Molecular mechanisms of root gravity sensing and signal transduction

Wiley Interdisciplinary Reviews: Developmental Biology

Volumn 1, Issue 2, 2012, Pages 276-285

  Strohm, Allison K ^a   Baldwin, Katherine L ^a   Masson, Patrick H ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABSCISIC ACID; CALCIUM ION; PHOSPHOLIPASE C; SYNAPTOJANIN; TRANSLOCON;

AMYLOPLAST; ARTICLE; AUXIN TRANSPORT; GRAVITROPISM; GRAVITY SENSING; NONHUMAN; PLANT ROOT; PLANT ROOT CAP; ROOT GROWTH; ROOT LENGTH; SIGNAL TRANSDUCTION;

GRAVITY SENSING; INDOLEACETIC ACIDS; MECHANOTRANSDUCTION, CELLULAR; PLANT ROOTS; PLANTS;

EID: 84871945646     PISSN: 17597684     EISSN: 17597692     Source Type: Journal    
DOI: 10.1002/wdev.14     Document Type: Article

References (70)

1. Digby J, Firn RD. Light modulation of the gravitropic set-point angle (GSA). J Exp Bot 2002, 53:377-381.
2. Blancaflor EB, Fasano JM, Gilroy S. Mapping the functional roles of cap cells in the response of Arabidopsis primary roots to gravity. Plant Physiol 1998, 116:213-222.
3. Tsugeki R, Fedoroff NV. Genetic ablation of root cap cells in Arabidopsis. Proc Natl Acad Sci U S A 1999, 96:12941-12946.
4. Zheng HQ, Staehelin LA. Nodal endoplasmic reticulum, a specialized form of endoplasmic reticulum found in gravity-sensing root tip columella cells. Plant Physiol 2001, 125:252-265.
5. Collings DA, Zsuppan G, Allen NS, Blancaflor EB. Demonstration of prominent actin filaments in the root columella. Planta 2001, 212:392-403.
6. Leitz G, Kang BH, Schoenwaelder ME, Staehelin LA. Statolith sedimentation kinetics and force transduction to the cortical endoplasmic reticulum in gravity-sensing Arabidopsis columella cells. Plant Cell 2009, 21:843-860.
7. Stanga JP, Boonsirichai K, Sedbrook JC, Otegui MS, Masson PH. A role for the TOC complex in Arabidopsis root gravitropism. Plant Physiol 2009, 149: 1896-1905.
8. Kondrachuk AV, Hasenstein KH. The effects of HGMFs on the plant gravisensing system. Adv Space Res 2001, 27:1001-1005.
9. Kuznetsov OA, Hasenstein KH. Intracellular magnetophoresis of amyloplasts and induction of root curvature. Planta 1996, 198:87-94.
10. Caspar T, Pickard BG. Gravitropism in a starchless mutant of Arabidopsis: implications for the starch-statolith theory of gravity sensing. Planta 1989, 177: 185-197.
11. Kiss JZ, Hertel R, Sack FD. Amyloplasts are necessary for full gravitropic sensitivity in roots of Arabidopsis thaliana. Planta 1989, 177:198-206.
12. Ishikawa H, Evans ML. The role of the distal elongation zone in the response of maize roots to auxin and gravity. Plant Physiol 1993, 102:1203-1210.
13. Miller ND, Parks BM, Spalding EP. Computer-vision analysis of seedling responses to light and gravity. Plant J 2007, 52:374-381.
14. Trewavas AJ. What remains of the Cholodny-Went theory? Plan Cell Environ 1992, 15:759-794.
15. Friml J, Wisniewska J, Benkova E, Mendgen K, Palme K. Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 2002, 415:806-809.
16. Kleine-Vehn J, Ding Z, Jones AR, Tasaka M, Morita MT, Friml J. Gravity-induced PIN transcytosis for polarization of auxin fluxes in gravity-sensing root cells. Proc Natl Acad Sci U S A 2010, 107: 22344-22349.
17. Boonsirichai K, Sedbrook JC, Chen R, Gilroy S, Masson PH. Altered response to gravity is a peripheral membrane protein that modulates gravity-induced cytoplasmic alkalinization and lateral auxin transport in plant statocytes. Plant Cell 2003, 15:2612-2625.
18. Ottenschlager I, Wolff P, Wolverton C, Bhalerao RP, Sandberg G, Ishikawa H, Evans M, Palme K. Gravity-regulated differential auxin transport from columella to lateral root cap cells. Proc Natl Acad Sci U S A 2003, 100:2987-2991.
19. Rashotte AM, DeLong A, Muday GK. Genetic and chemical reductions in protein phosphatase activity alter auxin transport, gravity response, and lateral root growth. Plant Cell 2001, 13:1683-1697.
20. Mullen JL, Turk E, Johnson K, Wolverton C, Ishikawa H, Simmons C, Soll D, Evans ML. Root-growth behavior of the Arabidopsis mutant rgr1. Roles of gravitropism and circumnutation in the waving/coiling phenomenon. Plant Physiol 1998, 118: 1139-1145.
21. Barlow PW, Rathfelder EL. Distribution and redistribution of extension growth along vertical and horizontal gravireacting maize roots. Planta 1985, 165: 134-141.
22. Iversen TH. Geotropic curvatures in roots of cress (lepidium sativum). Physiol Plant 1973, 28:332-340.
23. Zieschang HE, Sievers A. Graviresponse and the localization of its initiating cells in roots of Phleum pratense L. Planta 1991, 184:468-477.
24. Wolverton C, Ishikawa H, Evans ML. The kinetics of root gravitropism: dual motors and sensors. J Plant Growth Regul 2002, 21:102-112.
25. Wolverton C, Paya AM, Toska J. Root cap angle and gravitropic response rate are uncoupled in the Arabidopsis pgm-1 mutant. Physiol Plant 2011, 141: 373-382.
26. Mancuso S, Barlow PW, Volkmann D, Baluska F. Actin turnover-mediated gravity response in maize root apices: gravitropism of decapped roots implicates gravisensing outside of the root cap. Plant Signal Behav 2006, 1:52-58.
27. Chavarria-Krauser A, Nagel KA, Palme K, Schurr U, Walter A, Scharr H. Spatio-temporal quantification of differential growth processes in root growth zones based on a novel combination of image sequence processing and refined concepts describing curvature production. New Phytol 2008, 177:811-821.
28. Morita MT. Directional gravity sensing in gravitropism. Annu Rev Plant Biol 2010, 61:705-720.
29. 2+ in Arabidopsis roots changes in response to touch but not gravity. Plant Physiol 1997, 114:789-800.
30. Perozo E, Kloda A, Cortes DM, Martinac B. Physical principles underlying the transduction of bilayer deformation forces during mechanosensitive channel gating. Nat Struct Biol 2002, 9:696-703.
31. Baluska F, Hasenstein KH. Root cytoskeleton: its role in perception of and response to gravity. Planta 1997, 203(suppl):S69-S78.
32. Sievers A, Buchen B, Volkmann D, Hejnowicz Z. Role of the cytoskeleton in gravity perception. In: Lloyd CW, ed. The Cytoskeletal Basis of Plant Growth and Form. London: Academic Press; 1991, 169-182.
33. Yoder TL, Zheng HQ, Todd P, Staehelin LA. Amyloplast sedimentation dynamics in maize columella cells support a new model for the gravity-sensing apparatus of roots. Plant Physiol 2001, 125:1045-1060.
34. Ma Z, Hasenstein KH. The onset of gravisensitivity in the embryonic root of flax. Plant Physiol 2006, 140: 159-166.
35. Hou G, Kramer VL, Wang YS, Chen R, Perbal G, Gilroy S, Blancaflor EB. 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 2004, 39:113-125.
36. Hou G, Mohamalawari DR, Blancaflor EB. Enhanced gravitropism of roots with a disrupted cap actin cytoskeleton. Plant Physiol 2003, 131:1360-1373.
37. Staves MP. Cytoplasmic streaming and gravity sensing in chara internodal cells. Planta 1997, 203(suppl 1):S79-S84.
38. Staves MP, Wayne R, Leopold AC. The effect of the external medium on the gravitropic curvature of rice (Oryza sativa, Poaceae) roots. Am J Bot 1997, 84: 1522-1529.
39. Braun M. Gravity perception requires statoliths settled on specific plasma membrane areas in Characean rhizoids and protonemata. Protoplasma 2002, 219: 150-159.
40. Limbach C, Hauslage J, Schafer C, Braun M. How to activate a plant gravireceptor. Early mechanisms of gravity sensing studied in Characean rhizoids during parabolic flights. Plant Physiol 2005, 139: 1030-1040.
41. Fasano JM, Massa GD, Gilroy S. Ionic signaling in plant responses to gravity and touch. J Plant Growth Regul 2002, 21:71-88.
42. Johannes E, Collings DA, Rink JC, Allen NS. Cytoplasmic pH dynamics in maize pulvinal cells induced by gravity vector changes. Plant Physiol 2001, 127: 119-130.
43. +-PPase AVP1 regulates auxin-mediated organ development. Science 2005, 310:121-125.
44. Scott AC, Allen NS. Changes in cytosolic pH within Arabidopsis root columella cells play a key role in the early signaling pathway for root gravitropism. Plant Physiol 1999, 121:1291-1298.
45. 2+ and pH signaling in root growth revealed by integrating high-resolution imaging with automated computer vision-based analysis. Plant J 2011, 65:309-318.
46. Monshausen GB, Sievers A. Basipetal propagation of gravity-induced surface pH changes along primary roots of Lepidium sativum L. Planta 2002, 215: 980-988.
47. Perera IY, Heilmann I, Boss WF. Transient and sustained increases in inositol 1, 4, 5-trisphosphate precede the differential growth response in gravistimulated maize pulvini. Proc Natl Acad Sci U S A 1999, 96:5838-5843.
48. Perera IY, Heilmann I, Chang SC, Boss WF, Kaufman PB. A role for inositol 1, 4, 5-trisphosphate in gravitropic signaling and the retention of cold-perceived gravistimulation of oat shoot pulvini. Plant Physiol 2001, 125:1499-1507.
49. Perera IY, Hung CY, Brady S, Muday GK, Boss WF. A universal role for inositol 1, 4, 5-trisphosphate-mediated signaling in plant gravitropism. Plant Physiol 2006, 140:746-760.
50. Andreeva Z, Barton D, Armour WJ, Li MY, Liao LF, McKellar HL, Pethybridge KA, Marc J. Inhibition of phospholipase C disrupts cytoskeletal organization and gravitropic growth in Arabidopsis roots. Planta 2010, 232:1263-1279.
51. Salinas-Mondragon RE, Kajla JD, Perera IY, Brown CS, Sederoff HW. Role of inositol 1, 4, 5-trisphosphate signalling in gravitropic and phototropic gene expression. Plant Cell Environ 2010, 33:2041-2055.
52. Plieth C, Trewavas AJ. Reorientation of seedlings in the earth's gravitational field induces cytosolic calcium transients. Plant Physiol 2002, 129:786-796.
53. Massa GD, Gilroy S. Touch modulates gravity sensing to regulate the growth of primary roots of Arabidopsis thaliana. Plant J 2003, 33:435-445.
54. Sedbrook JC, Chen R, Masson PH. ARG1 (ALTERED RESPONSE TO GRAVITY1) encodes a DnaJ-like protein that potentially interacts with the cytoskeleton. Proc Natl Acad Sci U S A 1999, 96:1140-1145.
55. Wang Y, Lin WH, Chen X, Xue HW. The role of Arabidopsis 5PTase13 in root gravitropism through modulation of vesicle trafficking. Cell Res 2009, 19: 1191-1204.
56. Sack FD. Plant gravity sensing. Int Rev Cytol 1991, 127:193-252.
57. Young LM, Evans ML, Hertel R. Correlations between gravitropic curvature and auxin movement across gravistimulated roots of Zea mays. Plant Physiol 1990, 92:792-796.
58. Petrasek J, Friml J. Auxin transport routes in plant development. Development 2009, 136:2675-2688.
59. Harrison BR, Masson PH. ARL2, ARG1 and PIN3 define a gravity signal transduction pathway in root statocytes. Plant J 2008, 53:380-392.
60. Krecek P, Skupa P, Libus J, Naramoto S, Tejos R, Friml J, Zazimalova E. The PIN-FORMED (PIN) protein family of auxin transporters. Genome Biol 2009, 10:249.1-249.11.
61. Abas L, Benjamins R, Malenica N, Paciorek T, Wisniewska J, Wirniewska J, Moulinier-Anzola JC, Sieberer T, Friml J, Luschnig C. Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat Cell Biol 2006, 8:249-256.
62. Takahashi H, Miyazawa Y, Fujii N. Hormonal interactions during root tropic growth: hydrotropism versus gravitropism. Plant Mol Biol 2009, 69:489-502.
63. Takahashi N, Yamazaki Y, Kobayashi A, Higashitani A, Takahashi H. Hydrotropism interacts with gravitropism by degrading amyloplasts in seedling roots of Arabidopsis and radish. Plant Physiol 2003, 132: 805-810.
64. Ponce G, Rasgado FA, Cassab GI. Roles of amyloplasts and water deficit in root tropisms. Plant Cell Environ 2008, 31:205-217.
65. Kaneyasu T, Kobayashi A, Nakayama M, Fujii N, Takahashi H, Miyazawa Y. Auxin response, but not its polar transport, plays a role in hydrotropism of Arabidopsis roots. J Exp Bot 2007, 58:1143-1150.
66. Takahashi N, Goto N, Okada K, Takahashi H. Hydrotropism in abscisic acid, wavy, and gravitropic mutants of Arabidopsis thaliana. Planta 2002, 216: 203-211.
67. Taniguchi YY, Taniguchi M, Tsuge T, Oka A, Aoyama T. Involvement of Arabidopsis thaliana phospholipase Dzeta2 in root hydrotropism through the suppression of root gravitropism. Planta 2010, 231: 491-497.
68. Boccalandro HE, De Simone SN, Bergmann-Honsberger A, Schepens I, Fankhauser C, Casal JJ. PHYTOCHROME KINASE SUBSTRATE1 regulates root phototropism and gravitropism. Plant Physiol 2008, 146:108-115.
69. Molas ML, Kiss JZ. Phototropism and gravitropism in plants. Adv Bot Res 2009, 49:1-34.
70. Gilroy S, Masson PH, eds. Plant Tropisms. Ames: Blackwell Publishing; 2008.