REVIEW

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

  • Johanna Morrow 1,2 ,
  • Kyle T. Willenburg 1,2 ,
  • Emmanuel Liscum , 1,2
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  • 1. C.S. Bond Life Sciences Center, University of Missouri, Columbia, MO, USA
  • 2. Division of Biological Sciences, University of Missouri, Columbia, MO, USA

Received date: 22 Jun 2018

Accepted date: 08 Aug 2018

Published date: 25 Oct 2018

Copyright

2018 Higher Education Press and Springer-Verlag GmbH Germany, part of Springer Nature

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.

Cite this article

Johanna Morrow , Kyle T. Willenburg , Emmanuel Liscum . Phototropism in land plants: Molecules and mechanism from light perception to response[J]. Frontiers in Biology, 2018 , 13(5) : 342 -357 . DOI: 10.1007/s11515-018-1518-y

Acknowledgement

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

DOI PMID

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

DOI PMID

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

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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