Specificity and Crosstalk of Phototropin with Cryptochrome and Phytochrome in Regulating Hypocotyl Phototropism

doi:10.3724/SP.J.1259.2015.00122

Abstract

Abstract: Blue light (BL) is a key factor controlling plant growth and morphogenesis. BL receptors phototropin1 (PHOT1) and phototropin2 (PHOT2) mediate BL-induced plant movements such as phototropism, chloroplast relocation and stomatal opening responses. Phototropism allows plants to bend toward light by perceiving the direction, wavelength and intensity of incident light so that they can obtain optimum light. Phytochrome and cryptochrome are also involved in asymmetric regulation of hypocotyl growth, causing plant phototropic growth. In this review, we discuss the signaling for phototropins and focus on the crosstalk with phytochrome and cryptochrome signaling in regulating phototropism. Fundamental progress in understanding the role of phototropins and phytochrome or cryptochrome in phototropism will continue to provide a rational basis for biotechnological improvements in developing light-trapping plants with improved light-use efficiency.

Xiang Zhao, Qingping Zhao, Xu Yang, Shichao Mu, Xiao Zhang. Specificity and Crosstalk of Phototropin with Cryptochrome and Phytochrome in Regulating Hypocotyl Phototropism[J]. Chinese Bulletin of Botany, 2015, 50(1): 122-132.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.chinbullbotany.com/EN/10.3724/SP.J.1259.2015.00122

https://www.chinbullbotany.com/EN/Y2015/V50/I1/122

References 87

1	钱善勤, 王忠, 莫亿伟, 顾蕴洁 (2004). 植物向光性反应的研究进展. 植物学通报 21, 263-272.
2	Blakeslee JJ, Bandyopadhyay A, Lee OR, Mravec J, Titapiwatanakun B, Sauer M, Makam SN, Cheng Y, Bouchard R, Adamec J, Geisler M, Nagashima A, Sakai T, Martinoia E, Friml J, Peer WA, Murphy AS (2007). Interactions among PIN-FORMED and P-glyco- protein auxin transporters in Arabidopsis. Plant Cell 19, 131-147.
3	Blakeslee JJ, Bandyopadhyay A, Peer WA, Makam SN, Murphy AS (2004). Relocalization of the PIN1 auxin efflux facilitator plays a role in phototropic responses.Plant Physiol 134, 28-31.
4	Blakeslee JJ, Peer WA, Murphy AS (2005). Auxin transport.Curr Opin Plant Biol 8, 494-500.
5	Boccalandro HE, De Simone SN, Bergmann-Honsberger A, Schepens I, Fankhauser C, Casal JJ (2008). PHYTOCHROME KINASE SUBSTRATE1 regulates root phototropism and gravitropism.Plant Physiol 146, 108-115.
6	Briggs WR (1963). The phototropic responses of higher plants.Annu Rev Plant Physiol 14, 311-352.
7	Briggs WR (2014). Phototropism: some history, some puzzles, and a look ahead.Plant Physiol 164, 13-23.
8	Briggs WR, Christie JM (2002). Phototropins 1 and 2: versatile plant blue-light receptors.Trends Plant Sci 7, 204-210.
9	Christie JM (2007). Phototropin blue-light receptors. Annu Rev Plant Biol 58, 21-45.
10	Christie JM, Salomon M, Nozue K, Wada M, Briggs WR (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, 8779-8783.
11	Christie JM, Yang HB, Richter GL, Sullivan S, Thomson CE, Lin JS, Titapiwatanakun B, Ennis M, Kaiserli E, Lee OR, Adamec J, Peer WA, Murphy AS (2011). phot1 inhibition of ABCB19 primes lateral auxin fluxes in the shoot apex required for phototropism.PLoS Biol 9, e100-1076.
12	de Carbonnel M, Davis P, Roelfsema MRG, 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, 1391-1405.
13	Demarsy E, Schepens I, Okajima K, Hersch M, Bergmann S, Christie J, Shimazaki K, Tokutomi S, Fankhauser C (2012). Phytochrome kinase substrate 4 is phosphory- lated by the phototropin 1 photoreceptor.EMBO J 31, 3457-3467.
14	Devlin PF, Yanovsky MJ, Kay SA (2003). A genomic analysis of the shade avoidance response in Arabidopsis.Plant Physiol 133, 1617-1629.
15	Ding ZJ, Galván-Ampudia CS, Demarsy E, Langowski L, Kleine-Vehn J, Fan YW, Morita MT, Tasaka M, Fank- hauser C, Offringa R, Friml J (2011). Light-mediated polarization of the PIN3 auxin transporter for the phototropic response in Arabidopsis.Nat Cell Biol 13, 447-452.
16	Fankhauser C, Yeh KC, Lagarias JC, Zhang H, Elich TD, Chory J (1999). PKS1, a substrate phosphorylated by phytochrome that modulates light signaling in Arabidop- sis.Science 284, 1539-1541.
17	Friml J, Wiśniewska J, Benková E, Mendgen K, Palme K (2002). Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415, 806-809.
18	Goyal A, Szarzynska B, Fankhauser C (2013). Phototropism: at the crossroads of light-signaling pathways.Trends Plant Sci 18, 393-341.
19	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, 103-115.
20	Han IS, Tseng TS, Eisinger W, Briggs WR (2008). Phytochrome A regulates the intracellular distribution of phototropin 1-green fluorescent protein in Arabidopsis thaliana.Plant Cell 20, 2835-2847.
21	Hangarter RP (1997). Gravity, light and plant form.Plant Cell Environ 20, 796-800.
22	Harada A, Shimazaki K (2007). Phototropins and blue light-dependent calcium signaling in higher plants.Photo- chem Photobiol 83, 102-111.
23	Harper RM, Stowe-Evans EL, Luesse DR, Muto H, Tatematsu K, Watahiki MK, 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, 757-770.
24	Hohm T, Preuten T, Fankhauser C (2013). Phototropism: translating light into directional growth.Am J Bot 100, 47-59.
25	Holland JJ, Roberts D, Liscum E (2009). Understanding phototropism: from Darwin to today.J Exp Bot 60, 1969-1978.
26	Huala E, Oeller PW, Liscum E, Han IS, Larsen E, Briggs WR (1997). Arabidopsis NPH1: a protein kinase with a putative redox-sensing domain.Science 278, 2120-2123.
27	Iino M (2006). Toward understanding the ecological functions of tropisms: interactions among and effects of light on tropisms.Curr Opin Plant Biol 9, 89-93.
28	Inada S, Ohgishi M, Mayama T, Okada K, Sakai T (2004). RPT2 is a signal transducer involved in phototropic re- sponse and stomatal opening by association with photo- tropin 1 in Arabidopsis thaliana.Plant Cell 16, 887-896.
29	Inoue S, Kinoshita T, Matsumoto M, Nakayama KI, Doi M, Shimazaki K (2008). Blue light-induced autophosphory- lation of phototropin is a primary step for signaling.Proc Natl Acad Sci USA 105, 5626-5631.
30	Jaedicke K, Lichtenthäler AL, Meybreg R, Zeidler M, Hughes J (2012). A phytochrome-phototropin light signaling complex at the plasma membrane.Proc Natl Acad Sci USA 109, 12231-12236.
31	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, 2138-2141.
32	Kaiserli E, Sullivan S, Jones MA, Feeney KA, Christie JM (2009). Domain swapping to assess the mechanistic basis of Arabidopsis phototropin 1 receptor kinase activation and endocytosis by blue light.Plant Cell 21, 3226-3244.
33	Kami C, Hersch M, Trevisan M, Genoud T, Hiltbrunner A, Bergmann S, Fankhauser C (2012). Nuclear phyto- chrome A signaling promotes phototropism in Arabidopsis.Plant Cell 24, 566-576.
34	Kang B, Grancher N, Koyffmann V, Lardemer D, Burney S, Ahmad M (2008). Multiple interactions between cryp- tochrome and phototropin blue-light signaling pathways in Arabidopsis thaliana.Planta 227, 1091-1099.
35	Kim K, Shin J, Lee SH, Kweon HS, Maloof JN, Choi G (2011). Phytochromes inhibit hypocotyl negative gravitro- pism by regulating the development of endodermal amy- loplasts through phytochrome-interacting factors.Proc Natl Acad Sci USA 108, 1729-1734.
36	Knauer T, Dümmer M, Landgraf F, Forreiter C (2011). A negative effector of blue light-induced and gravitropic bending in Arabidopsis.Plant Physiol 156, 439-447.
37	Kong SG, 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, 994-1005.
38	Lariguet P, Boccalandro HE, Alonso JM, Ecker JR, Chory J, Casal JJ, Fankhauser C (2003). A growth regu- latory loop that provides homeostasis to phytochrome A signaling.Plant Cell 15, 2966-2978.
39	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, 826-834.
40	Lariguet P, Schepens I, Hodgson D, Pedmale UV, Tre- visan M, Kami C, de Carbonnel M, Alonso JM, Ecker JR, Liscum E, Fankhauser C (2006). PHYTOCHROME KINASE SUBSTRATE 1 is a phototropin 1 binding protein required for phototropism.Proc Natl Acad Sci USA 103, 10134-10139.
41	Lascève G, Leymarie J, Olney MA, Liscum E, Christie JM, Vavasseur A, Briggs WR (1999). Arabidopsis con- tains at least four independent blue-light-activated signal transduction pathways.Plant Physiol 120, 605-614.
42	Liscum E (2002). Phototropism: mechanisms and out- comes. In: Somerville C, Meyerowitz E, eds. The Arabidopsis Book. Rockville, MD: American Society of Plant Biologists.
43	Liscum E, Askinosie SK, Leuchtman DL, Morrow J, Willenburg KT, Coats DR (2014). Phototropism: growing towards an understanding of plant movement.Plant Cell 26, 38-55.
44	Liscum E, Briggs WR (1996). Mutations of Arabidopsis in potential transduction and response components of the phototropic signaling pathway.Plant Physiol 112, 291-296.
45	Liu HT, Liu B, Zhao CX, Pepper M, Lin CT (2011). The action mechanisms of plant cryptochromes.Trends Plant Sci 16, 684-691.
46	Marcotte EM, Pellegrini M, Ng HL, Rice DW, Yeates TO, Eisenberg D (1999). Detecting protein function and protein-protein interactions from genome sequences.Sci- ence 285, 751-753.
47	Martinoia E, Klein M, Geisler M, Bovet L, Forestier C, Kolukisaoglu Ü, Müller-Röber B, Schulz B (2002). Multifunctionality of plant ABC transporters—more than just detoxifiers.Planta 214, 345-355.
48	Motchoulski A, Liscum E (1999). Arabidopsis NPH3: a NPH1 photoreceptor-interacting protein essential for pho- totropism.Science 286, 961-964.
49	Mravec J, Skůpa P, Bailly A, Hoyerová K, Křeček P, Bielach A, Petrášek J, Zhang J, Gaykova V, Stierhof YD, Dobrev PI, Schwarzerová K, Rolčík J, Seifertová D, Luschnig C, Benková E, Zažímalová E, Geisler M, Friml J (2009). Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter. Nature 459, 1136-1140.
50	Nagashima A, Uehara Y, Sakai T (2008a). The ABC subfamily B auxin transporter AtABCB19 is involved in the inhibitory effects of N-1-naphthyphthalamic acid on the phototropic and gravitropic responses of Arabidopsis hypocotyls.Plant Cell Physiol 49, 1250-1255.
51	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 (2008b). Phytochromes and cryptochromes regulate the differential growth of Arabidopsis hypocotyls in both a PGP19-dependent and a PGP19-independent manner.Plant J 53, 516-529.
52	Noh B, Bandyopadhyay A, Peer WA, Spalding EP, Murphy AS (2003). Enhanced gravi- and phototropism in plant mdr mutants mislocalizing the auxin efflux protein PIN1.Nature 423, 999-1002.
53	Noh B, Murphy AS, Spalding EP (2001). Multidrug resistance-like genes of Arabidopsis required for auxin transport and auxin-mediated development.Plant Cell 13, 2441-2454.
54	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, 2223-2228.
55	Okada K, Shimura Y (1992). Mutational analysis of root gravitropism and phototropism of Arabidopsis thaliana seedlings.Aust J Plant Physiol 19, 439-448.
56	Okajima K, Matsuoka D, Tokutomi S (2011). LOV2-linker- kinase phosphorylates LOV1-containing N-terminal polypeptide substrate via photoreaction of LOV2 in Arabidopsis phototropin1.FEBS Lett 585, 3391-3395.
57	Pedmale UV, Liscum E (2007). Regulation of phototropic signaling in Arabidopsis via phosphorylation state changes in the phototropin 1-interacting protein NPH3.J Biol Chem 282, 19992-20001.
58	Robert HS, Friml J (2009). Auxin and other signals on the move in plants.Nat Chem Biol 5, 325-332.
59	Roberts D, Pedmale UV, Morrow J, Sachdev S, Lechner E, Tang XB, 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 CRL3NPH3.Plant Cell 23, 3627-3640.
60	Rösler J, Jaedicke K, Zeidler M (2010). Cytoplasmic phytochrome action.Plant Cell Physiol 51, 1248-1254.
61	Rösler J, Klein I, Zeidler M (2007). Arabidopsis fhl/fhy1 dou- ble mutant reveals a distinct cytoplasmic action of phyto- chrome A.Proc Natl Acad Sci USA 104, 10737-10742.
62	Sakai T, Kagawa T, Kasahara M, Swartz TE, Christie JM, Briggs WR, Wada M, Okada K (2001). Arabidopsis nph1 and npl1: blue light receptors that mediate both phototropism and chloroplast relocation.Proc Natl Acad Sci USA 98, 6969-6974.
63	Sakai T, Mochizuki S, Haga K, Uehara Y, Suzuki A, Harada A, Wada T, Ishiguro S, Okada K (2012). The WAVY GROWTH 3 E3 ligase family controls the gravitropic response in Arabidopsis roots.Plant J 70, 303-314.
64	Sakai T, Wada T, Ishiguro S, Okada K (2000). RPT2: a signal transducer of the phototropic response in Arabidopsis.Plant Cell 12, 225-236.
65	Sakamoto K, Briggs WR (2002). Cellular and subcellular localization of phototropin 1.Plant Cell 14, 1723-1735.
66	Salomon M, Knieb E, von Zeppelin T, Rüdiger W (2003). Mapping of low- and high-fluence autophosphorylation sites in phototropin 1.Biochemistry 42, 4217-4225.
67	Salomon M, Zacherl M, Luff L, Rüdiger W (1997a). Exposure of oat seedlings to blue light results in amplified phosphorylation of the putative photoreceptor for photo- tropism and in higher sensitivity of the plants to phototropic stimulation.Plant Physiol 115, 493-500.
68	Salomon M, Zacherl M, Rüdiger W (1997b). Asymmetric, blue light-dependent phosphorylation of a 116-kilodalton plasma membrane protein can be correlated with the first- and second-positive phototropic curvature of oat coleop- tiles. Plant Physiol 115, 485-491.
69	Schepens I, Boccalandro HE, Kami C, Casal JJ, Fankhauser C (2008). PHYTOCHROME KINASE SUB- STRATE4 modulates phytochrome-mediated control of hypocotyl growth orientation.Plant Physiol 147, 661-671.
70	Stone BB, Esmon CA, Liscum E (2005). Phototropins, other photoreceptors, and associated signaling: the lead and supporting cast in the control of plant movement responses.Curr Top Dev Biol 66, 215-238.
71	Stone BB, Stowe-Evans EL, Harper RM, Celaya RB, Ljung K, Sandberg G, Liscum E (2008). Disruptions in AUX1-dependent auxin influx alter hypocotyl phototropism in Arabidopsis.Mol Plant 1, 129-144.
72	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, 13705-13709.
73	Suetsugu N, Wada M (2007). Phytochrome-dependent photomovement responses mediated by phototropin fami- ly proteins in cryptogam plants.Photochem Photobiol 83, 87-93.
74	Sullivan S, Thomson CE, Lamont DJ, Jones MA, Christie JM (2008). In vivo phosphorylation site mapping and functional characterization of Arabidopsis phototropin 1.Mol Plant 1, 178-194.
75	Tanaka H, Dhonukshe P, Brewer PB, Friml J (2006). Spatiotemporal asymmetric auxin distribution: a means to coordinate plant development.Cell Mol Life Sci 63, 2738-2754.
76	Titapiwatanakun B, Blakeslee JJ, Bandyopadhyay A, Yang HB, Mravec J, Sauer M, Cheng Y, Adamec J, Nagashima A, Geisler M, Sakai T, Friml J, Peer WA, Murphy AS (2009). ABCB19/PGP19 stabilises PIN1 in membrane microdomains in Arabidopsis.Plant J 57, 27-44.
77	Titapiwatanakun B, Murphy AS (2009). Post-transcrip- tional regulation of auxin transport proteins: cellular trafficking, protein phosphorylation, protein maturation, ubi- quitination, and membrane composition.J Exp Bot 60, 1093-1107.
78	Tseng TS, Briggs WR (2010). The Arabidopsis rcn1-1 mutation impairs dephosphorylation of phot2, resulting in enhanced blue light responses.Plant Cell 22, 392-402.
79	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 trans- ducer, NPH3.Plant Sci 174, 626-633.
80	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, 653-662.
81	Vitha S, Zhao LM, Sack FD (2000). Interaction of root gravitropism and phototropism in Arabidopsis wild-type and starchless mutants.Plant Physiol 122, 453-462.
82	Wan YL, Eisinger W, Ehrhardt D, Kubitscheck U, Baluska F, Briggs W (2008). The subcellular localization and bl- ue-light-induced movement of phototropin 1-GFP in etio- lated seedlings ofArabidopsis thaliana. Mol Plant 1, 103-117.
83	Watahiki MK, Tatematsu K, Fujihira K, Yamamoto M, Yamamoto KT (1999). The MSG1 and AXR1 genes of Arabidopsis are likely to act independently in growth- curvature responses of hypocotyls.Planta 207, 362-369.
84	Went FW, Thimann KV (1937). Phytohormones. New York: Macmillan Company.
85	Whippo CW, Hangarter RP (2006). Phototropism: bending towards enlightenment.Plant Cell 18, 1110-1119.
86	Zažímalová E, Murphy AS, Yang H, Hoyerová K, Hošek P (2010). Auxin transporters. Why so many?Cold Spring Harb Perspect Biol 2, a001552.
87	Zhao X, Wang YL, Qiao XR, Wang J, Wang LD, Xu CS, Zhang X (2013). Phototropins function in high-intensity blue light-induced hypocotyl phototropism in Arabidopsis by altering cytosolic calcium.Plant Physiol 162, 1539-1551.