010). Light-regulated plant growth and development. Curr Top Dev Biol, 91: 29–66

[88] Kansup J, Tsugama D, Liu S, Takano T (2014). Arabidopsis G-protein β subunit AGB1 interacts with NPH3 and is involved in phototropism. Biochem Biophys Res Commun, 445(1): 54–57

[89] Khurana J P, Poff K L (1989). Mutants of Arabidopsis thaliana with altered phototropism. Planta, 178(3), 400–406.

[90] Kim J, Harter K, Theologis A (1997). Protein-protein interactions among the Aux/IAA proteins. Proc Natl Acad Sci USA, 94(22): 11786–11791

[91] Kinoshita T, Doi M, Suetsugu N, Kagawa T, Wada M, Shimazaki K (2001). Phot1 and phot2 mediate blue light regulation of stomatal opening. Nature, 414(6864): 656–660

[92] Knauer T, Dümmer M, Landgraf F, Forreiter C (2011). A negative effector of blue light-induced and gravitropic bending in Arabidopsis. Plant Physiol, 156(1): 439–447

[93] Kong S G, Kagawa T, Wada M, Nagatani A (2013a). A C-terminal membrane association domain of phototropin 2 is necessary for chloroplast movement. Plant Cell Physiol, 54(1): 57–68

[94] Kong S G, Kinoshita T, Shimazaki K, Mochizuki N, Suzuki T, Nagatani A (2007). The C-terminal kinase fragment of Arabidopsis phototropin 2 triggers constitutive phototropin responses. Plant J, 51(5): 862–873

[95] Kong S G, Suetsugu N, Kikuchi S, Nakai M, Nagatani A, Wada M (2013b). Both phototropin 1 and 2 localize on the chloroplast outer membrane with distinct localization activity. Plant Cell Physiol, 54(1): 80–92

[96] Kong S G, Suzuki T, Tamura K, Mochizuki N, Hara-Nishimura I, Nagatani A (2006). Blue light-induced association of phototropin 2 with the Golgi apparatus. Plant J, 45(6): 994–1005

[97] Korasick D A, Westfall C S, Lee S G, Nanao M H, Dumas R, Hagen G, Strader L C (2014). Molecular basis for AUXIN RESPONSE FACTOR protein interaction and the control of auxin response repression. Proc Nat Acad Sci , 111(14), 5427–5432.

[98] Kozuka T, Suetsugu N, Wada M, Nagatani A (2013). Antagonistic regulation of leaf flattening by phytochrome B and phototropin in Arabidopsis thaliana. Plant Cell Physiol, 54(1): 69–79

[99] Lalanne E, Michaelidis C, Moore J M, Gagliano W, Johnson A, Patel R, Howden R, Vielle-Calzada J P, Grossniklaus U, Twell D (2004). Analysis of transposon insertion mutants highlights the diversity of mechanisms underlying male progamic development in Arabidopsis. Genetics, 167(4): 1975–1986

[100] Lariguet P, Boccalandro H E, Alonso J M, Ecker J R, Chory J, Casal J J, Fankhauser C (2003). A growth regulatory loop that provides homeostasis to phytochrome a signaling. Plant Cell, 15(12): 2966–2978

[101] Lariguet P, Dunand C (2005). Plant photoreceptors: phylogenetic overview. J Mol Evol, 61(4): 559–569

[102] Lariguet P, Fankhauser C (2004). Hypocotyl growth orientation in blue light is determined by phytochrome A inhibition of gravitropism and phototropin promotion of phototropism. Plant J, 40(5): 826–834

[103] Lariguet P, Schepens I, Hodgson D, Pedmale U V, Trevisan M, Kami C, Liscum E (2006). PHYTOCHROME KINASE SUBSTRATE 1 is a phototropin 1 binding protein required for phototropism. Proc Nat Acad Sci, 103(26), 10134–10139.

[104] Lascève G, Leymarie J, Olney M A, Liscum E, Christie J M, Vavasseur A, Briggs W R (1999). Arabidopsis contains at least four independent blue-light-activated signal transduction pathways. Plant Physiol, 120(2): 605–614

[105] Lavy M, Estelle M (2016). Mechanisms of auxin signaling. Development, 143(18): 3226–3229

[106] Lee S, Lee S, Yang K Y, Kim Y M, Park S Y, Kim S Y, Soh M S (2006). Overexpression of PRE1 and its homologous genes activates Gibberellin-dependent responses in Arabidopsis thaliana. Plant Cell Physiol, 47(5): 591–600

[107] Lewis D R, Miller N D, Splitt B L, Wu G, Spalding E P (2007). Separating the roles of acropetal and basipetal auxin transport on gravitropism with mutations in two Arabidopsis multidrug resistance-like ABC transporter genes. Plant Cell, 19(6): 1838–1850

[108] Li F W, Rothfels C J, Melkonian M, Villarreal J C, Stevenson D W, Graham S W, Wong G K, Mathews S, Pryer K M (2015). The origin and evolution of phototropins. Front Plant Sci, 6: 637

[109] Li J, Dai X, Zhao Y (2006). A role for auxin response factor 19 in auxin and ethylene signaling in Arabidopsis. Plant Physiol, 140(3): 899–908

[110] Li Y, Dai X, Cheng Y, Zhao Y (2011). NPY genes play an essential role in root gravitropic responses in Arabidopsis. Mol Plant, 4(1): 171–179

[111] Lindeboom J J, Nakamura M, Hibbel A, Shundyak K, Gutierrez R, Ketelaar T, Emons A M, Mulder B M, Kirik V, Ehrhardt D W (2013). A mechanism for reorientation of cortical microtubule arrays driven by microtubule severing. Science, 342(6163): 1245533

[112] Liscum E (2016). Blue light-induced intracellular movement of phototropins: Functional relevance or red herring? Front Plant Sci, 7: 827

[113] Liscum E, Askinosie S K, Leuchtman D L, Morrow J, Willenburg K T, Coats D R (2014). Phototropism: growing towards an understanding of plant movement. Plant Cell, 26(1): 38–55

[114] Liscum E, Briggs W R (1995). Mutations in the NPH1 locus of Arabidopsis disrupt the perception of phototropic stimuli. Plant Cell, 7(4): 473–485

[115] Liscum E, Briggs W R (1996). Mutations of Arabidopsis in potential transduction and response components of the phototropic signaling pathway. Plant Physiol, 112(1): 291–296

[116] Liscum E, Reed J W (2002). Genetics of Aux/IAA and ARF action in plant growth and development. Plant Mol Biol, 49(3-4): 387–400

[117] Liu B, Yang Z, Gomez A, Liu B, Lin C, Oka Y (2016). Signaling mechanisms of plant cryptochromes in Arabidopsis thaliana. J Plant Res, 129(2): 137–148

[118] Mara C D, Huang T, Irish V F (2010). The Arabidopsis floral homeotic proteins APETALA3 and PISTILLATA negatively regulate the BANQUO genes implicated in light signaling. Plant Cell, 22(3): 690–702

[119] McSteen P (2010). Auxin and monocot development. Cold Spring Harb Perspect Biol, 2(3): a001479

[120] Michalski C, Dümmer M, Galland P, Forreiter C (2017). Impact of EHB1 and AGD12 on root and hypocotyl phototropism in Arabidopsis thaliana. J Plant Growth Regul, 36(3): 660–668

[121] Motchoulski A, Liscum E (1999). Arabidopsis NPH3: A NPH1 photoreceptor-interacting protein essential for phototropism. Science, 286(5441): 961–964

[122] Nagashima A, Suzuki G, Uehara Y, Saji K, Furukawa T, Koshiba T, Sekimoto M, Fujioka S, Kuroha T, Kojima M, Sakakibara H, Fujisawa N, Okada K, Sakai T (2008). Phytochromes and cryptochromes regulate the differential growth of Arabidopsis hypocotyls in both a PGP19-dependent and a PGP19-independent manner. Plant J, 53(3): 516–529

[123] Nakasako M, Zikihara K, Matsuoka D, Katsura H, Tokutomi S (2008). Structural basis of the LOV1 dimerization of Arabidopsis phototropins 1 and 2. J Mol Biol, 381(3): 718–733

[124] Nakazawa M, Yabe N, Ichikawa T, Yamamoto Y Y, Yoshizumi T, Hasunuma K, Matsui M (2001). DFL1, an auxin-responsive GH3 gene homologue, negatively regulates shoot cell elongation and lateral root formation, and positively regulates the light response of hypocotyl length. Plant J, 25(2): 213–221

[125] Noh B, Bandyopadhyay A, Peer W A, Spalding E P, Murphy A S (2003). Enhanced gravi- and phototropism in plant mdr mutants mislocalizing the auxin efflux protein PIN1. Nature, 423(6943): 999–1002

[126] Nozue K, Kanegae T, Imaizumi T, Fukuda S, Okamoto H, Yeh K C, Lagarias J C, Wada M (1998). A phytochrome from the fern Adiantum with features of the putative photoreceptor NPH1. Proc Natl Acad Sci USA, 95(26): 15826–15830

[127] Ohgishi M, Saji K, Okada K, Sakai T (2004). Functional analysis of each blue light receptor, cry1, cry2, phot1, and phot2, by using combinatorial multiple mutants in Arabidopsis. Proc Natl Acad Sci USA, 101(8): 2223–2228

[128] Okadaa K, Shimuraab Y (1992). Mutational analysis of root gravitropism and phototropism of Arabidopsis thaliana seedlings. Aust J Plant Physiol, 19(4): 439–448

[129] Okushima Y, Overvoorde P J, Arima K, Alonso J M, Chan A, Chang C, Ecker J R, Hughes B, Lui A, Nguyen D, Onodera C, Quach H, Smith A, Yu G, Theologis A (2005). Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19. Plant Cell, 17(2): 444–463

[130] Park J E, Seo P J, Lee A K, Jung J H, Kim Y S, Park C M (2007). An Arabidopsis GH3 gene, encoding an auxin-conjugating enzyme, mediates phytochrome B-regulated light signals in hypocotyl growth. Plant Cell Physiol, 48(8): 1236–1241

[131] Park J Y, Kim H J, Kim J (2002). Mutation in domain II of IAA1 confers diverse auxin-related phenotypes and represses auxin-activated expression of Aux/IAA genes in steroid regulator-inducible system. Plant J, 32(5): 669–683

[132] Parks B M, Quail P H, Hangarter R P (1996). Phytochrome A regulates red-light induction of phototropic enhancement in Arabidopsis. Plant Physiol, 110(1): 155–162

[133] Parry G, Delbarre A, Marchant A, Swarup R, Napier R, Perrot-Rechenmann C, Bennett M J (2001). Novel auxin transport inhibitors phenocopy the auxin influx carrier mutation aux1. Plant J, 25(4): 399–406

[134] Pedmale U V, Celaya R B, Liscum E (2002). Phototropism: Mechanisms and outcomes. The Arabidopsis Book, 8(8),

[135] Pedmale U V, Liscum E (2007). Regulation of phototropic signaling in Arabidopsis via phosphorylation state changes in the phototropin 1-interacting protein NPH3. J Biol Chem, 282(27): 19992–20001

[136] Peer W A, Blakeslee J J, Yang H, Murphy A S (2011). Seven things we think we know about auxin transport. Mol Plant, 4(3): 487–504

[137] Petricka J J, Clay N K, Nelson T M (2008). Vein patterning screens and the defectively organized tributaries mutants in Arabidopsis thaliana. Plant J, 56(2): 251–263

[138] Pires N, Dolan L (2010). Origin and diversification of basic-helix-loop-helix proteins in plants. Mol Biol Evol, 27(4): 862–874

[139] Preuten T, Blackwood L, Christie J M, Fankhauser C (2015). Lipid anchoring of Arabidopsis phototropin 1 to assess the functional significance of receptor internalization: should I stay or should I go? New Phytol, 206(3): 1038–1050

[140] Rademacher E H, Offringa R (2012). Evolutionary adaptations of plant AGC kinases: From light signaling to cell polarity regulation. Front Plant Sci, 3: 250

[141] Rayle D L, Cleland R (1970). Enhancement of wall loosening and elongation by Acid solutions. Plant Physiol, 46(2): 250–253

[142] Rayle D L, Cleland R E (1992). The Acid Growth Theory of auxin-induced cell elongation is alive and well. Plant Physiol, 99(4): 1271–1274

[143] Ren H, Gray W M (2015). SAUR proteins as effectors of hormonal and environmental signals in plant growth. Mol Plant, 8(8): 1153–1164

[144] Roberts D, Pedmale U V, Morrow J, Sachdev S, Lechner E, Tang X, Zheng N, Hannink M, Genschik P, Liscum E (2011). Modulation of phototropic responsiveness in Arabidopsis through ubiquitination of phototropin 1 by the CUL3-Ring E3 ubiquitin ligase CRL3(^NPH3). Plant Cell, 23(10): 3627–3640

[145] Rockwell N C, Su Y S, Lagarias J C (2006). Phytochrome structure and signaling mechanisms. Annu Rev Plant Biol, 57(26): 837–858

[146] Rodriguez L, Gonzalez-Guzman M, Diaz M, Rodrigues A, Izquierdo-Garcia A C, Peirats-Llobet M, Fernandez M A, Antoni R, Fernandez D, Marquez J A, Mulet J M, Albert A, Rodriguez P L (2014). C2-domain abscisic acid-related proteins mediate the interaction of PYR/PYL/RCAR abscisic acid receptors with the plasma membrane and regulate abscisic acid sensitivity in Arabidopsis. Plant Cell, 26(12): 4802–4820

[147] Rojas-Pirela M, Rigden D J, Michels P A, Cáceres A J, Concepción J L, Quiñones W (2018). Structure and function of Per-ARNT-Sim domains and their possible role in the life-cycle biology of Trypanosoma cruzi. Mol Biochem Parasitol, 219: 52–66

[148] Rösler J, Klein I, Zeidler M (2007). Arabidopsis fhl/fhy1 double mutant reveals a distinct cytoplasmic action of phytochrome A. Proc Natl Acad Sci USA, 104(25): 10737–10742

[149] Ruegger M, Dewey E, Hobbie L, Brown D, Bernasconi P, Turner J, Muday G, Estelle M (1997). Reduced naphthylphthalamic acid binding in the tir3 mutant of Arabidopsis is associated with a reduction in polar auxin transport and diverse morphological defects. Plant Cell, 9(5): 745–757

[150] Sakai T, Kagawa T, Kasahara M, Swartz T E, Christie J M, Briggs W R,Okada K (2001). Arabidopsis nph1 and npl1: blue light receptors that mediate both phototropism and chloroplast relocation. Pro Nat Acad Sci, 98(12), 6969–6974

[151] Sakai T, Wada T, Ishiguro S, Okada K (2000). RPT2. A signal transducer of the phototropic response in Arabidopsis. Plant Cell, 12(2): 225–236

[152] Sakamoto K, Briggs W R (2002). Cellular and subcellular localization of phototropin 1. Plant Cell, 14(8): 1723–1735

[153] Salomon M, Christie J M, Knieb E, Lempert U, Briggs W R (2000). Photochemical and mutational analysis of the FMN-binding domains of the plant blue light receptor, phototropin. Biochemistry, 39(31): 9401–9410

[154] Salomon M, Lempert U, Rüdiger W (2004). Dimerization of the plant photoreceptor phototropin is probably mediated by the LOV1 domain. FEBS Lett, 572(1-3): 8–10

[155] Sampedro J, Cosgrove D J (2005). The expansin superfamily. Genome Biol, 6(12): 242

[156] Sancar A (2004). Photolyase and cryptochrome blue-light photoreceptors. Adv Protein Chem, 69: 73–100

[157] Sanders D, Pelloux J, Brownlee C, Harper J F (2002). Calcium at the crossroads of signaling. Plant Cell, 14(Suppl): S401–S417

[158] Santner A A, Watson J C (2006). The WAG1 and WAG2 protein kinases negatively regulate root waving in Arabidopsis. Plant J, 45(5): 752–764

[159] Sauer M, Kleine-Vehn J (2011). AUXIN BINDING PROTEIN1: the outsider. Plant Cell, 23(6): 2033–2043

[160] Sawa S, Ohgishi M, Goda H, Higuchi K, Shimada Y, Yoshida S, Koshiba T (2002). The HAT2 gene, a member of the HD-Zip gene family, isolated as an auxin inducible gene by DNA microarray screening, affects auxin response in Arabidopsis. Plant J, 32(6): 1011–1022

[161] Schepens I, Boccalandro H E, Kami C, Casal J J, Fankhauser C (2008). PHYTOCHROME KINASE SUBSTRATE4 modulates phytochrome-mediated control of hypocotyl growth orientation. Plant Physiol, 147(2): 661–671

[162] Scherer G F (2011). AUXIN-BINDING-PROTEIN1, the second auxin receptor: what is the significance of a two-receptor concept in plant signal transduction? J Exp Bot, 62: 3339–3357

[163] Schumacher P, Demarsy E, Waridel P, Petrolati L A, Trevisan M, Fankhauser C (2018). A phosphorylation switch turns a positive regulator of phototropism into an inhibitor of the process. Nat Commun, 9(1): 2403

[164] Staswick P E, Serban B, Rowe M, Tiryaki I, Maldonado M T, Maldonado M C, Suza W (2005). Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell, 17(2): 616–627

[165] Stogios P J, Downs G S, Jauhal J J S, Nandra S K, Privé G G (2005). Sequence and structural analysis of BTB domain proteins. Genome Biol, 6(10): R82

[166] Stone B B, Stowe-Evans E L, Harper R M, Celaya R B, Ljung K, Sandberg G, Liscum E (2008). Disruptions in AUX1-dependent auxin influx alter hypocotyl phototropism in Arabidopsis. Mol Plant, 1(1): 129–144

[167] Stowe-Evans E L, Harper R M, Motchoulski A V, Liscum E (1998). NPH4, a conditional modulator of auxin-dependent differential growth responses in Arabidopsis. Plant Physiol, 118(4): 1265–1275

[168] Stowe-Evans E L, Luesse D R, 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, 126(2): 826–834

[169] Strader L C, Zhao Y (2016). Auxin perception and downstream events. Curr Opin Plant Biol, 33: 8–14

[170] Suetsugu N, Mittmann F, Wagner G, Hughes J, Wada M (2005). A chimeric photoreceptor gene, NEOCHROME, has arisen twice during plant evolution. Proc Natl Acad Sci USA, 102(38): 13705–13709

[171] Suetsugu N, Takemiya A, Kong S G, Higa T, Komatsu A, Shimazaki K, Kohchi T, Wada M (2016). RPT2/NCH1 subfamily of NPH3-like proteins is essential for the chloroplast accumulation response in land plants. Proc Natl Acad Sci USA, 113(37): 10424–10429

[172] Sullivan S, Hart J E, Rasch P, Walker C H, Christie J M (2016). Phytochrome A mediates blue-light enhancement of second-positive phototropism in Arabidopsis. Front Plant Sci, 7: 290

[173] Sullivan S, Kaiserli E, Tseng T S, Christie J M (2010). Subcellular localization and turnover of Arabidopsis phototropin 1. Plant Signal Behav, 5(2): 184–186

[174] Sullivan S, Thomson C E, Lamont D J, Jones M A, Christie J M (2008). In vivo phosphorylation site mapping and functional characterization of Arabidopsis phototropin 1. Mol Plant, 1(1): 178–194

[175] Sun J, Qi L, Li Y, Zhai Q, Li C (2013). PIF4 and PIF5 transcription factors link blue light and auxin to regulate the phototropic response in Arabidopsis. Plant Cell, 25, 2102–2114.

[176] Takemiya A, Inoue S, Doi M, Kinoshita T, Shimazaki K (2005). Phototropins promote plant growth in response to blue light in low light environments. Plant Cell, 17(4): 1120–1127

[177] Tatematsu K, Kumagai S, Muto H, Sato A, Watahiki M K, Harper R M, Liscum E, Yamamoto K T (2004). MASSUGU2 encodes Aux/IAA19, an auxin-regulated protein that functions together with the transcriptional activator NPH4/ARF7 to regulate differential growth responses of hypocotyl and formation of lateral roots in Arabidopsis thaliana. Plant Cell, 16(2): 379–393

[178] Thomann A, Lechner E, Hansen M, Dumbliauskas E, Parmentier Y, Kieber J, Scheres B, Genschik P (2009). Arabidopsis CULLIN3 genes regulate primary root growth and patterning by ethylene-dependent and-independent mechanisms. PLoS Genet, 5(1): e1000328

[179] Titapiwatanakun B, Blakeslee J J, Bandyopadhyay A, Yang H, Mravec J, Sauer M, Cheng Y, Adamec J, Nagashima A, Geisler M, Sakai T, Friml J, Peer W A, Murphy A S (2009). ABCB19/PGP19 stabilises PIN1 in membrane microdomains in Arabidopsis. Plant J, 57(1): 27–44

[180] Tokutomi S, Matsuoka D, Zikihara K (2008). Molecular structure and regulation of phototropin kinase by blue light. Biochim Biophys Acta, 1784(1): 133–142

[181] Treml B S, Winderl S, Radykewicz R, Herz M, Schweizer G, Hutzler P, Glawischnig E, Ruiz R A (2005). The gene ENHANCER OF PINOID controls cotyledon development in the Arabidopsis embryo. Development, 132(18): 4063–4074

[182] Tseng T S, Briggs W R (2010). The Arabidopsis rcn1-1 mutation impairs dephosphorylation of Phot2, resulting in enhanced blue light responses. Plant Cell, 22(2): 392–402

[183] Tsuchida-Mayama T, Nakano M, Uehara Y, Sano M, Fujisawa N, Okada K, Sakai T (2008). Mapping of the phosphorylation sites on the phototropic signal transducer, NPH3. Plant Sci, 174(6): 626–633

[184] Tsuchida-Mayama T, Sakai T, Hanada A, Uehara Y, Asami T, Yamaguchi S (2010). Role of the phytochrome and cryptochrome signaling pathways in hypocotyl phototropism. Plant J, 62(4): 653–662

[185] Ulmasov T, Hagen G, Guilfoyle T J (1997). ARF1, a transcription factor that binds to auxin response elements. Science, 276(5320), 1865–1868.

[186] Urano D, Chen J G, Botella J R, Jones A M (2013). Heterotrimeric G protein signalling in the plant kingdom. Open Biol, 3(3): 120186–120186

[187] Wan Y, Jasik J, Wang L, Hao H, Volkmann D, Menzel D, Mancuso S, Baluška F, Lin J (2012). The signal transducer NPH3 integrates the phototropin1 photosensor with PIN2-based polar auxin transport in Arabidopsis root phototropism. Plant Cell, 24(2): 551–565

[188] Wan Y L, Eisinger W, Ehrhardt D, Kubitscheck U, Baluska F, Briggs W (2008). The subcellular localization and blue-light-induced movement of phototropin 1-GFP in etiolated seedlings of Arabidopsis thaliana. Mol Plant, 1(1): 103–117

[189] Watahiki M K, Yamamoto K T (1997). The massugu1 mutation of Arabidopsis identified with failure of auxin-induced growth curvature of hypocotyl confers auxin insensitivity to hypocotyl and leaf. Plant Physiol, 115(2): 419–426

[190] Went, F. W., and Thimann, K. V. (1937). Phytohormones.

[191] Westfall C S, Herrmann J, Chen Q, Wang S, Jez J M (2010). Modulating plant hormones by enzyme action: the GH3 family of acyl acid amido synthetases. Plant Signal Behav, 5(12): 1607–1612

[192] Whippo C W, Hangarter R P (2003). Second positive phototropism results from coordinated co-action of the phototropins and cryptochromes. Plant Physiol, 132(3): 1499–1507

[193] Whippo C W, Hangarter R P (2004). Phytochrome modulation of blue-light-induced phototropism. Plant Cell Environ, 27(10): 1223–1228

[194] Willige B C, Ahlers S, Zourelidou M, Barbosa I C R, Demarsy E, Trevisan M, Davis P A, Roelfsema M R, Hangarter R, Fankhauser C, Schwechheimer C (2013). D6PK AGCVIII kinases are required for auxin transport and phototropic hypocotyl bending in Arabidopsis. Plant Cell, 25(5): 1674–1688

[195] Woo O G, Kim S H, Cho S K, Kim S H, Lee H N, Chung T, Yang S W, Lee J H (2018). BPH1, a novel substrate receptor of CRL3, plays a repressive role in ABA signal transduction. Plant Mol Biol, 96(6): 593–606

[196] Xue Y, Xing J, Wan Y, Lv X, Fan L, Zhang Y, Song K, Wang L, Wang X, Deng X, Baluška F, Christie J M, Lin J (2018). Arabidopsis blue light receptor phototropin 1 undergoes blue light-induced activation in membrane microdomains. Mol Plant, 11(6): 846–859

[197] Zazímalová E, Murphy A S, Yang H, Hoyerová K, Hosek P (2010). Auxin transporters--why so many? Cold Spring Harb Perspect Biol, 2(3): a001552

[198] Zhang L, Du L, Shen C, Yang Y, Poovaiah B W (2014). Regulation of plant immunity through ubiquitin-mediated modulation of Ca(2+) -calmodulin-AtSR1/CAMTA3 signaling. Plant J, 78(2): 269–281

[199] Zhang X S, O’Neill S D (1993). Ovary and gametophyte development are coordinately regulated by auxin and ethylene following pollination. Plant Cell, 5(4): 403–418

[200] Zhao X, Wang Y L, Qiao X R, Wang J, Wang L D, Xu C S, Zhang X (2013). Phototropins function in high-intensity blue light-induced hypocotyl phototropism in Arabidopsis by altering cytosolic calcium. Plant Physiol, 162(3): 1539–1551

[201] Zhao Y (2010). Auxin biosynthesis and its role in plant development. Annu Rev Plant Biol, 61(1): 49–64

[202] Zourelidou M, Müller I, Willige B C, Nill C, Jikumaru Y, Li H, Schwechheimer C (2009). The polarly localized D6 PROTEIN KINASE is required for efficient auxin transport in Arabidopsis thaliana. Development, 136(4): 627–636

Acknowledgement

Research in the Liscum laboratory is supported by the National Science Foundation (IOS-1146142).

RIGHTS & PERMISSIONS

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