The Role of Auxin Transport and Distribution in Plant Gravimorphogenesis

  • Chiaki Yamazaki
  • Nobuharu Fujii
  • Hideyuki TakahashiEmail author
Part of the Signaling and Communication in Plants book series (SIGCOMM, volume 17)


Auxin is one of plant hormones that regulate various aspects of plant growth and development. It has long been proposed that auxin redistribute in response to gravity, which regulates gravimorphogenesis in plants. Recent molecular genetic analysis of Arabidopsis thaliana demonstrated that the gravity-regulated auxin redistribution is brought by auxin transport mediated by auxin efflux carriers. On the other hand, we have shown that the gravity-regulated morphogenesis, peg formation, of cucurbit seedlings is also controlled by auxin redistribution. Namely, cucumber (Cucumis sativus L.) seedlings have ability to develop a peg on each side of the transition zone between hypocotyl and root but develop one peg on the lower flank of the gravistimulated transition zone because its development on the upper flank is suppressed when the seedlings were grown in a horizontal position. The peg suppression occurs due to a reduction of auxin level on the upper flank. This auxin redistribution appears to involve a cucumber auxin efflux carrier CsPIN1 whose localization changes in response to gravistimulation. Here, we attempt to compare the mechanisms for gravimorphogenesis of cucumber seedlings and for gravity response in Arabidopsis seedlings.


Transition Zone Auxin Transport Elongation Zone Auxin Response Factor Endodermal Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This work was supported by Research Fellowship for Young Scientists from the Japan Society for the Promotion of Science (JSPS) to C.Y. and Grants-in-Aid for Scientific Research on Priority Areas (no. 19039005) and Grants-in-Aid for Scientific Research on Innovative Areas (no. 22120004) from the Ministry of Education, Culture, Sports, Science and Technology of Japan (MEXT) to H.T. This work was also carried out as a part of the Global COE Program J03 (Ecosystem Management Adapting to Global Change) of MEXT and the Research Working Group Program of the Japan Aerospace Exploration Agency (JAXA).


  1. Barlow PW, Sargent JA (1978) The ultrastructure of the regenerating root cap of Zea mays L. Ann Bot 42:791–799Google Scholar
  2. Benjamins R, Quint A, Weijers D, Hooykaas P, Offringa R (2001) The PINOID protein kinase regulates organ development in Arabidopsis by enhancing polar auxin transport. Development 128:4057–4067PubMedGoogle Scholar
  3. Blancaflor EB, Masson PH (2003) Plant gravitropism. Unraveling the ups and downs of a complex process. Plant Physiol 133:1677–1690PubMedCrossRefGoogle Scholar
  4. Blancaflor EB, Fasano JM, Gilroy S (1998) Mapping the functional roles of cap cells in the response of Arabidopsis primary roots to gravity. Plant Physiol 116:213–222PubMedCrossRefGoogle Scholar
  5. Boonsirichai K, Sedbrook JC, Chen R, Gilroy S, Masson PH (2003) ALTERED RESPONSE TO GRAVITY is a peripheral membrane protein that modulates gravity-induced cytoplasmic alkalinization and lateral auxin transport in plant statocytes. Plant Cell 15:2612–2625PubMedCrossRefGoogle Scholar
  6. Cline M (1997) Concepts and terminology of apical dominance. Am J Bot 84:1064–1069PubMedCrossRefGoogle Scholar
  7. Correll MJ, Kiss JZ (2002) Interactions between gravitropism and phototropism in plants. J Plant Glowth Regul 21:89–101CrossRefGoogle Scholar
  8. Darwin C, Darwin F (1881) The power of movement in plants. John Murray, LondonGoogle Scholar
  9. Dhonukshe P, Aniento F, Hwang I, Robinson DG, Mravec J, Stierhof YD, Friml J (2007) Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Curr Biol 17:520–527PubMedCrossRefGoogle Scholar
  10. Dhonukshe P, Grigoriev I, Fischer R, Tominaga M, Robinson DG, Hašek J, Paciorek T, Petrášek J, Seifertová D, Tejos R, Meisel LA, Zažímalová E, Gadella TW Jr, Stierhof YD, Ueda T, Oiwa K, Akhmanova A, Brock R, Spang A, Friml J (2008) Auxin transport inhibitors impair vesicle motility and actin cytoskeleton dynamics in diverse eukaryotes. Proc Natl Acad Sci USA 105:4489–4494PubMedCrossRefGoogle Scholar
  11. Ding Z, Galvan-Ampudia CS, Demarsy E, Łangowski L, Kleine-Vehn J, Fan Y, Morita MT, 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 13:447–452PubMedCrossRefGoogle Scholar
  12. Dolan L, Janmaat K, Willemsen V, Linstead P, Poethig S, Roberts K, Scheres B (1993) Cellular organisation of the Arabidopsis thaliana root. Development 119:71–84PubMedGoogle Scholar
  13. Evans ML (1991) Gravitropism: interaction of sensitivity modulation and effector redistribution. Plant Physiol 95:1–5PubMedCrossRefGoogle Scholar
  14. Fitzelle KJ, Kiss JZ (2001) Restoration of gravitropic sensitivity in starch-deficient mutants of Arabidopsis by hypergravity. J Exp Bot 52:265–275PubMedCrossRefGoogle Scholar
  15. Friml J, Wiśniewska J, Benková E, Mendgen K, Palme K (2002) Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415:806–809PubMedCrossRefGoogle Scholar
  16. Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jürgens G (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426:147–153PubMedCrossRefGoogle Scholar
  17. Friml J, Yang X, Michniewicz M, Weijers D, Quint A, Tietz O, Benjamins R, Ouwerkerk PB, Ljung K, Sandberg G, Hooykaas PJ, Palme K, Offringa R (2004) A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science 306:862–865PubMedCrossRefGoogle Scholar
  18. Fujii N, Kamada M, Yamasaki S, Takahashi H (2000) Differential accumulation of Aux/IAA mRNA during seedling development and gravity response in cucumber (Cucumis sativus L.). Plant Mol Biol 42:731–740PubMedCrossRefGoogle Scholar
  19. Fukaki H, Fujisawa H, Tasaka M (1997) The RHG gene is involved in root and hypocotyl gravitropism in Arabidopsis thaliana. Plant Cell Physiol 38:804–810PubMedCrossRefGoogle Scholar
  20. Fukaki H, Wysocka-Diller J, Kato T, Fujisawa H, Benfey PN, Tasaka M (1998) Genetic evidence that the endodermis is essential for shoot gravitropism in Arabidopsis thaliana. Plant J 14:425–430PubMedCrossRefGoogle Scholar
  21. Gälweiler L, Guan C, Müller A, Wisman E, Mendgen K, Yephremov A, Palme K (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282:2226–2230PubMedCrossRefGoogle Scholar
  22. Geldner N, Friml J, Stierhof YD, Jürgens G, Palme K (2001) Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413:425–428PubMedCrossRefGoogle Scholar
  23. Geldner N, Anders N, Wolters H, Keicher J, Kornberger W, Muller P, Delbarre A, Ueda T, Nakano A, Jürgens G (2003) The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112:219–230PubMedCrossRefGoogle Scholar
  24. Gray WM, del Pozo JC, Walker L, Hobbie L, Risseeuw E, Banks T, Crosby WL, Yang M, Ma H, Estelle M (1999) Identification of an SCF ubiquitin-ligase complex required for auxin response in Arabidopsis thaliana. Genes Dev 13:1678–1691PubMedCrossRefGoogle Scholar
  25. Gray WM, Kepinski S, Rouse D, Leyser O, Estelle M (2001) Auxin regulates SCF(TIR1)-dependent degradation of AUX/IAA proteins. Nature 414:271–276PubMedCrossRefGoogle Scholar
  26. Guan C, Rosen ES, Boonsirichai K, Poff KL, Masson PH (2003) The ARG1-LIKE2 gene of Arabidopsis functions in a gravity signal transduction pathway that is genetically distinct from the PGM pathway. Plant Physiol 133:100–112PubMedCrossRefGoogle Scholar
  27. Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10:453–460PubMedCrossRefGoogle Scholar
  28. Haberlandt G (1900) Über die Perzeption des geotropischen Reizes. Ber Dtsch Bot Ges 18:261–272Google Scholar
  29. Hagen G, Guilfoyle T (2002) Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol Biol 49:373–385PubMedCrossRefGoogle Scholar
  30. 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 12:757–770PubMedGoogle Scholar
  31. Harrison BR, Masson PH (2008) ARL2, ARG1 and PIN3 define a gravity signal transduction pathway in root statocytes. Plant J 53:380–392PubMedCrossRefGoogle Scholar
  32. Hatakeda Y, Kamada M, Goto N, Fukaki H, Tasaka M, Suge H, Takahashi H (2003) Gravitropic response plays an important role in the nutational movements of the shoots of Pharbitis nil and Arabidopsis thaliana. Physiol Plant 118:464–473Google Scholar
  33. Hoson T, Soga K (2003) New aspects of gravity responses in plant cells. Int Rev Cytol 229:209–244PubMedCrossRefGoogle Scholar
  34. Iino M (1995) Gravitropism and phototropism of maize coleoptiles: evaluation of the Cholodny-Went theory through effects of auxin application and decapitation. Plant Cell Physiol 36:361–367Google Scholar
  35. Kamada M, Fujii N, Aizawa S, Kamigaichi S, Mukai C, Shimazu T, Takahashi H (2000) Control of gravimorphogenesis by auxin: accumulation pattern of CS-IAA1 mRNA in cucumber seedlings grown in space and on the ground. Planta 211:493–501PubMedCrossRefGoogle Scholar
  36. Kamada M, Yamasaki S, Fujii N, Higashitani A, Takahashi H (2003) Gravity-induced modification of auxin transport and distribution for peg formation in cucumber seedlings: possible roles for CS-AUX1 and CS-PIN1. Planta 218:15–26PubMedCrossRefGoogle Scholar
  37. Kiss JZ, Sack FD (1989) Reduced gravitropic sensitivity in roots of a starch-deficient mutant of Nicotiana sylvestris. Planta 180:123–130PubMedCrossRefGoogle Scholar
  38. Kiss JZ, Hertel R, Sack FD (1989) Amyloplasts are necessary for full gravitropic sensitivity in roots of Arabidopsis thaliana. Planta 177:198–206PubMedCrossRefGoogle Scholar
  39. Kiss JZ, Wright JB, Caspar T (1996) Gravitropism in roots of intermediate-starch mutants of Arabidopsis. Physiol Plant 97:237–244PubMedCrossRefGoogle Scholar
  40. Kiss JZ, Guisinger MM, Miller AJ, Stackhouse KS (1997) Reduced gravitropism in hypocotyls of starch-deficient mutants of Arabidopsis. Plant Cell Physiol 38:518–525PubMedCrossRefGoogle Scholar
  41. Kitazawa D, Hatakeda Y, Kamada M, Fujii N, Miyazawa Y, Hoshino A, Iida S, Fukaki H, Morita MT, Tasaka M, Suge H, Takahashi H (2005) Shoot circumnutation and winding movements require gravisensing cells. Proc Natl Acad Sci USA 102:18742–18747Google Scholar
  42. Kitazawa D, Miyazawa Y, Fujii N, Hoshino A, Iida S, Nitasaka E, Takahashi H (2008) The gravity-regulated growth of axillary buds is mediated by a mechanism different from decapitation-induced release. Plant Cell Physiol 49:891–900Google Scholar
  43. Kleine-Vehn J, Dhonukshe P, Swarup R, Bennett M, Friml J (2006) Subcellular trafficking of the Arabidopsis auxin influx carrier AUX1 uses a novel pathway distinct from PIN1. Plant Cell 18:3171–3181PubMedCrossRefGoogle Scholar
  44. Kleine-Vehn J, Ding Z, Jones AR, Tasaka M, Morita MT, Friml J (2010) Gravity-induced PIN transcytosis for polarization of auxin fluxes in gravity-sensing root cells. Proc Natl Acad Sci USA 107:22344–22349PubMedCrossRefGoogle Scholar
  45. Knight TA (1806) On the direction of the radicle and germen during the vegetation of seeds. Philos Trans R Soc 99:108–120Google Scholar
  46. Kobayashi M, Murata T, Fujii N, Yamashita M, Higashitani A, Takahashi H (1999) A role of cytoskeletal structure of cortical cells in the gravity-regulated formation of a peg in cucumber seedlings. Adv Space Res 24:771–773PubMedCrossRefGoogle Scholar
  47. Leyser HM, Lincoln CA, Timpte C, Lammer D, Turner J, Estelle M (1993) Arabidopsis auxin-resistance gene AXR1 encodes a protein related to ubiquitin-activating enzyme E1. Nature 364:161–164PubMedCrossRefGoogle Scholar
  48. Li H, Lin D, Dhonukshe P, Nagawa S, Chen D, Friml J, Scheres B, Guo H, Yang Z (2011) Phosphorylation switch modulates the interdigitated pattern of PIN1 localization and cell expansion in Arabidopsis leaf epidermis. Cell Res 21:970–978PubMedCrossRefGoogle Scholar
  49. Lincoln C, Britton JH, Estelle M (1990) Growth and development of the axr1 mutants of Arabidopsis. Plant Cell 2:1071–1080PubMedGoogle Scholar
  50. Massa GD, Gilroy S (2003) Touch modulates gravity sensing to regulate the growth of primary roots of Arabidopsis thaliana. Plant J 33:435–445PubMedCrossRefGoogle Scholar
  51. Michniewicz M, Zago MK, Abas L, Weijers D, Schweighofer A, Meskiene I, Heisler MG, Ohno C, Zhang J, Huang F, Schwab R, Weigel D, Meyerowitz EM, Luschnig C, Offringa R, Friml J (2007) Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell 130:1044–1056PubMedCrossRefGoogle Scholar
  52. Morita MT (2010) Directional gravity sensing in gravitropism. Annu Rev Plant Biol 61:705–720PubMedCrossRefGoogle Scholar
  53. Morita Y, Kyozuka J (2007) Characterization of OsPID, the rice ortholog of PINOID, and its possible involvement in the control of polar auxin transport. Plant Cell Physiol 48:540–549PubMedCrossRefGoogle Scholar
  54. Morita MT, Kato T, Nagafusa K, Saito C, Ueda T, Nakano A, Tasaka M (2002) Involvement of the vacuoles of the endodermis in the early process of shoot gravitropism in Arabidopsis. Plant Cell 14:47–56PubMedCrossRefGoogle Scholar
  55. Muday GK (2001) Auxins and tropisms. J Plant Growth Regul 20:226–243PubMedCrossRefGoogle Scholar
  56. Müller A, Guan C, Gälweiler L, Tänzler P, Huijser P, Marchant A, Parry G, Bennett M, Wisman E, Palme K (1998) AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J 17:6903–6911PubMedCrossRefGoogle Scholar
  57. Nemec B (1900) Über die Art der Wahmehmung des. Schwerkraftes bei den Pflanzen. Ber Dtsch Bot Ges 18:241–245Google Scholar
  58. Niihama M, Uemura T, Saito C, Nakano A, Sato MH, Tasaka M, Morita MT (2005) Conversion of functional specificity in Qb-SNARE VTI1 homologues of Arabidopsis. Curr Biol 15:555–560PubMedCrossRefGoogle Scholar
  59. Okushima Y, Overvoorde PJ, Arima K, Alonso JM, Chan A, Chang C, Ecker JR, 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 17:444–463PubMedCrossRefGoogle Scholar
  60. Peer WA, Blakeslee JJ, Yang H, Murphy AS (2011) Seven things we think we know about auxin transport. Mol Plant 4:487–504PubMedCrossRefGoogle Scholar
  61. Perbal G, Driss-Ecole D (2003) Mechanotransduction in gravisensing cells. Trends Plant Sci 8:498–504PubMedCrossRefGoogle Scholar
  62. Perrin RM, Young LS, Murthy UMN, Harrison BR, Wang Y, Will JL, Masson PH (2005) Gravity signal transduction in primary roots. Ann Bot 96:737–743PubMedCrossRefGoogle Scholar
  63. Peyroche A, Antonny B, Robineau S, Acker J, Cherfils J, Jackson CL (1999) Brefeldin A acts to stabilize an abortive ARF-GDP-Sec7 domain protein complex: involvement of specific residues of the Sec7 domain. Mol Cell 3:275–285PubMedCrossRefGoogle Scholar
  64. Rakusová H, Gallego-Bartolomé J, Vanstraelen M, Robert HS, Alabadí D, Blázquez MA, Benková E, Friml J (2011) Polarization of PIN3-dependent auxin transport for hypocotyl gravitropic response in Arabidopsis thaliana. Plant J 67:817–826PubMedCrossRefGoogle Scholar
  65. Rouse D, Mackay P, Stirnberg P, Estelle M, Leyser O (1998) Changes in auxin response from mutations in an AUX/IAA gene. Science 279:1371–1373PubMedCrossRefGoogle Scholar
  66. Sachs J (1882) Über Ausschliessung der geotropischen und heliotropischen Krümmungen während des Wachsens. Arb Bot Inst Würzburg 2:209–225Google Scholar
  67. Saito Y, Yamasaki S, Fujii N, Hagen G, Guilfoyle T, Takahashi H (2004) Isolation of cucumber CsARF cDNAs and expression of the corresponding mRNAs during gravity-regulated morphogenesis of cucumber seedlings. J Exp Bot 55:1315–1323PubMedCrossRefGoogle Scholar
  68. Saito Y, Yamasaki S, Fujii N, Takahashi H (2005) Possible involvement of CS-ACS1 and ethylene in auxin-induced peg formation of cucumber seedlings. Ann Bot 95:413–422PubMedCrossRefGoogle Scholar
  69. Sanderfoot AA, Raikhel NV (1999) The specificity of vesicle trafficking: coat proteins and SNAREs. Plant Cell 11:629–642PubMedGoogle Scholar
  70. Shimizu M, Suzuki K, Miyazawa Y, Fujii N, Takahashi H (2006) Differential accumulation of the mRNA of the auxin-repressed gene CsGRP1 and the auxin-induced peg formation during gravimorphogenesis of cucumber seedlings. Planta 225:13–22PubMedCrossRefGoogle Scholar
  71. Shimizu M, Miyazawa Y, Fujii N, Takahashi H (2008) p-Chlorophenoxyisobutyric acid impairs auxin response for gravity-regulated peg formation in cucumber (Cucumis sativus) seedlings. J Plant Res 121:107–114PubMedCrossRefGoogle Scholar
  72. Sievers A (1991) Gravity sensing mechanisms in plant cells. ASGSB Bull 4:43–50PubMedGoogle Scholar
  73. Skirpan A, Culler AH, Gallavotti A, Jackson D, Cohen JD, McSteen P (2009) BARREN INFLORESCENCE2 interaction with ZmPIN1a suggests a role in auxin transport during maize inflorescence development. Plant Cell Physiol 50:652–657PubMedCrossRefGoogle Scholar
  74. Stanga JP, Boonsirichai K, Sedbrook JC, Otegui MS, Masson PH (2009) A role for the TOC complex in Arabidopsis root gravitropism. Plant Physiol 149:1896–1905PubMedCrossRefGoogle Scholar
  75. Stowe-Evans EL, Harper RM, Motchoulski AV, Liscum E (1998) NPH4, a conditional modulator of auxin-dependent differential growth responses in Arabidopsis. Plant Physiol 118:1265–1275PubMedCrossRefGoogle Scholar
  76. Sukumar P, Edwards KS, Rahman A, Delong A, Muday GK (2009) PINOID kinase regulates root gravitropism through modulation of PIN2-dependent basipetal auxin transport in Arabidopsis. Plant Physiol 150:722–735PubMedCrossRefGoogle Scholar
  77. Takahashi H (1997) Gravimorphogenesis: gravity-regulated formation of the peg in cucumber seedlings. Planta 203:S164–S169PubMedCrossRefGoogle Scholar
  78. Takahashi H, Scott TK (1994) Gravity-regulated formation of the peg in developing cucumber seedlings. Planta 193:580–584PubMedCrossRefGoogle Scholar
  79. Takahashi H, Suge H (1988) Involvement of ethylene in gravity-regulated peg development in cucumber seedling. Plant Cell Physiol 29:313–320Google Scholar
  80. Takahashi H, Kamada M, Yamazaki Y, Fujii N, Higashitani A, Aizawa S, Yoshizaki I, Kamigaichi S, Mukai C, Shimazu T, Fukui K (2000) Morphogenesis in cucumber seedlings is negatively controlled by gravity. Planta 210:515–518PubMedCrossRefGoogle Scholar
  81. Takahashi H, Miyazawa Y, Fujii N (2009) Hormonal interactions during root tropic growth: hydrotropism versus gravitropism. Plant Mol Biol 69:489–502PubMedCrossRefGoogle Scholar
  82. Tan X, Calderon-Villalobos LI, Sharon M, Zheng C, Robinson CV, Estelle M, Zheng N (2007) Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446:640–645PubMedCrossRefGoogle Scholar
  83. Tatematsu K, Kumagai S, Muto H, Sato A, Watahiki MK, Harper RM, Liscum E, Yamamoto KT (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 16:379–393PubMedCrossRefGoogle Scholar
  84. Tiwari SB, Hagen G, Guilfoyle TJ (2004) Aux/IAA proteins contain a potent transcriptional repression domain. Plant Cell 16:533–543PubMedCrossRefGoogle Scholar
  85. Trewavas AJ (1992a) What remains of the Cholodny-Went theory? A summing up. Plant Cell Environ 15:793–794PubMedGoogle Scholar
  86. Trewavas AJ (1992b) What remains of the Cholodny-Went theory? Introduction. Plant Cell Environ 15:761PubMedGoogle Scholar
  87. Ulmasov T, Hagen G, Guilfoyle TJ (1997) ARF1, a transcription factor that binds to auxin response elements. Science 276:1865–1868PubMedCrossRefGoogle Scholar
  88. Ulmasov T, Hagen G, Guilfoyle TJ (1999) Activation and repression of transcription by auxin-response factors. Proc Natl Acad Sci USA 96:5844–5849PubMedCrossRefGoogle Scholar
  89. Wareing PF, NASR TAA (1958) Gravimorphism in trees: effect of gravity on growth, apical dominance and flowering in fruit trees. Nature 182:379–381Google Scholar
  90. Watahiki MK, Yamamoto KT (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 115:419–426PubMedCrossRefGoogle Scholar
  91. Watanabe C, Fujii N, Yanai K, Hotta T, Kim DH, Kamada M, Sasagawa-Saito Y, Nishimura T, Koshiba T, Miyazawa Y, Kim KM, Takahashi H (2012) Gravistimulation changes the accumulation pattern of the CsPIN1 auxin efflux facilitator in the endodermis of the transition zone in cucumber seedlings. Plant Physiol 158:239–251PubMedCrossRefGoogle Scholar
  92. Went FW, Thimann KV (1937) Phytohormones. Macmillian, NewYorkGoogle Scholar
  93. Wiśniewska J, Xu J, Seifertová D, Brewer PB, Ruzicka K, Blilou I, Rouquié D, Benková E, Scheres B, Friml J (2006) Polar PIN localization directs auxin flow in plants. Science 312:883PubMedCrossRefGoogle Scholar
  94. Witztum A, Gersani M (1975) The role of IAA in the development of the peg in Cucumis sativus L. Bot Gaz 136:5–16CrossRefGoogle Scholar
  95. Yano D, Sato M, Saito C, Sato MH, Morita MT, Tasaka M (2003) A SNARE complex containing SGR3/AtVAM3 and ZIG/VTI11 in gravity-sensing cells is important for Arabidopsis shoot gravitropism. Proc Natl Acad Sci USA 100:8589–8594PubMedCrossRefGoogle Scholar
  96. Zhang J, Nodzynski T, Pencík A, Rolcík J, Friml J (2010) PIN phosphorylation is sufficient to mediate PIN polarity and direct auxin transport. Proc Natl Acad Sci USA 107:918–922PubMedCrossRefGoogle Scholar
  97. Zheng H, von Mollard GF, Kovaleva V, Stevens TH, Raikhel NV (1999) The plant vesicle-associated SNARE AtVTI1a likely mediates vesicle transport from the trans-Golgi network to the prevacuolar compartment. Mol Biol Cell 10:2251–2264PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Chiaki Yamazaki
    • 1
    • 2
  • Nobuharu Fujii
    • 1
  • Hideyuki Takahashi
    • 1
    Email author
  1. 1.Graduate School of Life SciencesTohoku UniversityAoba-kuJapan
  2. 2.Kihara Institute of Biological ResearchYokohama City UniversityTotsukaJapan

Personalised recommendations