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Gravitropism in Higher Plants: Molecular Aspects

  • Klaus Palme
  • William Teale
  • Franck Ditengou
Chapter
Part of the SpringerBriefs in Space Life Sciences book series (BRIEFSSLS)

Abstract

The pervasive influence of gravity on life on Earth presents barriers to our identifying and understanding of the signaling pathways which have evolved in response to it. Plants are at the same time positively and negatively gravitropic, using the Earth’s gravity to define their stature both above and below ground. Here we review some of the signaling pathways which use the plant hormone auxin to carry information on orientation from regions of perception to regions of growth response. The regulation of these pathways is at once diverse and as yet poorly understood but involves the control of members of a family of polarly localized cellular auxin efflux carriers, the PINs, by factors such as phosphorylation. Auxin transport is also influenced by the availability of calcium ions; this interaction is likely to emerge as a key node in a plant’s responses to gravity. It is hoped that understanding the mechanism of these responses will not only allow more efficient cultivation of plants in space, but open paths to greater control over plant stature which will enable us, in the future, better to respond to the challenges of feeding those of us still living on Earth.

Keywords

Auxin Higher plant gravitropism Kinase signaling Microgravity Plant hormone 

References

  1. Aloni R, Langhans M, Aloni E, Ullrich CI (2004) Role of cytokinin in the regulation of root gravitropism. Planta 220:177–182PubMedCrossRefGoogle Scholar
  2. Aloni R, Aloni E, Langhans M, Ullrich CI (2006) Role of Cytokinin and Auxin in shaping root architecture: regulating vascular differentiation, lateral root initiation, root apical dominance and root Gravitropism. Ann Bot 97:883–893PubMedPubMedCentralCrossRefGoogle Scholar
  3. Aubry-Hivet D, Nziengui H, Rapp K, Oliveira O, Paponov IA, Li Y, Hauslage J, Vagt N, Braun M, Ditengou FA, Dovzhenko A, Palme K (2014) Analysis of gene expression during parabolic flights reveals distinct early gravity responses in Arabidopsis roots. Plant Biol 16:129–141PubMedCrossRefGoogle Scholar
  4. Barlow PW (2015) Leaf movements and their relationship with the lunisolar gravitational force. Ann Bot 116:149–187PubMedPubMedCentralCrossRefGoogle Scholar
  5. Barlow PW, Fisahn J (2012) Lunisolar tidal force and the growth of plant roots, and some other of its effects on plant movements. Ann Bot 110:301–318PubMedPubMedCentralCrossRefGoogle Scholar
  6. Bennett MJ, Marchant A, Green HG, May ST, Ward SP, Millner PA, Walker AR, Schulz B, Feldmann KA (1996) Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science 273:948–950CrossRefPubMedGoogle Scholar
  7. Boonsirichai K, Sedbrook JC, Chen RJ, 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 15:2612–2625PubMedPubMedCentralCrossRefGoogle Scholar
  8. Braybrook SA (2017) Plant development: lessons from getting it twisted. Curr Biol 27:R758–R760PubMedCrossRefGoogle Scholar
  9. Briegleb W (1992) Some qualitative and quantitative aspects of the fast-rotating clinostat as a research tool. ASGSB Bull 5:23–30PubMedGoogle Scholar
  10. Buer CS, Muday GK (2004) The transparent testa4 mutation prevents flavonoid synthesis and alters auxin transport and the response of Arabidopsis roots to gravity and light. Plant Cell 16:1191–1205PubMedPubMedCentralCrossRefGoogle Scholar
  11. Buer CS, Muday GK, Djordjevic MA (2007) Flavonoids are differentially taken up and transported long distances in Arabidopsis. Plant Physiol 145:478–490PubMedPubMedCentralCrossRefGoogle Scholar
  12. Cho M, Henry EM, Lewis DR, Wu GS, Muday GK, Spalding EP (2014) Block of ATP-binding cassette B19 ion channel activity by 5-Nitro-2-(3-Phenylpropylamino)-benzoic acid impairs polar auxin transport and toot gravitropism. Plant Physiol 166:2091–2099PubMedPubMedCentralCrossRefGoogle Scholar
  13. Corydon TJ, Kopp S, Wehland M, Braun M, Schutte A, Mayer T, Hulsing T, Oltmann H, Schmitz B, Hemmersbach R, Grimm D (2016) Alterations of the cytoskeleton in human cells in space proved by life-cell imaging. Sci Rep 6:20043PubMedPubMedCentralCrossRefGoogle Scholar
  14. Darwin C (1880) The power of movement in plants. John Murray, LondonCrossRefGoogle Scholar
  15. De Bortoli S, Teardo E, Szabò I, Morosinotto T, Alboresi A (2016) Evolutionary insight into the ionotropic glutamate receptor superfamily of photosynthetic organisms. Biophys Chem 218:14–26PubMedCrossRefGoogle Scholar
  16. De Smet I, Tetsumura T, De Rybel B, Frey NFD, Laplaze L, Casimiro I, Swarup R, Naudts M, Vanneste S, Audenaert D, Inze D, Bennett MJ, Beeckman T (2007) Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis. Development 134:681–690PubMedCrossRefGoogle Scholar
  17. Dindas J, Scherzer S, Roelfsema MRG, von Meyer K, Muller HM, Al-Rasheid KAS, Palme K, Dietrich P, Becker D, Bennett MJ, Hedrich R (2018) AUX1-mediated root hair auxin influx governs SCF(TIR1/AFB)-type Ca(2+) signaling. Nat Commun 9:1174PubMedPubMedCentralCrossRefGoogle Scholar
  18. Ditengou FA, Teale WD, Kochersperger P, Flittner KA, Kneuper I, Van Der Graaff E, Nziengui H, Pinosa F, Li X, Nitschke R, Laux T, Palme K (2008) Mechanical induction of lateral root initiation in Arabidopsis thaliana. Proc Natl Acad Sci U S A 105:18818–18823PubMedPubMedCentralCrossRefGoogle Scholar
  19. Ditengou FA, Gomes D, Nziengui H, Kochersperger P, Lasok H, Medeiros V, Paponov IA, Nagy SK, Nadai TV, Meszaros T, Barnabas B, Ditengou BI, Rapp K, Qi LL, Li XG, Becker C, Li CY, Doczi R, Palme K (2018) Characterization of auxin transporter PIN6 plasma membrane targeting reveals a function for PIN6 in plant bolting. New Phytol 217:1610–1624PubMedCrossRefGoogle Scholar
  20. Dory M, Hatzimasoura E, Kallai BM, Nagy SK, Jager K, Darula Z, Nadai TV, Meszaros T, Lopez-Juez E, Barnabas B, Palme K, Bogre L, Ditengou FA, Doczi R (2018) Coevolving MAPK and PID phosphosites indicate an ancient environmental control of PIN auxin transporters in land plants. FEBS Lett 592:89–102PubMedCrossRefGoogle Scholar
  21. Dummer M, Michalski C, Essen LO, Rath M, Galland P, Forreiter C (2016) EHB1 and AGD12, two calcium-dependent proteins affect gravitropism antagonistically in Arabidopsis thaliana. J Plant Physiol 206:114–124PubMedCrossRefGoogle Scholar
  22. Fasano JM, Swanson SJ, Blancaflor EB, Dowd PE, Kao TH, Gilroy S (2001) Changes in root cap pH are required for the gravity response of the Arabidopsis root. Plant Cell 13:907–921PubMedPubMedCentralCrossRefGoogle Scholar
  23. Fisahn J, Yazdanbakhsh N, Klingele E, Barlow P (2012) Arabidopsis thaliana root growth kinetics and lunisolar tidal acceleration. New Phytol 195:346–355PubMedCrossRefGoogle Scholar
  24. Fisahn J, Klingele E, Barlow P (2015) Lunar gravity affects leaf movement of Arabidopsis thaliana in the international Space Station. Planta 241:1509–1518PubMedCrossRefGoogle Scholar
  25. Friml J, Wisniewska J, Benkova E, Mendgen K, Palme K (2002) Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415:806–809CrossRefPubMedGoogle Scholar
  26. 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
  27. Ganguly A, Cho H-T (2012) The phosphorylation code is implicated in cell type-specific trafficking of PIN-FORMEDs. Plant Signal Behav 7:1215–1218PubMedPubMedCentralCrossRefGoogle Scholar
  28. Grossmann G, Guo WJ, Ehrhardt DW, Frommer WB, Sit RV, Quake SR, Meier M (2011) The RootChip: an integrated microfluidic chip for plant science. Plant Cell 23:4234–4240PubMedPubMedCentralCrossRefGoogle Scholar
  29. Guan CH, 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 133:100–112PubMedPubMedCentralCrossRefGoogle Scholar
  30. Harper JE, Breton G, Harmon A (2004) Decoding Ca2+ signals through plant protein kinases. Annu Rev Plant Biol 55:263–288PubMedCrossRefGoogle Scholar
  31. Harrison BR, Masson PH (2008) ARL2, ARG1 and PIN3 define a gravity signal transduction pathway in root statocytes. Plant J 53:380–392PubMedPubMedCentralCrossRefGoogle Scholar
  32. Hayatsu M, Suzuki S (2015) Electron probe X-ray microanalysis studies on the distribution change of intra- and extracellular calcium in the elongation zone of horizontally reoriented soybean roots. Microscopy (Oxf) 64:327–334CrossRefGoogle Scholar
  33. He W, Brumos J, Li H, Ji Y, Ke M, Gong X, Zeng Q, Li W, Zhang X, An F, Wen X, Li P, Chu J, Sun X, Yan C, Yan N, Xie DY, Raikhel N, Yang Z, Stepanova AN, Alonso JM, Guo H (2011) A small-molecule screen identifies L-kynurenine as a competitive inhibitor of TAA1/TAR activity in ethylene-directed auxin biosynthesis and root growth in Arabidopsis. Plant Cell 23:3944–3960PubMedPubMedCentralCrossRefGoogle Scholar
  34. Hejnowicz Z, Sondag C, Alt W, Sievers A (1998) Temporal course of graviperception in intermittently stimulated cress roots. Plant Cell Environ 21:1293–1300PubMedCrossRefGoogle Scholar
  35. Herranz R, Medina FJ (2014) Cell proliferation and plant development under novel altered gravity environments. Plant Biol 16:23–30PubMedCrossRefGoogle Scholar
  36. Herranz R, Anken R, Boonstra J, Braun M, Christianen PCM, de Geest M, Hauslage J, Hilbig R, Hill JA, Lebert M, Medina J, Vagt N, Ullrich O, van JWA L, Hemmersbach R (2013a) Ground-based facilities for simulation of microgravity, including terminology and organism-specific recommendations for their use. Astrobiology 13.  https://doi.org/10.1089/ast.2012.0876PubMedPubMedCentralCrossRefGoogle Scholar
  37. Herranz R, Anken R, Boonstra J, Braun M, Christianen PCM, de Geest M, Hauslage J, Hilbig R, Hill RJA, Lebert M, Medina FJ, Vagt N, Ullrich O, van Loon JJWA, Hemmersbach R (2013b) Ground-based facilities for simulation of microgravity: organism-specific recommendations for their use, and recommended terminology. Astrobiology 13:1–17PubMedPubMedCentralCrossRefGoogle Scholar
  38. Hou G, Kramer VL, Wang YS, Chen R, Perbal G, Gilroy S, Blancaflor EB (2004) The promotion of gravitropism in Arabidopsis roots upon actin disruption is coupled with the extended alkalinization of the columella cytoplasm and a persistent lateral auxin gradient. Plant J 39:113–125CrossRefPubMedGoogle Scholar
  39. Joo JH, Bae YS, Lee JS (2001) Role of auxin-induced reactive oxygen species in root gravitropism. Plant Physiol 126:1055–1060PubMedPubMedCentralCrossRefGoogle Scholar
  40. Kircher S, Schopfer P (2016) Priming and positioning of lateral roots in Arabidopsis. An approach for an integrating concept. J Exp Bot 67:1411–1420PubMedCrossRefGoogle Scholar
  41. Kiss JZ, Wright JB, Caspar T (1996) Gravitropism in roots of intermediate-starch mutants of Arabidopsis. Physiol Plant 97:237–244PubMedCrossRefGoogle Scholar
  42. 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 U S A 107:22344–22349PubMedPubMedCentralCrossRefGoogle Scholar
  43. Krieger G, Shkolnik D (2016) Reactive oxygen species tune root tropic responses. Plant Physiol 172:1209–1220PubMedPubMedCentralGoogle Scholar
  44. Kuhn BM, Nodzynski T, Errafi S, Bucher R, Gupta S, Aryal B, Dobrev P, Bigler L, Geisler M, Zazimalova E, Friml J, Ringli C (2017) Flavonol-induced changes in PIN2 polarity and auxin transport in the Arabidopsis thaliana rol1-2 mutant require phosphatase activity. Sci Rep 7:41906PubMedPubMedCentralCrossRefGoogle Scholar
  45. Lewis DR, Negi S, Sukumar P, Muday GK (2011) Ethylene inhibits lateral root development, increases IAA transport and expression of PIN3 and PIN7 auxin efflux carriers. Development 138:3485–3495PubMedCrossRefGoogle Scholar
  46. Löfke C, Zwiewka M, Heilmann I, Van Montagu MCE, Teichmann T, Friml J (2013) Asymmetric gibberellin signaling regulates vacuolar trafficking of PIN auxin transporters during root gravitropism. Proc Natl Acad Sci U S A 110:3627–3632PubMedPubMedCentralCrossRefGoogle Scholar
  47. 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 130:1044–1056CrossRefPubMedGoogle Scholar
  48. Middleton AM, Dal Bosco C, Chlap P, Bensch R, Harz H, Ren F, Bergmann S, Wend S, Weber W, Hayashi KI, Zurbriggen MD, Uhl R, Ronneberger O, Palme K, Fleck C, Dovzhenko A (2018) Data-driven modeling of intracellular auxin fluxes indicates a dominant role of the ER in controlling nuclear auxin uptake. Cell Rep 22:3044–3057PubMedCrossRefGoogle Scholar
  49. Miller ND, Brooks TLD, Assadi AH, Spalding EP (2010) Detection of a Gravitropism phenotype in glutamate receptor-like 3.3 mutants of Arabidopsis thaliana using machine vision and computation. Genetics 186:585–U206PubMedPubMedCentralCrossRefGoogle Scholar
  50. Monshausen GB, Gilroy S (2009) The exploring root - root growth responses to local environmental conditions. Curr Opin Plant Biol 12:766–772PubMedCrossRefGoogle Scholar
  51. Monshausen GB, Miller ND, Murphy AS, Gilroy S (2011) Dynamics of auxin-dependent Ca2+ and pH signaling in root growth revealed by integrating high-resolution imaging with automated computer vision-based analysis. Plant J 65:309–318CrossRefPubMedGoogle Scholar
  52. Moreno-Risueno MA, Van Norman JM, Moreno A, Zhang J, Ahnert SE, Benfey PN (2010) Oscillating gene expression determines competence for periodic Arabidopsis root bBranching. Science 329:1306–1311PubMedPubMedCentralCrossRefGoogle Scholar
  53. Muday GK, Rahman A, Binder BM (2012) Auxin and ethylene: collaborators or competitors? Trends Plant Sci 17:181–195PubMedCrossRefGoogle Scholar
  54. Mullen JL, Wolverton C, Ishikawa H, Evans ML (2000) Kinetics of constant gravitropic stimulus responses in Arabidopsis roots using a feedback system. Plant Physiol 123:665–670PubMedPubMedCentralCrossRefGoogle Scholar
  55. 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. EMBO J 17:101–109PubMedPubMedCentralCrossRefGoogle Scholar
  56. Nagashima A, Uehara Y, Sakai T (2008) 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 49:1250–1255PubMedCrossRefGoogle Scholar
  57. Naramoto S, Kleine-Vehn J, Robert S, Fujimoto M, Dainobu T, Paciorek T, Ueda T, Nakano A, Van Montagu MCE, Fukuda H, Friml J (2010) ADP-ribosylation factor machinery mediates endocytosis in plant cells. Proc Natl Acad Sci U S A 107:21890–21895PubMedPubMedCentralCrossRefGoogle Scholar
  58. Negi S, Ivanchenko MG, Muday GK (2008) Ethylene regulates lateral root formation and auxin transport in Arabidopsis thaliana. Plant J 55:175–187PubMedPubMedCentralCrossRefGoogle Scholar
  59. Noll F (1900) Über den bestimmenden Einfluss von Wurzelkrümmungen auf Entstehung und Anordnung der Seitenwurze. Landwirtschaftliche Jahrbucher 29:361–426Google Scholar
  60. Ottenschlager I, Wolff P, Wolverton C, Bhalerao RP, Sandberg G, Ishikawa H, Evans M, Palme K (2003) Gravity-regulated differential auxin transport from columella to lateral root cap cells. Proc Natl Acad Sci U S A 100:2987–2991PubMedPubMedCentralCrossRefGoogle Scholar
  61. Paul A-L, Manak MS, Mayfield JD, Reyes MF, Gurley WB, Ferl RJ (2011) Parabolic flight iInduces changes in gene expression patterns in Arabidopsis thaliana. Astrobiology 11:743–758PubMedCrossRefGoogle Scholar
  62. Paul AL, Amalfitano CE, Ferl RJ (2012) Plant growth strategies are remodeled by spaceflight. BMC Plant Biol 12:232PubMedPubMedCentralCrossRefGoogle Scholar
  63. Perbal G, Driss-Ecole D (2003) Mechanotransduction in gravisensing cells. Trends Plant Sci 8:498–504PubMedCrossRefGoogle Scholar
  64. Perbal G, Driss-Ecole D, Tewinkel M, Volkmann D (1997) Statocyte polarity and gravisensitivity in seedling roots grown in microgravity. Planta 203:S57–S62PubMedCrossRefGoogle Scholar
  65. Perbal G, Jeune B, Lefranc A, Carnero-Diaz E, Driss-Ecole D (2002) The dose-response curve of the gravitropic reaction: a re-analysis. Physiol Plant 114:336–342PubMedCrossRefGoogle Scholar
  66. Philosoph-Hadas S, Friedman H, Meir S (2005) Gravitropic bending and plant hormones. Plant Horm 72:31–78CrossRefGoogle Scholar
  67. Ponce G, Corkidi G, Eapen D, Lledias F, Cardenas L, Cassab G (2017) Root hydrotropism and thigmotropism in Arabidopsis thaliana are differentially controlled by redox status. Plant Signal Behav 12:e1305536PubMedPubMedCentralCrossRefGoogle Scholar
  68. Provart NJ, Alonso J, Assmann SM, Bergmann D, Brady SM, Brkljacic J, Browse J, Chapple C, Colot V, Cutler S, Dangl J, Ehrhardt D, Friesner JD, Frommer WB, Grotewold E, Meyerowitz E, Nemhauser J, Nordborg M, Pikaard C, Shanklin J, Somerville C, Stitt M, Torii KU, Waese J, Wagner D, McCourt P (2016) 50 years of Arabidopsis research: highlights and future directions. New Phytol 209:921–944PubMedCrossRefGoogle Scholar
  69. Richter GL, Monshausen GB, Krol A, Gilroy S (2009) Mechanical Stimuli Modulate Lateral Root Organogenesis. Plant Physiol 151:1855–1866PubMedPubMedCentralCrossRefGoogle Scholar
  70. Rigo G, Ayaydin F, Tietz O, Zsigmond L, Kovacs H, Pay A, Salchert K, Darula Z, Medzihradszky KF, Szabados L, Palme K, Koncz C, Cseplo A (2013) Inactivation of plasma membrane-localized CDPK-RELATED KINASE5 decelerates PIN2 exocytosis and root gravitropic response in Arabidopsis. Plant Cell 25:1592–1608PubMedPubMedCentralCrossRefGoogle Scholar
  71. Roux SJ (2012) Root waving and skewing - unexpectedly in micro-g. BMC Plant Biol 12:231PubMedPubMedCentralCrossRefGoogle Scholar
  72. Roy R, Bassham DC (2014) Root growth movements: waving and skewing. Plant Sci 221:42–47PubMedCrossRefGoogle Scholar
  73. Roy R, Bassham DC (2017) TNO1, a TGN-localized SNARE-interacting protein, modulates root skewing in Arabidopsis thaliana. BMC Plant Biol 17:73PubMedPubMedCentralCrossRefGoogle Scholar
  74. Roy SJ, Gilliham M, Berger B, Essah PA, Cheffings C, Miller AJ, Davenport RJ, Liu LH, Skynner MJ, Davies JM, Richardson P, Leigh RA, Tester M (2008) Investigating glutamate receptor-like gene co-expression in Arabidopsis thaliana. Plant Cell Environ 31:861–871PubMedCrossRefGoogle Scholar
  75. Ruzicka K, Ljung K, Vanneste S, Podhorska R, Beeckman T, Friml J, Benkova E (2007) Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. Plant Cell 19:2197–2212PubMedPubMedCentralCrossRefGoogle Scholar
  76. Salmi ML, ul Haque A, Bushart TJ, Stout SC, Roux SJ, Porterfield DM (2011) Changes in gravity rapidly alter the magnitude and direction of a cellular calcium current. Planta 233:911–920PubMedCrossRefGoogle Scholar
  77. Santelia D, Henrichs S, Vincenzetti V, Sauer M, Bigler L, Klein M, Bailly A, Lee Y, Friml J, Geisler M, Martinoia E (2008) Flavonoids redirect PIN-mediated polar auxin fluxes during root gravitropic responses. J Biol Chem 283:31218–31226PubMedPubMedCentralCrossRefGoogle Scholar
  78. Sato EM, Hijazi H, Bennett MJ, Vissenberg K, Swarup R (2015) New insights into root gravitropic signalling. J Exp Bot 66:2155–2165PubMedCrossRefGoogle Scholar
  79. Schmidt T, Pasternak T, Liu K, Blein T, Aubry-Hivet D, Dovzhenko A, Duerr J, Teale W, Ditengou FA, Burkhardt H, Ronneberger O, Palme K (2014) The iRoCS toolbox - 3D analysis of the plant root apical meristem at cellular resolution. Plant J 77:806–814PubMedCrossRefGoogle Scholar
  80. Schultz ER, Zupanska AK, Sng NJ, Paul AL, Ferl RJ (2017) Skewing in Arabidopsis roots involves disparate environmental signaling pathways. BMC Plant Biol 17:31PubMedPubMedCentralCrossRefGoogle Scholar
  81. Scott AC, Allen NS (1999) Changes in cytosolic pH within Arabidopsis root columella cells play a key role in the early signaling pathway for root gravitropism. Plant Physiol 121:1291–1298PubMedPubMedCentralCrossRefGoogle Scholar
  82. Sedbrook JC, Chen R, Masson PH (1999) ARG1 (altered response to gravity) encodes a DnaJ-like protein that potentially interacts with the cytoskeleton. Proc Natl Acad Sci U S A 96:1140–1145PubMedPubMedCentralCrossRefGoogle Scholar
  83. Singh R, Singh S, Parihar P, Mishra RK, Tripathi DK, Singh VP, Chauhan DK, Prasad SM (2016) Reactive oxygen species (ROS): beneficial companions of plants’ developmental processes. Front Plant Sci 7:1299PubMedPubMedCentralGoogle Scholar
  84. Steinmann T, Geldner N, Grebe M, Mangold S, Jackson CL, Paris S, Galweiler L, Palme K, Jurgens G (1999) Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science 286:316–318PubMedCrossRefGoogle Scholar
  85. Stepanova AN, Alonso JM (2005) Arabidopsis ethylene signaling pathway. Sci STKE 2005:1–4Google Scholar
  86. Stepanova AN, Hoyt JM, Hamilton AA, Alonso JM (2005) A link between ethylene and auxin uncovered by the characterization of two root-specific ethylene-insensitive mutants in Arabidopsis. Plant Cell 17:2230–2242PubMedPubMedCentralCrossRefGoogle Scholar
  87. Stepanova AN, Yun J, Likhacheva AV, Alonso JM (2007) Multilevel interactions between ethylene and auxin in Arabidopsis roots. Plant Cell 19:2169–2185PubMedPubMedCentralCrossRefGoogle Scholar
  88. Stepanova AN, Robertson-Hoyt J, Yun J, Benavente LM, Xie DY, Dolezal K, Schlereth A, Jurgens G, Alonso JM (2008) TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133:177–191PubMedCrossRefGoogle Scholar
  89. Street IH, Mathews DE, Yamburkenko MV, Sorooshzadeh A, John RT, Swarup R, Bennett MJ, Kieber JJ, Schaller GE (2016) Cytokinin acts through the auxin influx carrier AUX1 to regulate cell elongation in the root. Development 143:3982–3993PubMedPubMedCentralCrossRefGoogle Scholar
  90. Tan TH, Silverberg JL, Floss DS, Harrison MJ, Henley CL, Cohen I (2015) How grow-and-switch gravitropism generates root coiling and root waving growth responses in Medicago truncatula. Proc Natl Acad Sci U S A 112:12938–12943PubMedPubMedCentralCrossRefGoogle Scholar
  91. Taylor LP, Grotewold E (2005) Flavonoids as developmental regulators. Curr Opin Plant Biol 8:317–323PubMedCrossRefGoogle Scholar
  92. Teale W, Palme K (2018) Naphthylphthalamic acid and the mechanism of polar auxin transport. J Exp Bot 69:303–312PubMedCrossRefGoogle Scholar
  93. Tsuchisaka A, Theologis A (2004) Unique and overlapping expression patterns among the Arabidopsis 1-amino-cyclopropane-1-carboxylate synthase gene family members. Plant Physiol 136:2982–3000PubMedPubMedCentralCrossRefGoogle Scholar
  94. Vandenbussche F, Petrasek J, Zadnikova P, Hoyerova K, Pesek B, Raz V, Swarup R, Bennett M, Zazimalova E, Benkova E, Van Der Straeten D (2010) The auxin influx carriers AUX1 and LAX3 are involved in auxin-ethylene interactions during apical hook development in Arabidopsis thaliana seedlings. Development 137:597–606PubMedCrossRefGoogle Scholar
  95. Vandenbussche F, Vaseva I, Vissenberg K, Van Der Straeten D (2012) Ethylene in vegetative development: a tale with a riddle. New Phytol 194:895–909PubMedCrossRefGoogle Scholar
  96. Weerasinghe RR, Swanson SJ, Okada SF, Garrett MB, Kim SY, Stacey G, Boucher RC, Gilroy S, Jones AM (2009) Touch induces ATP release in Arabidopsis roots that is modulated by the heterotrimeric G-protein complex. FEBS Lett 583:2521–2526PubMedPubMedCentralCrossRefGoogle Scholar
  97. Weller B, Zourelidou M, Frank L, Barbosa ICR, Fastner A, Richter S, Juergens G, Hammes UZ, Schwechheimer C (2017) Dynamic PIN-FORMED auxin efflux carrier phosphorylation at the plasma membrane controls auxin efflux-dependent growth. Proc Natl Acad Sci USA 114:E887–E896PubMedCrossRefGoogle Scholar
  98. Woeste KE, Ye C, Kieber JJ (1999) Two Arabidopsis mutants that overproduce ethylene are affected in the posttranscriptional regulation of 1-aminocyclopropane-1-carboxylic acid synthase. Plant Physiol 119:521–530PubMedPubMedCentralCrossRefGoogle Scholar
  99. Wolverton C, Mullen JL, Ishikawa H, Evans ML (2002) Root gravitropism in response to a signal originating outside of the cap. Planta 215:153–157PubMedCrossRefGoogle Scholar
  100. Wolverton C, Paya AM, Toska J (2011) Root cap angle and gravitropic response rate are uncoupled in the Arabidopsis pgm-1 mutant. Physiol Plant 141:373–382PubMedCrossRefGoogle Scholar
  101. Xuan W, Audenaert D, Parizot B, Moller BK, Njo MF, De Rybel B, De Rop G, Van Isterdael G, Mahonen AP, Vanneste S, Beeckman T (2015) Root cap-derived auxin pre-patterns the longitudinal axis of the Arabidopsis root. Curr Biol 25:1381–1388PubMedCrossRefGoogle Scholar
  102. Zajaczkowska U, Barlow PW (2017) The effect of lunisolar tidal acceleration on stem elongation growth, nutations and leaf movements in peppermint (Menthaxpiperita L.). Plant Biol 19:630–642PubMedCrossRefGoogle Scholar
  103. Zheng ZY, Zou JJ, Li HH, Xue S, Wang YR, Le J (2015) Microrheological insights into the dynamics of amyloplasts in root gravity-sensing cells. Mol Plant 8:660–663PubMedCrossRefGoogle Scholar
  104. Zourelidou M, Absmanner B, Weller B, Barbosa ICR, Willige BC, Fastner A, Streit V, Port S, Colcombet J, van Bentem SDLF, Hirt H, Kuster B, Schulze WX, Hammes UZ, Schwechheimer C (2014) Auxin efflux by PIN-FORMED proteins is activated by two different protein kinases, D6 PROTEIN KINASE and PINOID. elife 3Google Scholar

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© The Author(s), under exclusive licence to Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Klaus Palme
    • 1
  • William Teale
    • 2
  • Franck Ditengou
    • 2
  1. 1.Institute of Biology II, Molecular Plant Physiology, BIOSS Centre for Biological Signaling Studies, ZBSA Centre for Biosystems StudiesUniversity of FreiburgFreiburg im BreisgauGermany
  2. 2.Institute of Biology II, Molecular Plant PhysiologyUniversity of FreiburgFreiburg im BreisgauGermany

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