Molecular mechanisms of hydrotropism in seedling roots of Arabidopsis Thaliana (Brassicaceae)

American Journal of Botany

Volumn 100, Issue 1, 2013, Pages 25-34

  Moriwaki, Teppei ^a   Miyazawa, Yutaka ^b   Kobayashi, Akie ^a   Takahashi, Hideyuki ^a  

^a TOHOKU UNIVERSITY   (Japan)

^b YAMAGATA UNIVERSITY   (Japan)

Author keywords

Abscisic acid (ABA); Arabidopsis; Auxin; GNOM; Gravitropism; Hydrotropism; Light signaling; MIZ1; MIZ2; Vesicle trafficking

Indexed keywords

WATER;

ABSCISIC ACID; CYTOPLASM; DICOTYLEDON; GENE EXPRESSION; GENETIC ANALYSIS; GRAVITY FIELD; HORMONE; MOISTURE CONTENT; MOLECULAR ANALYSIS; MUTATION; PROTEIN; ROOT SYSTEM; SEEDLING; TAXIS;

ARABIDOPSIS; ARTICLE; BIOLOGICAL MODEL; GENETICS; PHYSIOLOGY; PLANT ROOT; SEEDLING; TROPISM;

ARABIDOPSIS; MODELS, BIOLOGICAL; PLANT ROOTS; SEEDLING; TROPISM; WATER;

ARABIDOPSIS; ARABIDOPSIS THALIANA; BRASSICACEAE;

EID: 84871989065     PISSN: 00029122     EISSN: None     Source Type: Journal    
DOI: 10.3732/ajb.1200419     Document Type: Article

References (65)

1. ALONI, R., E. ALONI, M. LANGHANS, and C. I. ULLRICH. 2006. Role of cytokinin and auxin in shaping root architecture: Regulating vascular differentiation, lateral root initiation, root apical dominance and root gravitropism. Annals of Botany 97: 883-893.
2. BENNETT, M. J., A. MARCHANT, H. G. GREEN, S. T. MAY, S. P. WARD, P. A. MILLNER, A. R. WALKER, B. SCHULZ, and K. A. FELDMANN. 1996. Arabidopsis AUX1 gene: A permease-like regulator of root gravitropism. Science 273: 948-950.
3. CORRELL, M. J., and J. Z. KISS. 2002. Interactions between gravitropism and phototropism in plants. Journal of Plant Growth Regulation 21: 89-101.
4. DING, Z., and J. FRIML. 2010. Auxin regulates distal stem cell differentiation in Arabidopsis roots. Proceedings of the National Academy of Sciences, USA 107: 12046-12051.
5. EAPEN, D., M. L. BARROSO, M. E. CAMPOS, G. PONCE, G. CORKIDI, J. G. DUBROVSKY, and G. I. CASSAB. 2003. A no hydrotropic response root mutant that responds positively to gravitropism in Arabidopsis. Plant Physiology 131: 536-546.
6. GALEN, C., J. J. RABENOLD, and E. LSCUM. 2007. Functional ecology of a blue light photoreceptor: Effects of phototropin-1 on root growth enhance drought tolerance in Arabidopsis thaliana. New Phytologist 173: 91-99.
7. GELDNER, N., N. ANDERS, H. WOLTERS, J. KEICHER, W. KORNBERGER, P. MULLER, A. DELBARRE, T. UEDA, A. NAKANO, and G. JÜRGENS. 2003.The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112: 219-230.
8. GELDNER, N., S. RICHTER, A. VIETEN, S. MARQUARDT, R. A. TORRES-RUIZ, U. MAYER, and G. JÜRGENS. 2004. Partial loss-of-function alleles reveal a role for GNOM in auxin transport-related, post-embryonic development of Arabidopsis. Development 131: 389-400.
9. HART, J. W. 1990. Plant tropism and growth movement. Unwin Hyman, London, UK.
10. IKEDA, Y., S. MEN, U. FISCHER, A. N. STEPANOVA, J. M. ALONSO, K. LJUNG, and M. GREBE. 2009. Local auxin biosynthesis modulates gradient-directed planar polarity in Arabidopsis. Nature Cell Biology 11: 731-738.
11. IWATA, S., Y. MIYAZAWA, and H. T AKAHASHI. 2012. MIZU-KUSSEI1 plays an essential role in the hydrotropism of lateral roots in Arabidopsis thaliana. Environmental and Experimental Botany 75: 167-172.
12. IYER-PASCUZZI, A. S., T. JACKSON, H. CUI, J. J. PETRICKA, W. BUSCH, H. TSUKAGOSHI, and P. N. BENFEY. 2011. Cell identity regulators link development and stress responses in the Arabidopsis root. Developmental Cell 21: 770-782.
13. JAFFE, M. J., H. TAKAHASHI, and R. L. BIRO. 1985. A pea mutant for the study of hydrotropism in roots. Science 230: 445-447.
14. JONES, B., S. A. GUNNERÅS, S. V. PETERSSON, P. TARKOWSKI, N. GRAHAN, S. MAY, K. DOLEZAL, G. SANDBERG, and K. LJUNG. 2010. Cytokinin regulation of auxin synthesis in Arabidopsis involves a homeostatic feedback loop regulated via auxin and cytokinin signal transduction. Plant Cell 22: 2956-2969.
15. KANEYASU, T., A. KOBAYASHI, M. NAKAYAMA, N. FUJII, H. TAKAHASHI, and Y. MIYAZAWA. 2007. Auxin response, but not its polar transport, plays a role in hydrotropism of Arabidopsis roots. Journal of Experimental Botany 58: 1143-1150.
16. KISS, J. Z. 2000. Mechanisms of the early phases of plant gravitropism. CRC Critical Review of Plant Science 19: 556-573.
17. KLEINE-VEHN, J., P. DHONUKSHE, M. SAUER, P. B. BREWER, J. WIŚNIEWSKA, T. PACIOREK, E. BENKOVÁ, and J. FRIML. 2008. ARF-GEF-dependent transcytosis and polar delivery of PIN auxin carriers in Arabidopsis. Current Biology 18: 526-531.
18. KOBAYASHI, A., A. TAKAHASHI, Y. KAKIMOTO, Y. MIYAZAWA, N. FUJII, A. HIGASHITANI, and H. TAKAHASHI. 2007. A gene essential for hydrotropism. Proceedings of the National Academy of Sciences, USA 104: 4724-4729.
19. LAXMI, A., J. PAN, M. MORSY, and R. CHEN. 2008. Light plays an essential role in ntracellular distribution of auxin efflux carrier PIN2 in Arabidopsis thaliana. Plos One 3: e1510.
20. LEOPOLD, A. C., and A. K. LAFAVRE. 1989. Interactions between red light, abscisic acid, and calcium in gravitropism. Plant Physiology 89: 875-878.
21. LEYSER, O., C. A. LINCOLN, C. TIMPTE, D. LAMMER, J. TURNER, and M. ESTELLE. 1993. Arabidopsis auxin-resistant gene AXR1 encodes a protein related to ubiquitin activating enzyme E1. Nature 364: 161-164.
22. LI, G., and H. W. XUE. 2007. Arabidopsis PLD ζ 2 regulates vesicle trafficking and is required for auxin response. Plant Cell 19: 281-295.
23. LIN, R., and H. WANG. 2005. Two homologous ATP-binding cassette transporter proteins, AtMDR1 and AtPGP1, regulate Arabidopsis photomorphogenesis and root development by mediating polar auxin transport. Plant Physiology 138: 949-964.
24. MANDOLI, D. F., G. A. FORD, L. J. WALDRON, J. A. NEMSON, and W. R. BRIGGS. 1990. Some spectral properties of several soil types: Implications for photomorphogenesis. Plant, Cell & Environment 13: 287-294.
25. MICHNIEWICZ, M., P. B. BREWER, and J. FRIML. 2007. Polar auxin transport and asymmetric auxin distribution. The Arabidopsis Book 5: e0108.
26. MIYAZAWA, Y., Y. ITO, T. MORIWAKI, A. KOBAYASHI, N. FUJII, and T. TAKAHASHI. 2009a. A molecular mechanism unique to hydrotropism in roots. Plant Science 177: 297-301.
27. MIYAZAWA, Y., T. MORIWAKI, M. UCHIDA, A. KOBAYASHI, N. FUJII, and H. TAKAHASHI. 2012. Overexpression of MIZU-KUSSEI1 enhances root hydrotropic response by retaining cell viability under hydrostimulated condition in Arabidopsis thaliana. Plant & Cell Physiology 53: 1926-1933.
28. MIYAZAWA, Y., T. SAKASHITA, T. FUNAYAMA, N. HAMADA, H. NEGISHI, A. KOBAYASHI, T. KANEYASU, et al. 2008. Effects of locally targeted heavy-ion and laser microbeam on root hydrotropism in Arabidopsis thaliana. Journal of Radiation Research 49: 373-379.
29. MIYAZAWA, Y., A. TAKAHASHI, A. KOBAYASHI, T. KANEYASU, N. FUJII, and H. TAKAHASHI. 2009b. GNOM-mediated vesicular trafficking plays an essential role in hydrotropism of Arabidopsis roots. Plant Physiology 149: 835-840.
30. MIYAZAWA, Y., T. YAMAZAKI, T. MORIWAKI, and T. TAKAHASHI. 2011. Root tropisms: Its mechanism and possible functions in drought avoidance. Advances in Botanical Research 57: 349-375.
31. MIZUNO, H., A. KOBAYASHI, N. FUJII, M. YAMASHITA, and H. TAKAHASHI. 2002. Hydrotropic response and expression pattern of auxin-inducible gene, CS-IAA1, in the primary roots of clinorotated cucumber seedlings. Plant & Cell Physiology 43: 793-801.
32. MONSHAUSEN, G. B., J. S. SARAH, and S. GILROY. 2008. Touch sensing and thigmotropism. In S. Gilroy and P. H. Masson [eds.], Plant tropisms, 91-122. Blackwell, Oxford, UK.
33. MORITA, M. T. 2010. Directional gravity sensing in gravitropism. Annual Review of Plant Biology 61: 705-720.
34. MORIWAKI, T., Y. MIYAZAWA, N. FUJII, and H. TAKAHASHI. 2012. Light and abscisic acid signalling are integrated by MIZ1 gene expression and regulate hydrotropic response in roots of Arabidopsis thaliana. Plant, Cell & Environment 35: 1359-1368.
35. MORIWAKI, T., Y. MIYAZAWA, A. KOBAYASHI, M. UCHIDA, C. WATANABE, N. FIJII, and H. TAKAHASHI. 2011. Hormonal regulation of lateral root development in Arabidopsis modulated by MIZ1 and requirement of GNOM activity for MIZ1 function. Plant Physiology 157: 1209-1220.
36. MORIWAKI, T., Y. MIYAZAWA, and H. TAKAHASHI. 2010. Transcriptome analysis of gene expression during the hydrotropic response in Arabidopsis seedlings. Environmental and Experimental Botany 69: 148-157.
37. MULLEN, J. L., and J. Z. KISS. 2008. Phototropism and its relationship to gravitropism. In S. Gilroy and P. H. Masson [eds.], Plant tropisms, 79-90. Blackwell, Oxford, UK.
38. MÜLLER, A., C. GUAN, L. GÄLWEILER, P. TÄNZLER, P. HUIJSER, A. MARCHANT, G. PARRY, M. BENNETT, E. WISMAN, and K. PALME. 1998. AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO Journal 17: 6903-6911.
39. MULLER, B., and J. SHEEN. 2008. Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis. Nature 453: 1094-1097.
40. NAGPAL, P., L. M. WALKER, J. C. YOUNG, A. SONAWALA, C. TIMPET, M. ESTELLE, and J. W. REED. 2000. AXR2 encodes a member of the Aux/ IAA protein family. Plant Physiology 123: 563-573.
41. NAKAYAMA, M., Y. KANEKO, Y. MIYAZAWA, N. FUJII, N. HIGASHITANI, S. WADA, H. ISHIDA, et al. 2012. A possible involvement of autophagy in amyloplast degradation in columella cells during hydrotropic response of Arabidopsis roots. Planta 236: 999-1012.
42. OONO, Y., C. O OURA, A. RAHMAN, E. T. ASPURIA, K. HAYASHI, A. TANAKA, and H. UCHIMIYA. 2003. p -Chlorophenoxyisobutyric acid impairs auxin response in Arabidopsis root. Plant Physiology 133: 1135-1147.
43. OYANAGI, A., H. T AKAHASHI, and H. SUGE. 1995. Interactions between hydrotropism and gravitropism in the primary seminal roots of Triticum aestivum L. Annals of Botany 75: 229-235.
44. PEDMALE, U. V., R. B. CELAYA, and E. LISCUM. 2010. Phototropism: Mechanism and outcomes. The Arabidopsis Book 8: e0125.
45. PERNISOVÁ, M., P. KLIMA, J. HORAK, M. VALKOVA, J. MALBECK, P. SOUCEK, P. REICHMAN, et al. 2009. Cytokinins modulate auxin-induced organogenesis in plants via regulation of the auxin efflux. Proceedings of the National Academy of Sciences, USA 106: 3609-3614.
46. PERRIN, R. M., L. S. YOUNG, U. M. N. MURTHY, B. R. HARRISON, Y. WANG, J. L. WILL, and P. H. MASSON. 2005. Gravity signal transduction in primary roots. Annals of Botany 96: 737-743.
47. PONCE, G., F. A. RASGADO, and G. I. CASSAB. 2008. Roles of amyloplasts and water deficit in root tropisms. Plant, Cell & Environment 31: 205-217.
48. Quiroz-Figueroa, F., A. RODRÍGUEZ-ACOSTA, A. Salazar-Blas, E. Hernández-Domínguez, M. E. CAMPOS, N. KITAHATA, T. ASAMI, R. M. GALAZ-AVALOS, and G. I. CASSAB. 2010. Accumulation of high levels of ABA regulates the pleiotropic response of the nhr1 Arabidopsis mutant. Journal of Plant Biology 53: 32-44.
49. REN, H., Z. GAO, L. CHEN, K. WEI, J. LIU, Y. FAN, W. J. DAVIES, W. JIA, and J. ZHANG. 2007. Dynamic analysis of ABA accumulation in relation to the rate of ABA catabolism in maize tissues under water deficit. Journal of Experimental Botany 58: 211-219.
50. SAUCEDO, M., G. PONCE, M. E. CAMPOS, D. EAPEN, E. G ARCÍA, R. LUJÁN, Y. SÁNCHEZ, and G. I. CASSAB. 2012. An altered hydrotropic response (ahr1) mutant of Arabidopsis recovers root hydrotropism with cytokinin. Journal of Experimental Botany 63: 3587-3602.
51. SHARP, R. E., and W. J. DAVIES. 1985. Root growth and water uptake by maize plants in drying soil. Journal of Experimental Botany 36: 1441-1456.
52. SHEVELL, D. E., W. M. LEU, C. S. GILLMOR, G. XIA, K. A. FELDMANN, and N. H. CHUA. 1994. EMB30 is essential for normal cell division, cell expansion, and cell adhesion in Arabidopsis and encodes a protein that has similarity to Sec7. Cell 77: 1051-1062.
53. STEINMANN, T., N. GELDNER, M. GREBE, S. MANGOLD, C. L. JACKSON, S. PARIS, L. GÄLWEILER, K. PALME, and G. JÜRGENS. 1999. Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF-GEF. Science 286: 316-318.
54. SUN, F., W. ZHANG, H. HU, B. LI, Y. WANG, Y. ZHAO, K. LI, M. LIU, and X. LI. 2008. Salt modulates gravity signaling pathway to regulate growth direction of primary roots in Arabidopsis. Plant Physiology 146: 178-188.
55. SUZUKI, T., and T. FUJII. 1978. Spectral dependence of the light-induced geotropic response in Zea roots. Planta 142: 275-279.
56. TAKAHASHI, H. 1997. Hydrotropism: The current state of our knowledge. Journal of Plant Research 110: 163-169.
57. TAKAHASHI, H., Y. MIYAZAWA, and N. FUJII. 2009. Hormonal interactions during root tropic growth: Hydrotropism versus gravitropism. Plant Molecular Biology 69: 489-502.
58. TAKAHASHI, H., and T. K. SCOTT. 1991. Hydrotropism and its interaction with gravitropism in maize roots. Plant Physiology 96: 558-564.
59. TAKAHASHI, H., and T. K. SCOTT. 1993. Intensity of hydrostimulation for the induction of root hydrotropism and its sensing by the root cap. Plant, Cell & Environment 16: 99-103.
60. TAKAHASHI, N., N. GOTO, K. OKADA, and H. TAKAHASHI. 2002. Hydrotropism in abscisic acid, wavy, and gravitropic mutants of Arabidopsis thaliana. Planta 216: 203-211.
61. TAKAHASHI, N., Y. YAMAZAKI, A. KOBAYASHI, A. HIGASHITANI, and H. TAKAHASHI. 2003. Hydrotropism interacts with gravitropism by degrading amyloplasts in seedling roots of Arabidopsis and radish. Plant Physiology 132: 805-810.
62. TANIGUCHI, Y. Y., M. TANIGUCHI, T. TSUGE, A. OKA, and T. AOYAMA. 2010. Involvement of Arabidopsis thaliana phospholipase D ζ 2 in root hydrotropism through the suppression of root gravitropism. Planta 231: 491-497.
63. THIMANN, K. V. 1938. Hormones and the analysis of growth. Plant Physiology 13: 437-449.
64. YAMAZAKI, T., Y. MIYAZAWA, A. KOBAYASHI, T. MORIWAKI, N. FUJII, and T. TAKAHASHI. 2012. MIZ1, an essential protein for root hydrotropism, is associated with the cytoplasmic face of the endoplasmic reticulum membrane in Arabidopsis root cells. FEBS Letters 586: 398-402.
65. ZHAO, Y., and K. H. HASENSTEIN. 2009. Primary root growth regulation: The role of auxin and ethylene antagonists. Journal of Plant Growth Regulation 28: 309-320.