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Molecular basis of chloroplast photorelocation movement

  • JPR Symposium
  • The Cutting Edge of Photoresponse Mechanisms: Photoreceptor and Signaling Mechanism
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Abstract

Chloroplast photorelocation movement is an essential physiological response for sessile plant survival and the optimization of photosynthetic ability. Simple but effective experiments on the physiological, cell biological and molecular genetic aspects have been widely used to investigate the signaling components of chloroplast photorelocation movement in Arabidopsis for the past few decades. Although recent knowledge on chloroplast photorelocation movement has led us to a deeper understanding of its physiological and molecular basis, the biochemical roles of the downstream factors remain largely unknown. In this review, we briefly summarize recent advances regarding chloroplast photorelocation movement and propose that a new high-resolution approach is necessary to investigate the molecular mechanism underlying actin-based chloroplast photorelocation movement.

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Abbreviations

Cp-actin:

Chloroplast actin

LOV:

Light, oxygen, or voltage

phot:

Phototropin

phy:

Phytochrome

References

  • Aggarwal C, Banaś AK, 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 65:3263–3276

    Article  PubMed Central  PubMed  Google Scholar 

  • Aihara Y, Tabata R, Suzuki T, Shimazaki K-I, Nagatani A (2008) Molecular basis of the functional specificities of phototropin 1 and 2. Plant J 56:364–375

    Article  CAS  PubMed  Google Scholar 

  • Banaś AK, Aggarwal C, Łabuz J, Sztatelman O, Gabryś H (2012) Blue light signalling in chloroplast movements. J Exp Bot 63:1559–1574

    Article  PubMed  Google Scholar 

  • Boex-Fontvieille E, Jossier M, Davanture M, Zivy M, Hodges M, Tcherkez G (2014) Differential protein phosphorylation regulates chloroplast movement in response to strong light and darkness in Arabidopsis thaliana. Plant Mol Biol Rep 32:987–1001

    Article  CAS  Google Scholar 

  • Briggs WR, Christie JM (2002) Phototropins 1 and 2: versatile plant blue-light receptors. Trends Plant Sci 7:204–210

    Article  CAS  PubMed  Google Scholar 

  • Briggs WR, Beck CF, Cashmore AR, Christie JM, Hughes J, Jarillo JA, Kagawa T, Kanegae H, Liscum E, Nagatani A, Okada K, Salomon M, Rudiger W, Sakai T, Takano M, Wada M, Watson JC (2001) The phototropin family of photoreceptors. Plant Cell 13:993–997

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Christie JM (2007) Phototropin blue-light receptors. Annu Rev Plant Biol 58:21–45

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Christie JM, Yang H, Richter GL, Sullivan S, Thomson CE, Lin J, 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:e1001076

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Davis PA, Hangarter RP (2012) Chloroplast movement provides photoprotection to plants by redistributing PSII damage within leaves. Photosynth Res 112:153–161

    Article  CAS  PubMed  Google Scholar 

  • de Carbonnel M, Davis P, Roelfsema MR, Inoue S-I, Schepens I, Lariguet P, Geisler M, Shimazaki K-I, 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

    Article  PubMed Central  PubMed  Google Scholar 

  • DeBlasio SL, Mullen JL, Luesse DR, Hangarter RP (2003) Phytochrome modulation of blue light-induced chloroplast movements in Arabidopsis. Plant Physiol 133:1471–1479

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • DeBlasio SL, Luesse DL, Hangarter RP (2005) A plant-specific protein essential for blue-light-induced chloroplast movements. Plant Physiol 139:101–114

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Demarsy E, Fankhauser C (2009) Higher plants use LOV to perceive blue light. Curr Opin Plant Biol 12:69–74

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Deng Z, Oses-Prieto JA, Kutschera U, Tseng T-S, Hao L, Burlingame AL, Wang Z-Y, Briggs WR (2014) Blue light-induced proteomic changes in etiolated Arabidopsis seedlings. J Proteome Res 13:2524–2533

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Franklin KA, Larner VS, Whitelam GC (2005) The signal transducing photoreceptors of plants. Int J Dev Biol 49:653–664

    Article  CAS  PubMed  Google Scholar 

  • Gabryś H, Walczak T (1980) Photometric study of chloroplast phototranslocation in leaves of land plant. Acta Physiol Plant 2:281–290

    Google Scholar 

  • Higa T, Wada M (2015) Clues to the signals for chloroplast photo-relocation from the lifetimes of accumulation and avoidance responses. J Integr Plant Biol 57:120–126

    Article  CAS  PubMed  Google Scholar 

  • Ichikawa S, Yamada N, Suetsugu N, Wada M, Kadota A (2011) Red light, phot1 and JAC1 modulate phot2-dependent reorganization of chloroplast actin filaments and chloroplast avoidance movement. Plant Cell Physiol 52:1422–1432

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Jaedicke K, Lichtenthaler AL, Meyberg R, Zeidler M, Hughes J (2012) A phytochrome-phototropin light signaling complex at the plasma membrane. Proc Natl Acad Sci USA 109:12231–12236

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jarillo JA, Gabryś H, Capel J, Alonso JM, Ecker JR, Cashmore AR (2001) Phototropin-related NPL1 controls chloroplast relocation induced by blue light. Nature 410:952–954

    Article  CAS  PubMed  Google Scholar 

  • Jenkins GI (2014) Structure and function of the UV-B photoreceptor UVR8. Curr Opin Struct Biol 29:52–57

    Article  CAS  PubMed  Google Scholar 

  • Kadota A, Sato Y, Wada M (2000) Intracellular chloroplast photorelocation in the moss Physcomitrella patens is mediated by phytochrome as well as by a blue-light receptor. Planta 210:932–937

    Article  CAS  PubMed  Google Scholar 

  • Kadota A, Yamada N, Suetsugu N, Hirose M, Saito C, Shoda K, Ichikawa S, Kagawa T, Nakano A, Wada M (2009) Short actin-based mechanism for light-directed chloroplast movement in Arabidopsis. Proc Natl Acad Sci USA 106:13106–13111

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kagawa T, Wada M (1994) Brief irradiation with red or blue light induces orientational movement of chloroplasts in dark-adapted prothallial cells of the fern Adiantum. J Plant Res 107:389–398

    Article  Google Scholar 

  • Kagawa T, Wada M (2000) Blue light-induced chloroplast relocation in Arabidopsis thaliana as analyzed by microbeam irradiation. Plant Cell Physiol 41:84–93

    Article  CAS  PubMed  Google Scholar 

  • Kagawa T, Wada M (2004) Velocity of chloroplast avoidance movement is fluence rate dependent. Photochem Photobiol Sci 3:592–595

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kasahara M, Kagawa T, Oikawa K, Suetsugu N, Miyao M, Wada M (2002) Chloroplast avoidance movement reduces photodamage in plants. Nature 420:829–832

    Article  CAS  PubMed  Google Scholar 

  • Kasahara M, Kagawa T, Sato Y, Kiyosue T, Wada M (2004) Phototropins mediate blue and red light-induced chloroplast movements in Physcomitrella patens. Plant Physiol 135:1388–1397

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kataoka H (2015) Gustav Senn (1875–1945): the pioneer of chloroplast movement research. J Integr Plant Biol 57:4–13

    Article  PubMed  Google Scholar 

  • Kawai H, Kanegae T, Christensen S, Kiyosue T, Sato Y, Imaizumi T, Kadota A, Wada M (2003) Responses of ferns to red light are mediated by an unconventional photoreceptor. Nature 421:287–290

    Article  CAS  PubMed  Google Scholar 

  • Kimura M, Kagawa T (2009) Blue light-induced chloroplast avoidance and phototropic responses exhibit distinct dose dependency of PHOTOTROPIN2 in Arabidopsis thaliana. Photochem Photobiol 85:1260–1264

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed Central  PubMed  Google Scholar 

  • Kodama Y, Suetsugu N, Kong S-G, Wada M (2010) Two interacting coiled-coil proteins, WEB1 and PMI2, maintain the chloroplast photorelocation movement velocity in Arabidopsis. Proc Natl Acad Sci USA 107:19591–19596

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kong S-G, Wada M (2011) New insights into dynamic actin-based chloroplast photorelocation movement. Mol Plant 4:771–781

    Article  CAS  PubMed  Google Scholar 

  • Kong S-G, Wada M (2014) Recent advances in understanding the molecular mechanism of chloroplast photorelocation movement. Biochim Biophys Acta 1837:522–530

    Article  CAS  PubMed  Google Scholar 

  • 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 45:994–1005

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kong S-G, Arai Y, Suetsugu N, Yanagida T, Wada M (2013a) Rapid severing and motility of chloroplast-actin filaments are required for the chloroplast avoidance response in Arabidopsis. Plant Cell 25:572–590

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kozuka T, Kong S-G, Doi M, Shimazaki K-I, Nagatani A (2011) Tissue-autonomous promotion of palisade cell development by phototropin 2 in Arabidopsis. Plant Cell 23:3684–3695

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Łabuz J, Sztatelman O, Banas AK, Gabryś H (2012) The expression of phototropins in Arabidopsis leaves: developmental and light regulation. J Exp Bot 63:1763–1771

    Article  PubMed  Google Scholar 

  • Luesse DR, DeBlasio SL, Hangarter RP (2010) Integration of phot1, phot2, and phyB signalling in light-induced chloroplast movements. J Exp Bot 61:4387–4397

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Matsuoka D, Tokutomi S (2005) Blue light-regulated molecular switch of Ser/Thr kinase in phototropin. Proc Natl Acad Sci USA 102:13337–13342

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Oikawa K, Kasahara M, Kiyosue T, Kagawa T, Suetsugu N, Takahashi F, Kanegae T, Niwa Y, Kadota A, Wada M (2003) Chloroplast unusual positioning1 is essential for proper chloroplast positioning. Plant Cell 15:2805–2815

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Oikawa K, Yamasato A, Kong S-G, Kasahara M, Nakai M, Takahashi F, Ogura Y, Kagawa T, Wada M (2008) Chloroplast outer envelope protein CHUP1 is essential for chloroplast anchorage to the plasma membrane and chloroplast movement. Plant Physiol 148:829–842

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Preuten T, Blackwood L, Christie JM, 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 206:1038–1050

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sakamoto K, Briggs WR (2002) Cellular and subcellular localization of phototropin 1. Plant Cell 14:1723–1735

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Salomon M, Christie JM, Knieb E, Lempert U, Briggs WR (2000) Photochemical and mutational analysis of the FMN-binding domains of the plant blue light receptor, phototropin. Biochemistry 39:9401–9410

    Article  CAS  PubMed  Google Scholar 

  • Schönbohm E (1980) Phytochrome and non-phytochrome dependent blue light effects on intracellular movements in fresh-water algae. In: Senger H (ed) The Blue Light Syndrome. Springer-Verlag, New York, pp 69–96

    Chapter  Google Scholar 

  • Senn G (1908) Die Gestalts- und Lageveränderung der Pflanzen- Chromatophoren. Wilhelm Engelmann, Leipzig

    Google Scholar 

  • Staiger CJ, Sheahan MB, Khurana P, Wang X, McCurdy DW, Blanchoin L (2009) Actin filament dynamics are dominated by rapid growth and severing activity in the Arabidopsis cortical array. J Cell Biol 184:269–280

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Suetsugu N, Wada M (2003) Cryptogam blue-light photoreceptors. Curr Opin Plant Biol 6:91–96

    Article  CAS  PubMed  Google Scholar 

  • Suetsugu N, Wada M (2007a) Chloroplast photorelocation movement mediated by phototropin family proteins in green plants. Biol Chem 388:927–935

    Article  CAS  PubMed  Google Scholar 

  • Suetsugu N, Wada M (2007b) Phytochrome-dependent photomovement responses mediated by phototropin family proteins in cryptogam plants. Photochem Photobiol 83:87–93

    CAS  PubMed  Google Scholar 

  • Suetsugu N, Kagawa T, Wada M (2005a) An auxilin-like J-domain protein, JAC1, regulates phototropin-mediated chloroplast movement in Arabidopsis. Plant Physiol 139:151–162

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Suetsugu N, Yamada N, Kagawa T, Yonekura H, Uyeda TQ, Kadota A, Wada M (2010) Two kinesin-like proteins mediate actin-based chloroplast movement in Arabidopsis thaliana. Proc Natl Acad Sci USA 107:8860–8865

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Suetsugu N, Higa T, Kong S-G, Wada M (2015) PLASTID MOVEMENT IMPAIRED1 and PLASTID MOVEMENT IMPAIRED1-RELATED1 mediate photorelocation movements of both chloroplasts and nuclei. Plant Physiol 169:1155–1167

    Article  PubMed Central  PubMed  Google Scholar 

  • Swartz TE, Corchnoy SB, Christie JM, Lewis JW, Szundi I, Briggs WR, Bogomolni RA (2001) The photocycle of a flavin-binding domain of the blue light photoreceptor phototropin. J Biol Chem 276:36493–36500

    Article  CAS  PubMed  Google Scholar 

  • Sztatelman O, Waloszek A, Banaś AK, Gabryś H (2010) Photoprotective function of chloroplast avoidance movement: In vivo chlorophyll fluorescence study. J Plant Physiol 167:709–716

    Article  CAS  PubMed  Google Scholar 

  • Takagi S, Islam MS, Iwabuchi K (2011) Dynamic behavior of double-membrane-bounded organelles in plant cells. Int Rev Cell Mol Biol 286:181–222

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Takemiya A, Sugiyama N, Fujimoto H, Tsutsumi T, Yamauchi S, Hiyama A, Tada Y, Christie JM, Shimazaki K-I (2013) Phosphorylation of BLUS1 kinase by phototropins is a primary step in stomatal opening. Nat Commun 4:2094

    Article  PubMed  Google Scholar 

  • Tsuboi H, Wada M (2010) Speed of signal transfer in the chloroplast accumulation response. J Plant Res 123:381–390

    Article  CAS  PubMed  Google Scholar 

  • Tsuboi H, Wada M (2011) Chloroplasts can move in any direction to avoid strong light. J Plant Res 124:201–210

    Article  PubMed  Google Scholar 

  • Tsuboi H, Wada M (2013) Chloroplasts continuously monitor photoreceptor signals during accumulation movement. J Plant Res 126:557–566

    Article  CAS  PubMed  Google Scholar 

  • Tsuboi H, Yamashita H, Wada M (2009) Chloroplasts do not have a polarity for light-induced accumulation movement. J Plant Res 122:131–140

    Article  PubMed  Google Scholar 

  • Wada M (2013) Chloroplast movement. Plant Sci 210:177–182

    Article  CAS  PubMed  Google Scholar 

  • Wada M, Kong S-G (2011) Analysis of chloroplast movement and relocation in Arabidopsis. Methods Mol Biol 774:87–102

    Article  CAS  PubMed  Google Scholar 

  • Wada M, Kagawa T, Sato Y (2003) Chloroplast movement. Annu Rev Plant Biol 54:455–468

    Article  CAS  PubMed  Google Scholar 

  • Whippo CW, Khurana P, Davis PA, DeBlasio SL, DeSloover D, Staiger CJ, Hangarter RP (2011) THRUMIN1 is a light-regulated actin-bundling protein involved in chloroplast motility. Curr Biol 21:59–64

    Article  CAS  PubMed  Google Scholar 

  • Yatsuhashi H, Kadota A, Wada M (1985) Blue- and red-light action in photoorientation of chloroplasts in Adiantum protonemata. Planta 165:43–50

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by JSPS KAKENHI grant number 25440140 to S.-G. K. and 23120523, 25120721, and 25251033 to M.W.

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Authors and Affiliations

  1. Division of Structural Biology, Medical Institute of Bioregulation, Kyushu University, Higashi-ku, Fukuoka, 812-8582, Japan

    Sam-Geun Kong

  2. Research Center for Live-Protein Dynamics, Kyushu University, Higashi-ku, Fukuoka, 812-8582, Japan

    Sam-Geun Kong

  3. Department of Biological Sciences, Graduate School of Science and Engineering, Tokyo Metropolitan University, Tokyo, 192-0397, Japan

    Masamitsu Wada

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  1. Sam-Geun Kong
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  2. Masamitsu Wada
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Correspondence to Sam-Geun Kong.

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Kong, SG., Wada, M. Molecular basis of chloroplast photorelocation movement. J Plant Res 129, 159–166 (2016). https://doi.org/10.1007/s10265-016-0788-1

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