Close relationships between polar auxin transport and graviresponse in plants

Plant Biology

Volumn 16, Issue SUPPL.1, 2014, Pages 43-49

  Ueda, J ^a   Miyamoto, K ^a   Uheda, E ^a   Oka, M ^b   Yano, S ^c   Higashibata, A ^c   Ishioka, N ^c  

^a Osaka Prefecture University   (Japan)

^b TOTTORI UNIVERSITY   (Japan)

^c JAPAN AEROSPACE EXPLORATION AGENCY   (Japan)

Author keywords

Automorphosis; Graviresponse; Indole 3 acetic acid; Polar auxin transport; PsAUX1; PsPINs; Space

Indexed keywords

ENVIRONMENTAL FACTOR; GRAVITY FIELD; HORMONE; LEGUME; MOLECULAR ANALYSIS; MORPHOGENESIS; PHYSIOLOGY; SEEDLING;

AGEOTROPUM; PISUM SATIVUM;

INDOLEACETIC ACID DERIVATIVE;

AUTOMORPHOSIS; GRAVIRESPONSE; GRAVITROPISM; INDOLE-3-ACETIC ACID; METABOLISM; MICROCLIMATE; PHYSIOLOGY; PLANT; PLANT DEVELOPMENT; POLAR AUXIN TRANSPORT; PSAUX1; PSPINS; REVIEW; SPACE; TRANSPORT AT THE CELLULAR LEVEL;

AUTOMORPHOSIS; GRAVIRESPONSE; INDOLE-3-ACETIC ACID; POLAR AUXIN TRANSPORT; PSAUX1; PSPINS; SPACE;

BIOLOGICAL TRANSPORT; EXTRATERRESTRIAL ENVIRONMENT; GRAVITROPISM; INDOLEACETIC ACIDS; PLANT DEVELOPMENT; PLANTS;

EID: 84890956587     PISSN: 14358603     EISSN: 14388677     Source Type: Journal    
DOI: 10.1111/plb.12101     Document Type: Review

References (88)

1. Antonsen F., Johnsson A. (1998) Effects of microgravity on the growth of Lepidium root. Journal of Gravitational Physiology, 5, 13-21.
2. Benjamins R., Quint A., Weijers D., Hooykaas P., Offringa R. (2001) The PINOID protein kinase regulates organ development in Arabidopsis by enhancing auxin polar transport. Development, 128, 4057-4067.
3. Benková E., Michniewicz M., Sauer M., Teichmann T., Seifertová D., Jürgens G., Friml J. (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell, 115, 591-602.
4. Beyer A. (1928) Beiträge zum Problem der Reizleitung. Zeitschrift für Botanik, 20, 321-417.
5. Blakeslee J.J., Peer W.A., Murphy A.S. (2005) Auxin transport. Current Opinion in Plant Biology, 8, 494-500.
6. Blilou I., Xu J., Wildwater M., Willemsen V., Paponov I., Friml J., Heidstra R., Aida M., Palme K., Scheres B. (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature, 433, 39-44.
7. Blixt S., Ehrenberg L., Gelin O. (1958) Quantitative studies of induced mutations in peas. I. Methodological investigation. Agricultural and Horticultural Genetics, 16, 238-250.
8. Boysen-Jensen P., Nielsen N. (1925) Studien tüber die hormonalen Beziehungen zwischen Spitze und Basis der Avena coleoptile. Planta, 1, 321-331.
9. Brown D.E., Rashotte A.M., Murphy A.S., Normanly J., Tague B.W., Peer W.A., Taiz L., Muday G.K. (2001) Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis. Plant Physiology, 126, 524-535.
10. Chawla R., DeMason D.A. (2003) PsPIN1, putative auxin efflux protein. AY222857, DDBJ/EMBL/GenBank databases.
11. Chen R., Masson P.H. (2005) Auxin transport and recycling of PIN proteins in plants. Šamaja J., Balška F., Menzel D. (Eds), Plant endocytosis. Springer, Berlin, Germany, pp 139-157.
12. Dal Bosco C., Dovzhenko A., Palme K. (2012) Intracellular auxin transport in pollen: PIN8, PIN 5 and PILS5. Plant Signaling & Behavior, 7, 1504-1505.
13. Ding J.P., Pickard B.G. (1993) Mechanosensory calcium-selective cation channels in epidermal cells. The Plant Journal, 3, 83-110.
14. Driss-Ecole D., Legu V., Carnero-Diaz E., Perbal G. (2008) Gravisensitivity and automorphogenesis of lentil seedling roots grown on board the International Space Station. Physiologia Plantarum, 134, 191-201.
15. Friml J. (2010) Subcellular trafficking of PIN auxin efflux carriers in auxin transport. European Journal of Cell Biology, 89, 231-235.
16. Friml J., Wisniewska J., Benková E., Mendger K., Palme K. (2002) Lateral relocation of auxin efflux regulator AtPIN3 mediates tropism in Arabidopsis. Nature, 415, 806-809.
17. Friml J., Yang X., Michniewicz M., Weijers D., Quint A., Tietz O., Benjamins R., Ouwerkerk P.B.F., Ljung K., Sandberg G., Hooykaas P.J.J., Palme K., Offringa R. (2004) A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science, 306, 862-865.
18. 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, 2226-2230.
19. Geisler M., Murphy A.S. (2006) The ABC of auxin transport: the role of p-glycoproteins in plant development. FEBS Letters, 580, 1094-1102.
20. Geisler M., Blakeslee J.J., Bouchard R., Lee O.R., Vincenzetti V., Bandyopadhyay A., Titapiwatanakun B., Peer W.A., Bailly A., Richards E.L., Ejendal K.F.K., Smith A.P., Baroux C., Grossniklaus U., Müller A., Hrycyna C.A., Dudler R., Murphy A.S., Martinoia E. (2005) Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1. The Plant Journal, 44, 179-194.
21. Geldner N., Richter S., Vieten A., Marquardt S., Torres-Ruiz R.A., Mayer Ü., Jürgens G. (2004) Partial loss-of-function alleles reveal a role for GNOM in auxin transport-related, post-embryonic development of Arabidopsis. Development, 131, 389-400.
22. Goeschl J.D., Pratt H.K., Bonner B.A. (1967) An effect of light on the production of ethylene and the growth of the plumular portion of etiolated pea seedlings. Plant Physiology, 42, 1077-1080.
23. Grunewald W., Friml J. (2010) The march of the PINs: developmental plasticity by dynamic polar targeting in plant cells. The EMBO Journal, 29, 2700-2714.
24. Guzman P., Ecker J.A. (1990) Exploiting the response to identify ethylene-related mutants. The Plant Cell, 2, 513-523.
25. Halstead T.W., Dutcher F.R. (1987) Plants in space. Annual Review of Plant Physiology, 38, 317-345.
26. Holweg C., Nick P. (2004) Arabidopsis myosin XI mutant is defective in organelle movement and polar auxin transport. Proceedings of the National Academy of Sciences USA, 101, 10488-10493.
27. Hoshino T., Hitotsubashi R., Miyamoto K., Tanimoto E., Ueda J. (2005) Isolation of PsPIN2 and PsAUX1 from etiolated pea epicotyls and their expression on a three-dimensional clinostat. Advances in Space Research, 36, 1284-1291.
28. Hoshino T., Miyamoto K., Ueda J. (2006) Requirement of the gravity-controlled transport of auxin for a negative gravitropic response in early growth stage of etiolated pea epicotyls. Plant and Cell Physiology, 47, 1496-1508.
29. Hoshino T., Miyamoto K., Ueda J. (2007) Gravity-controlled asymmetrical transport of auxin regulates a gravitropic response in the early growth stage of etiolated pea (Pisum sativum) epicotyls: studies using simulated microgravity conditions on a three-dimensional clinostat and using an agravitropic mutant, ageotropum. Journal of Plant Research, 120, 619-628.
30. Hoson T., Soga K. (2003) New aspects of gravity responses in plant cells. International Review of Cytology, 229, 209-244.
31. Hoson T., Kamisaka S., Masuda Y., Yamashita M. (1992) Changes in plant growth processes under microgravity conditions simulated by a three-dimensional clinostat. The Botanical Magazine, Tokyo, 105, 53-70.
32. Hoson T., Kamisaka S., Yamamoto R., Yamashita M., Masuda Y. (1995) Automorphosis of maize shoots under simulated microgravity on a three-dimensional clinostat. Physiologia Plantarum, 93, 346-351.
33. Hoson T., Kamisaka S., Buchen B., Sievers A., Yamashita M., Masuda Y. (1996) Possible use of a 3-dimensional clinostat to analyze plant growth processes under microgravity conditions. Advances in Space Research, 17, 47-53.
34. Hoson T., Kamisaka S., Masuda Y., Yamashita M., Buchen B. (1997) Evaluation of the three-dimensional clinostat as a simulator of weightlessness. Planta, 203, S187-S197.
35. Hoson T., Soga K., Mori R., Saiki M., Wakabayashi K., Kamisaka S., Kamigaichi S., Aizawa S., Yoshizaki I., Mukai C., Shimazu T., Fukui K., Yamashita M. (1999) Morphogenesis of rice and Arabidopsis seedlings in space. Journal of Plant Research, 112, 477-486.
36. Johnsson A. (1997) Circumnutations: results from recent experiments on earth and in space. Planta, 203, S147-S158.
37. Kang B.G., Yocum C.S., Burg S.P., Ray P.M. (1967) Ethylene and carbon dioxide: mediation of hook opening response. Science, 156, 958-959.
38. Kiss J.Z. (2000) Mechanisms of the early phases of plant gravitropism. Critical Reviews in Plant Sciences, 19, 551-573.
39. Kraft T.F.B., Loon J.J.W.A., Kiss J.Z. (2000) Plastid position in Arabidopsis columella cells is similar in microgravity and on a random-positioning machine. Planta, 211, 415-422.
40. Legu V., Yu F., Driss-Ecole D., Perbal G. (1996) Effects of gravitropic stress on the development of the primary root of lentil seedlings grown in space. Journal of Biotechnology, 47, 129-135.
41. Lehman A., Black R., Ecker J.R. (1996) Hookless1, an ethylene response gene, is required for differential cell elongation in the Arabidopsis hypocotyl. Cell, 85, 183-194.
42. Luschnig C., Gaxiola R.A., Grisafi P., Fink G.R. (1998) EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes and Development, 12, 2175-2187.
43. Marchant A., Kargul J., May S.T., Muller P., Delbarre A., Perrot-Rechenmann C., Bennett M.J. (1999) AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues. The EMBO Journal, 18, 2066-2073.
44. Miyamoto K., Hoshino T., Hitotsubashi R., Yamashita M., Ueda J. (2005a) Automorphosis-like growth in etiolated pea seedlings is induced by the application of chemicals affecting perception of gravistimulation and its signal transduction. Advances in Space Research, 36, 1263-1268.
45. Miyamoto K., Hoshino T., Yamashita M., Ueda J. (2005b) Automorphosis of etiolated pea seedlings in space is simulated by a three-dimensional clinostat and the application of inhibitors of auxin polar transport. Physiologia Plantarum, 123, 467-474.
46. Miyamoto K., Hoshino T., Takahashi Y., Ueda J. (2007) Auxin polar transport of etiolated ageotropum pea epicotyls is not affected by gravistimulation: relevance to automorphosis-like growth and development. Advances in Space Research, 39, 1140-1146.
47. Miyamoto K., Ueda E., Oka M., Ueda J. (2011) Auxin polar transport and automorphosis in plants. Biological Sciences in Space, 25, 57-68.
48. Morita M.T. (2010) Directional gravity sensing in gravitropism. Annual Review of Plant Biology, 61, 705-720.
49. Mravec J., Kubeš M., Bielach A., Gaykova V., Petrášek J., Skůpa P., Chand S., Benková E., Zažímalová E., Friml J. (2008) Interaction of PIN and PGP transport mechanisms in auxin distribution-dependent development. Development, 135, 3345-3354.
50. Mravec J., Skůpa P., Bally A., Hoyerova K., Krěcěk P., Bielach A., Petrášek J., Zhang J., Gaykova V., Stierhof Y.-D., Schwarzerová K., Rolčik J., Dobrev P., Seifertová D., Luschnig C., Benková E., Zažimalová E., Geisler M., Friml J. (2009) ER-localized PIN5 auxin transporter mediates subcellular homeostasis of phytohormone auxin. Nature, 439, 1136-1140.
51. Noh B., Angus S., Murphy A.S., Spalding E.P. (2001) Multidrug Resistance-like genes of Arabidopsis required for auxin transport and auxin-mediated development. The Plant Cell, 13, 2441-2454.
52. 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, 999-1002.
53. Okada K., Ueda J., Komaki M.K., Bell C.J., Shimura Y. (1991) Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. The Plant Cell, 3, 677-684.
54. Olsen G.M., Iversen T.-H. (1980a) Growth and curvature in seedlings of Pisum sativum and an ageotropic mutant. Physiologia Plantarum, 50, 269-274.
55. Olsen G.M., Iversen T.-H. (1980b) Ultrastructure and movements of cell structures in normal and an ageotropic mutant. Physiologia Plantarum, 50, 275-284.
56. Petrášek J., Mravec J., Bouchard R., Blakeslee J., Abas M., Seifertová D., Wiśniewska J., Tadele Z., Čovanová M., Dhonukshe P., Skúpa P., Benková E., Perry L., Křeček P., Lee O.R., Fink G., Geisler M., Murphy A., Luschung C., Zažímalová E., Friml J. (2006) PIN proteins perform a rate-limiting function in cellular auxin efflux. Science, 312, 914-918.
57. Pfeffer W. (1904) Pflanzenphysiologie, 2nd edition. W. Engelmann, Leipzig, Germany.
58. Platonova R.N., Parfenov G.P., Zhvalikovskaya V.P. (1979) Orientation of plants in weightlessness. Ilyin, Ye. A ., Parfenov, G.P. (Eds), Biological Studies on the Kosmos Biosatellites [Translation of Biologicheskiye Issledovaniya na Biosputnikakh "Kosmos"]. NASA, TM-75769, Washington, D.C., pp 153-165.
59. Platonova R.N., Lyubchenko V.Y., Devyatko A.V., Malysheve G.I., Tairbekov M.G. (1980) Orientation of tomato seedlings grown in weightlessness (investigation on satellite "Cosmos-1129"). Izvestiia Akademii nauk. Seriia Biologicheskaia/Rossiǐskaia Akademiia Nauk, 6, 891-896.
60. Rakusová H., Gallego-Bartolom J., Vanstraelen M., Robert H.S., Alabadi D., Blázquez M.A., Benková E., Friml J. (2011) Polarization of PIN3-dependent auxin transport for hypocotyl gravitropic response in Arabidopsis thaliana. The Plant Journal, 67, 817-826.
61. Rashotte A.M., Brady S., Reed R., Ante S., Muday G.K. (2000) Basipetal auxin transport is required for gravitropism in roots of Arabidopsis. Plant Physiology, 122, 481-490.
62. Roman G., Lubarski B., Kieber J.J., Rothenberg M., Ecker J.R. (1995) Genetic analysis of ethylene signal transduction in Arabidopsis thaliana: five novel mutant loci integrated into a stress response pathway. Genetics, 139, 1393-1409.
63. Sack F.D. (1997) Plastids and gravitropic sensing. Planta, 203, S63-S68.
64. Santelia D., Vincenzetti V., Azzarello E., Bovet L., Fukao Y., Duchtig P., Mancuso S., Martinoia E., Geisler M. (2005) MDR-like ABC transporter AtPGP4 is involved in auxin -mediated lateral root and root hair development. FEBS Letters, 579, 5399-5406.
65. 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. Journal of Biological Chemistry, 283, 31218-31226.
66. Schöldéen C., Burström H. (1960) Physiological studies of an ageotropic pea mutant. Physiologia Plantarum, 13, 831-838.
67. Schulze A., Jensen P.J., Desrosiers M., Buta J.G., Bandurski R.S. (1992) Studies on the growth and indole-3-acetic acid and abscisic acid content of Zea mays seedlings grown in microgravity. Plant Physiology, 100, 692-698.
68. Shimazu T., Yuda T., Miyamoto K., Yamashita M., Ueda J. (2001) Growth and development in higher plants under simulated microgravity conditions on a 3-dimensional clinostat. Advances in Space Research, 27, 995-1000.
69. Sievers A., Buchen B., Volkmann D., Hejinowicz Z. (1991) Role of the cytoskeleton in gravity perception. Lloyd C.W. (Ed.), The cytoskeletal basis of plant growth and form. Academic Press, London, UK, pp 169-182.
70. Soga K. (2010) Gravity resistance in plants. Biological Sciences in Space, 24, 129-134.
71. Stanković B., Volkmann D., Sack F.D. (1998) Autotropism, automorphogenesis, and gravity. Physiologia Plantarum, 102, 328-335.
72. Sukumar P., Edwards K.S., Rahman A., DeLong A., Muday G.K. (2009) PINOID kinase regulates root gravitropism through modulation of PIN2-dependent basipetal auxin transport in Arabidopsis. Plant Physiology, 150, 722-735.
73. Swarup R., Friml J., Marchant A., Ljung K., Sandberg G., Palme K., Bennett M. (2001) Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. Genes & Development, 15, 2648-2653.
74. Takahashi H., Suge H. (1991) Root hydrotropism of an agravitropic pea mutant, ageotropum. Physiologia Plantarum, 82, 24-31.
75. Takahashi H., Suge H., Jaffe M.J. (1991) Agravitropic growth and its relation to the formation of the plumular hook in etiolated shoots of the pea mutant, ageotropum. Journal of Plant Physiology, 138, 212-216.
76. 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, 515-518.
77. Tsuda E., Yang H., Nishimura T., Uehara Y., Sakai T., Furutani M., Koshiba T., Hirose M., Nozaki H., Murphy A.S., Hayashi K. (2011) Alkoxy-auxins are selective inhibitors of auxin transport mediated by PIN, ABCB, and AUX1 transporters. Journal of Biological Chemistry, 286, 2354-2364.
78. Ueda J., Miyamoto K., Yuda T., Hoshino T., Fujii S., Mukai C., Kamigaichi S., Aizawa S., Yoshizaki I., Shimazu T., Fukui K. (1999) Growth and development, and auxin polar transport in higher plants under microgravity conditions in space: BRIC-AUX on STS-95 space experiment. Journal of Plant Research, 112, 487-492.
79. Ueda J., Miyamoto K., Yuda T., Hoshino T., Sato K., Fujii S., Kamigaichi S., Izumi R., Ishioka N., Aizawa S., Yoshizaki I., Shimazu T., Fukui K. (2000) STS-95 space experiment for growth and development, and auxin polar transport. Biological Sciences in Space, 14, 47-57.
80. Ueda J., Miyamoto K., Uheda E., Oka M. (2011) Auxin transport and a graviresponse in plants: relevance to ABC proteins. Biological Sciences in Space, 25, 69-75.
81. Ueda J., Tada T., Hoshino T., Miyamoto K., Uheda E., Oka M. (2012) Isolation of PsPINs and PsAUX1 cDNAs encoding putative auxin efflux and influx carriers and/or facilitators, respectively, from etiolated epicotyls of an agravitropic pea (Pisum sativum L.) mutant, ageotropum. Biological Sciences in Space, 26, 32-41.
82. van der Weij H.G. (1932) Der Mechanisms des Wuchsstofftranportes. Thimann K.V. (1977) Hormone action in the whole life of plants. University of Massachusetts Press, Amherst, MA, USA, pp 71-92.
83. van der Weij H.G. (1934) Der Mechanisms des Wuchsstofftranportes. Thimann K.V. (1977) Hormone action in the whole life of plants. The University of Massachusetts Press, Amherst, MA, USA, pp 71-92.
84. Volkmann D., Behrens H.M., Sievers A. (1986) Development and gravity sensing of cress roots under microgravity. Naturwissenschaften, 73, 438-441.
85. Wayne R., Staves M.P.A. (1997) A down-to earth model of gravisensing. Gravitational and Space Biology Bulletin, 10, 57-61.
86. Wendy A.P., Murphy A.S. (2007) Flavonoids and auxin transport: modulators or regulators? Trends in Plant Sciences, 12, 556-563.
87. Wu G., Lewis D.R., Spaldin E.P. (2007) Mutation in Arabidopsis multidrug resistance-like ABC transporters separates the roles of acropetal and basipetal auxin transport in lateral root development. The Plant Cell, 19, 1826-1837.
88. Wu G., Cameron J., Ljung K., Spalding E.P. (2010) A role for ABCB19-mediated polar auxin transport in seedling photomorphogenesis mediated by cryptochrome 1 and pytochrome B. The Plant Journal, 62, 179-191.