Please wait a minute...
Frontiers in Biology

ISSN 1674-7984

ISSN 1674-7992(Online)

CN 11-5892/Q

Frontiers in Biology  2018, Vol. 13 Issue (5): 342-357   https://doi.org/10.1007/s11515-018-1518-y
  本期目录
Phototropism in land plants: Molecules and mechanism from light perception to response
Johanna Morrow1,2, Kyle T. Willenburg1,2, Emmanuel Liscum1,2()
1. C.S. Bond Life Sciences Center, University of Missouri, Columbia, MO, USA
2. Division of Biological Sciences, University of Missouri, Columbia, MO, USA
 全文: PDF(291 KB)   HTML
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.

Key wordsphototropism    phototropin    phytochrome    crytochrome    auxin    auxin response factor    phosphorylation    ubiquitination    transcriptional control    cell elongation    growth    non-phototropic hypocotyl 3    NPH3/RPT2-like    protein kinase    calcium
收稿日期: 2018-06-22      出版日期: 2018-10-25
Corresponding Author(s): Emmanuel Liscum   
 引用本文:   
. [J]. Frontiers in Biology, 2018, 13(5): 342-357.
Johanna Morrow, Kyle T. Willenburg, Emmanuel Liscum. Phototropism in land plants: Molecules and mechanism from light perception to response. Front. Biol., 2018, 13(5): 342-357.
 链接本文:  
https://academic.hep.com.cn/fib/CN/10.1007/s11515-018-1518-y
https://academic.hep.com.cn/fib/CN/Y2018/V13/I5/342
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
https://doi.org/10.1093/jxb/eru172 pmid: 24821953
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
https://doi.org/10.1038/366162a0 pmid: 8232555
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
pmid: 9490743
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
https://doi.org/10.1093/aob/mch126 pmid: 15155378
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
https://doi.org/10.1073/pnas.96.23.13554 pmid: 10557359
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
https://doi.org/10.1104/pp.103.019943 pmid: 12857841
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
https://doi.org/10.1046/j.1365-313X.1995.8040505.x
10 Bennett T (2015). PIN proteins and the evolution of plant development. Trends Plant Sci, 20(8): 498–507
https://doi.org/10.1016/j.tplants.2015.05.005 pmid: 26051227
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
https://doi.org/10.1104/pp.103.031690 pmid: 14730061
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
https://doi.org/10.1016/j.cell.2013.12.027 pmid: 24485461
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
https://doi.org/10.1016/S1360-1385(03)00188-2 pmid: 13678909
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
https://doi.org/10.1104/pp.103.021170 pmid: 12805588
15 Briggs W R, Huala E (1999). Blue-light photoreceptors in higher plants. Annu Rev Cell Dev Biol, 15(1): 33–62
https://doi.org/10.1146/annurev.cellbio.15.1.33 pmid: 10611956
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
https://doi.org/10.1104/pp.110.153593 pmid: 20472752
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
https://doi.org/10.1146/annurev-arplant-042110-103759 pmid: 21526969
18 Chen L, Hellmann H (2013). Plant E3 ligases: flexible enzymes in a sessile world. Mol Plant, 6(5): 1388–1404
https://doi.org/10.1093/mp/sst005 pmid: 23307436
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
https://doi.org/10.1073/pnas.0708506104 pmid: 18000043
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
https://doi.org/10.1073/pnas.0809761106 pmid: 19075219
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
https://doi.org/10.1105/tpc.107.054288 pmid: 18156217
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
https://doi.org/10.1016/S0092-8674(00)80682-0 pmid: 10693763
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
https://doi.org/10.1126/science.282.5394.1698 pmid: 9831559
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
https://doi.org/10.1073/pnas.96.15.8779 pmid: 10411952
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
https://doi.org/10.1104/pp.17.00835 pmid: 28720608
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
https://doi.org/10.1371/journal.pbio.1001076 pmid: 21666806
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
https://doi.org/10.1007/BF00043870 pmid: 8049367
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
https://doi.org/10.1021/bi026978l pmid: 12515534
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
https://doi.org/10.1104/pp.109.150441 pmid: 20071603
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
https://doi.org/10.1104/pp.103.029116 pmid: 14605230
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
https://doi.org/10.1038/emboj.2012.186 pmid: 22781128
33 Deshaies R J, Joazeiro C A (2009). RING domain E3 ubiquitin ligases. Annu Rev Biochem, 78(1): 399–434
https://doi.org/10.1146/annurev.biochem.78.101807.093809 pmid: 19489725
34 Dezfulian M H, Jalili E, Roberto D K A, Moss B L, Khoo K, Nemhauser J L, Crosby W L (2016). Oligomerization of SCFTIR1 is essential for Aux/IAA degradation and auxin signaling in Arabidopsis. PLoS Genet, 12(9): e1006301
https://doi.org/10.1371/journal.pgen.1006301 pmid: 27618443
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
https://doi.org/10.1038/ncb2208 pmid: 21394084
36 Doherty G J, McMahon H T (2009). Mechanisms of endocytosis. Annu Rev Biochem, 78(1): 857–902
https://doi.org/10.1146/annurev.biochem.78.081307.110540 pmid: 19317650
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
https://doi.org/10.1016/j.jplph.2016.09.006 pmid: 27728837
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
https://doi.org/10.1073/pnas.0507127103 pmid: 16371470
39 Fankhauser C (2001). The phytochromes, a family of red/far-red absorbing photoreceptors. J Biol Chem, 276(15): 11453–11456
https://doi.org/10.1074/jbc.R100006200 pmid: 11279228
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
https://doi.org/10.1126/science.284.5419.1539 pmid: 10348744
41 Felle H (1988). Auxin causes oscillations of cytosolic free calcium and pH in Zea mays coleoptiles. Planta, 174(4): 495–499
https://doi.org/10.1007/BF00634478 pmid: 24221565
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
https://doi.org/10.1105/tpc.105.031989 pmid: 15772280
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
https://doi.org/10.1104/pp.103.024372 pmid: 14645723
44 Franklin K A, Quail P H (2010). Phytochrome functions in Arabidopsis development. J Exp Bot, 61(1): 11–24
https://doi.org/10.1093/jxb/erp304 pmid: 19815685
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
https://doi.org/10.1038/415806a pmid: 11845211
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
https://doi.org/10.1126/science.1100618 pmid: 15514156
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
https://doi.org/10.1242/dev.009654 pmid: 17913786
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
https://doi.org/10.1038/345528a0 pmid: 11540625
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
https://doi.org/10.1016/S0092-8674(03)00003-5 pmid: 12553910
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
https://doi.org/10.1242/dev.00926 pmid: 14681187
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
https://doi.org/10.1038/emboj.2013.173 pmid: 23912815
52 Grones P, Friml J (2015). Auxin transporters and binding proteins at a glance. J Cell Sci, 128(1): 1–7
https://doi.org/10.1242/jcs.159418 pmid: 25556248
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
https://doi.org/10.1038/emboj.2010.181 pmid: 20717140
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
https://doi.org/10.1105/tpc.114.132753 pmid: 25604444
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
https://doi.org/10.1016/S0070-2153(10)91004-1 pmid: 20705180
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
https://doi.org/10.1093/pcp/pcy048 pmid: 29490064
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
https://doi.org/10.1105/tpc.104.028357 pmid: 15598797
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
https://doi.org/10.1105/tpc.15.00178 pmid: 25873385
59 Haglund K, Dikic I (2005). Ubiquitylation and cell signaling. EMBO J, 24(19): 3353–3359
https://doi.org/10.1038/sj.emboj.7600808 pmid: 16148945
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
https://doi.org/10.1093/pcp/pcs098 pmid: 22782888
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
https://doi.org/10.1105/tpc.108.059915 pmid: 18952772
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
https://doi.org/10.1073/pnas.1419525112 pmid: 25512488
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
https://doi.org/10.1073/pnas.1336802100 pmid: 12821778
64 Harada A, Shimazaki K (2007). Phototropins and blue light-dependent calcium signaling in higher plants. Photochem Photobiol, 83(1): 102–111
https://doi.org/10.1562/2006-03-08-IR-837 pmid: 16906793
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
https://doi.org/10.1093/pcp/pcs094 pmid: 22739508
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
https://doi.org/10.1105/tpc.12.5.757 pmid: 10810148
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
https://doi.org/10.1021/bi048092i pmid: 15610012
68 Holland J J, Roberts D, Liscum E (2009). Understanding phototropism: from Darwin to today. J Exp Bot, 60(7): 1969–1978
https://doi.org/10.1093/jxb/erp113 pmid: 19357428
69 Hotton S K, Callis J (2008). Regulation of cullin RING ligases. Annu Rev Plant Biol, 59(1): 467–489
https://doi.org/10.1146/annurev.arplant.58.032806.104011 pmid: 18444905
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
https://doi.org/10.1126/science.278.5346.2120 pmid: 9405347
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
https://doi.org/10.1105/tpc.109.072678 pmid: 20407025
72 Hughes J (2013). Phytochrome cytoplasmic signaling. Annu Rev Plant Biol, 64(1): 377–402
https://doi.org/10.1146/annurev-arplant-050312-120045 pmid: 23506333
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
https://doi.org/10.1105/tpc.019901 pmid: 15031408
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
https://doi.org/10.1073/pnas.0709189105 pmid: 18378899
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
https://doi.org/10.1093/mp/ssm001 pmid: 20031912
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
https://doi.org/10.1104/pp.111.175943 pmid: 21427282
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
https://doi.org/10.1073/pnas.1120203109 pmid: 22773817
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
https://doi.org/10.1104/pp.113.3.975 pmid: 9085579
79 Janoudi A K, Poff K L (1993). Desensitization and recovery of phototropic responsiveness in Arabidopsis thaliana. Plant Physiol, 101(101): 1175–1180
https://doi.org/10.1104/pp.101.4.1175 pmid: 11537496
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
https://doi.org/10.1104/pp.99.4.1422 pmid: 11537887
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
https://doi.org/10.1038/35073622 pmid: 11309623
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
https://doi.org/10.1074/jbc.M605969200 pmid: 17164248
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
https://doi.org/10.1126/science.291.5511.2138 pmid: 11251116
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
https://doi.org/10.1105/tpc.109.067876 pmid: 19880798
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
https://doi.org/10.1111/tpj.12395 pmid: 24286493
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
https://doi.org/10.1105/tpc.111.095083 pmid: 22374392
87 Kami C, Lorrain S, Hornitschek P, Fankhauser C (2010). Light-regulated plant growth and development. Curr Top Dev Biol, 91: 29–66
https://doi.org/10.1016/S0070-2153(10)91002-8 pmid: 20705178
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
https://doi.org/10.1016/j.bbrc.2014.01.106 pmid: 24486545
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
https://doi.org/10.1073/pnas.94.22.11786 pmid: 9342315
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.
https://doi.org/10.1038/414656a pmid: 11740564
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
https://doi.org/10.1104/pp.110.167411 pmid: 21367967
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
https://doi.org/10.1093/pcp/pcs132 pmid: 23012349
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
https://doi.org/10.1111/j.1365-313X.2007.03187.x pmid: 17662032
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
https://doi.org/10.1093/pcp/pcs151 pmid: 23161859
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
https://doi.org/10.1111/j.1365-313X.2006.02667.x pmid: 16507089
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
https://doi.org/10.1093/pcp/pcs134 pmid: 23054390
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
https://doi.org/10.1534/genetics.104.030270 pmid: 15342534
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
https://doi.org/10.1105/tpc.014563 pmid: 14615593
101 Lariguet P, Dunand C (2005). Plant photoreceptors: phylogenetic overview. J Mol Evol, 61(4): 559–569
https://doi.org/10.1007/s00239-004-0294-2 pmid: 16170454
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
https://doi.org/10.1111/j.1365-313X.2004.02256.x pmid: 15546364
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
https://doi.org/10.1104/pp.120.2.605 pmid: 10364413
105 Lavy M, Estelle M (2016). Mechanisms of auxin signaling. Development, 143(18): 3226–3229
https://doi.org/10.1242/dev.131870 pmid: 27624827
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
https://doi.org/10.1093/pcp/pcj026 pmid: 16527868
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
https://doi.org/10.1105/tpc.107.051599 pmid: 17557805
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
https://doi.org/10.3389/fpls.2015.00637 pmid: 26322073
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
https://doi.org/10.1104/pp.105.070987 pmid: 16461383
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
https://doi.org/10.1093/mp/ssq052 pmid: 20833732
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
https://doi.org/10.1126/science.1245533 pmid: 24200811
112 Liscum E (2016). Blue light-induced intracellular movement of phototropins: Functional relevance or red herring? Front Plant Sci, 7: 827
https://doi.org/10.3389/fpls.2016.00827 pmid: 27375670
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
https://doi.org/10.1105/tpc.113.119727 pmid: 24481074
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
https://doi.org/10.1105/tpc.7.4.473 pmid: 7773019
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
https://doi.org/10.1104/pp.112.1.291 pmid: 8819327
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
https://doi.org/10.1023/A:1015255030047 pmid: 12036262
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
https://doi.org/10.1007/s10265-015-0782-z pmid: 26810763
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
https://doi.org/10.1105/tpc.109.065946 pmid: 20305124
119 McSteen P (2010). Auxin and monocot development. Cold Spring Harb Perspect Biol, 2(3): a001479
https://doi.org/10.1101/cshperspect.a001479 pmid: 20300208
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
https://doi.org/10.1007/s00344-017-9667-9
121 Motchoulski A, Liscum E (1999). Arabidopsis NPH3: A NPH1 photoreceptor-interacting protein essential for phototropism. Science, 286(5441): 961–964
https://doi.org/10.1126/science.286.5441.961 pmid: 10542152
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
https://doi.org/10.1111/j.1365-313X.2007.03358.x pmid: 18086281
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
https://doi.org/10.1016/j.jmb.2008.06.033 pmid: 18585389
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
https://doi.org/10.1046/j.1365-313x.2001.00957.x pmid: 11169197
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
https://doi.org/10.1038/nature01716 pmid: 12827205
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
https://doi.org/10.1073/pnas.95.26.15826 pmid: 9861055
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
https://doi.org/10.1073/pnas.0305984101 pmid: 14982991
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
https://doi.org/10.1071/PP9920439
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
https://doi.org/10.1105/tpc.104.028316 pmid: 15659631
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
https://doi.org/10.1093/pcp/pcm086 pmid: 17602188
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
https://doi.org/10.1046/j.1365-313X.2002.01459.x pmid: 12472684
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
https://doi.org/10.1104/pp.110.1.155 pmid: 8587979
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
https://doi.org/10.1046/j.1365-313x.2001.00970.x pmid: 11260496
134 Pedmale U V, Celaya R B, Liscum E (2002). Phototropism: Mechanisms and outcomes. The Arabidopsis Book, 8(8),
https://doi.org/10.1199/tab.0042
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
https://doi.org/10.1074/jbc.M702551200 pmid: 17493935
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
https://doi.org/10.1093/mp/ssr034 pmid: 21505044
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
https://doi.org/10.1111/j.1365-313X.2008.03595.x pmid: 18643975
138 Pires N, Dolan L (2010). Origin and diversification of basic-helix-loop-helix proteins in plants. Mol Biol Evol, 27(4): 862–874
https://doi.org/10.1093/molbev/msp288 pmid: 19942615
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
https://doi.org/10.1111/nph.13299 pmid: 25643813
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
https://doi.org/10.3389/fpls.2012.00250 pmid: 23162562
141 Rayle D L, Cleland R (1970). Enhancement of wall loosening and elongation by Acid solutions. Plant Physiol, 46(2): 250–253
https://doi.org/10.1104/pp.46.2.250 pmid: 16657445
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
https://doi.org/10.1104/pp.99.4.1271 pmid: 11537886
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
https://doi.org/10.1016/j.molp.2015.05.003 pmid: 25983207
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
https://doi.org/10.1105/tpc.111.087999 pmid: 21990941
145 Rockwell N C, Su Y S, Lagarias J C (2006). Phytochrome structure and signaling mechanisms. Annu Rev Plant Biol, 57(26): 837–858
https://doi.org/10.1146/annurev.arplant.56.032604.144208 pmid: 16669784
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
https://doi.org/10.1105/tpc.114.129973 pmid: 25465408
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
https://doi.org/10.1016/j.molbiopara.2017.11.002 pmid: 29133150
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
https://doi.org/10.1073/pnas.0703855104 pmid: 17566111
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
https://doi.org/10.1105/tpc.9.5.745 pmid: 9165751
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
https://doi.org/10.1105/tpc.12.2.225 pmid: 10662859
152 Sakamoto K, Briggs W R (2002). Cellular and subcellular localization of phototropin 1. Plant Cell, 14(8): 1723–1735
https://doi.org/10.1105/tpc.003293 pmid: 12172018
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
https://doi.org/10.1021/bi000585+ pmid: 10924135
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
https://doi.org/10.1016/j.febslet.2004.06.081 pmid: 15304315
155 Sampedro J, Cosgrove D J (2005). The expansin superfamily. Genome Biol, 6(12): 242
https://doi.org/10.1186/gb-2005-6-12-242 pmid: 16356276
156 Sancar A (2004). Photolyase and cryptochrome blue-light photoreceptors. Adv Protein Chem, 69: 73–100
https://doi.org/10.1016/S0065-3233(04)69003-6 pmid: 15588840
157 Sanders D, Pelloux J, Brownlee C, Harper J F (2002). Calcium at the crossroads of signaling. Plant Cell, 14(Suppl): S401–S417
https://doi.org/10.1105/tpc.002899 pmid: 12045291
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
https://doi.org/10.1111/j.1365-313X.2005.02641.x pmid: 16460509
159 Sauer M, Kleine-Vehn J (2011). AUXIN BINDING PROTEIN1: the outsider. Plant Cell, 23(6): 2033–2043
https://doi.org/10.1105/tpc.111.087064 pmid: 21719690
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
https://doi.org/10.1046/j.1365-313X.2002.01488.x pmid: 12492842
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
https://doi.org/10.1104/pp.108.118166 pmid: 18390804
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
https://doi.org/10.1038/s41467-018-04752-1 pmid: 29921904
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
https://doi.org/10.1105/tpc.104.026690 pmid: 15659623
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
https://doi.org/10.1186/gb-2005-6-10-r82 pmid: 16207353
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
https://doi.org/10.1093/mp/ssm013 pmid: 20031920
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
https://doi.org/10.1104/pp.118.4.1265 pmid: 9847100
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
https://doi.org/10.1104/pp.126.2.826 pmid: 11402210
169 Strader L C, Zhao Y (2016). Auxin perception and downstream events. Curr Opin Plant Biol, 33: 8–14
https://doi.org/10.1016/j.pbi.2016.04.004 pmid: 27131035
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
https://doi.org/10.1073/pnas.0504734102 pmid: 16174755
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
https://doi.org/10.1073/pnas.1602151113 pmid: 27578868
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
https://doi.org/10.3389/fpls.2016.00290 pmid: 27014313
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
https://doi.org/10.4161/psb.5.2.11082 pmid: 20173419
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
https://doi.org/10.1093/mp/ssm017 pmid: 20031924
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
https://doi.org/10.1105/tpc.104.030049 pmid: 15749755
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
https://doi.org/10.1105/tpc.018630 pmid: 14729917
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
https://doi.org/10.1371/journal.pgen.1000328 pmid: 19132085
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
https://doi.org/10.1111/j.1365-313X.2008.03668.x pmid: 18774968
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
https://doi.org/10.1016/j.bbapap.2007.09.010 pmid: 17988963
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
https://doi.org/10.1242/dev.01969 pmid: 16107478
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
https://doi.org/10.1105/tpc.109.066423 pmid: 20139163
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
https://doi.org/10.1016/j.plantsci.2008.03.018
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
https://doi.org/10.1111/j.1365-313X.2010.04180.x pmid: 20202166
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
https://doi.org/10.1098/rsob.120186 pmid: 23536550
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
https://doi.org/10.1105/tpc.111.094284 pmid: 22374399
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
https://doi.org/10.1093/mp/ssm011 pmid: 20031918
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
https://doi.org/10.1104/pp.115.2.419 pmid: 9342863
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
https://doi.org/10.4161/psb.5.12.13941 pmid: 21150301
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
https://doi.org/10.1104/pp.102.018481 pmid: 12857830
193 Whippo C W, Hangarter R P (2004). Phytochrome modulation of blue-light-induced phototropism. Plant Cell Environ, 27(10): 1223–1228
https://doi.org/10.1111/j.1365-3040.2004.01227.x
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
https://doi.org/10.1105/tpc.113.111484 pmid: 23709629
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
https://doi.org/10.1007/s11103-018-0717-x pmid: 29560577
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
https://doi.org/10.1016/j.molp.2018.04.003 pmid: 29689384
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
https://doi.org/10.1101/cshperspect.a001552 pmid: 20300209
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
https://doi.org/10.1111/tpj.12473 pmid: 24528504
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
https://doi.org/10.1105/tpc.5.4.403 pmid: 12271070
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
https://doi.org/10.1104/pp.113.216556 pmid: 23674105
201 Zhao Y (2010). Auxin biosynthesis and its role in plant development. Annu Rev Plant Biol, 61(1): 49–64
https://doi.org/10.1146/annurev-arplant-042809-112308 pmid: 20192736
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
https://doi.org/10.1242/dev.028365 pmid: 19168677
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed