Joining forces: The interface of gravitropism and plastid protein import

Plant Signaling and Behavior

Volumn 4, Issue 10, 2009, Pages 933-941

  Stanga, John ^a   Baldwin, Katherine ^a   Masson, Patrick H ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Amyloplast; Gravitropism; Root; TOC complex; TOC132; TOC75

Indexed keywords

BIOLOGICAL MODEL; GENETICS; GRAVITROPISM; GRAVITY SENSING; PHYSIOLOGY; PLANT; PLANT GENE; PLANT PHYSIOLOGY; PLANT ROOT; PLASTID; REVIEW; SIGNAL TRANSDUCTION;

GENES, PLANT; GRAVITROPISM; GRAVITY SENSING; MODELS, BIOLOGICAL; PLANT PHYSIOLOGICAL PROCESSES; PLANT ROOTS; PLANT SHOOTS; PLASTIDS; SIGNAL TRANSDUCTION;

COLUMELLA; MAGNOLIOPHYTA;

EID: 70450189577     PISSN: 15592316     EISSN: 15592324     Source Type: Journal    
DOI: 10.4161/psb.4.10.9470     Document Type: Review

References (98)

1. Perrin R, et al. Gravity signal transduction in primary roots. Ann Bot 2005; 96:737-43.
2. Harrison B, et al. Signal transduction in gravitropism. In: Plant Tropisms. Gilroy S, Masson P, (eds.,) Blackwell Publishing 2008; 2:21-45.
3. Boonsirichai K, et al. Root gravitropism: An experimental tool to investigate basic cellular and molecular processes underlying mechanosensing and signal transmission in plants. Ann Rev Plant Biol 2002; 53:421-47.
4. Trewavas A. What remains of the Cholodny-Went theory? Plant Cell Environ 1992; 15:759-94.
5. Went F. Wuchstoff und Wachstum. Rec Trav Bot Neerl 1928; 25:1-116.
6. Cholodny H. Beiträge zur hormonalen theorie von tropismen. Planta 1928; 6:118-34.
7. Muday G, Rahman A. Auxin transport and the integration of gravitropic growth. In Plant Tropisms. Gilroy S, Masson P, (eds.,) Blakwell Publishing 2008; 3:47-78.
8. Rashotte A, et al. Basipetal auxin transport is required for gravitropism in roots of Arabidopsis. Plant Physiol 2000; 122:481-90.
9. Boonsirichai K, et al. ARG1 is a peripheral membrane protein that modulates gravity-induced cytoplasmic alkalinization and lateral auxin transport in plant statocytes. Plant Cell 2003; 15:2612-25.
10. Ottenschlager I, et al. Gravity-regulated differential auxin transport from columella to lateral root cap cells. Proc Natl Acad Sci USA 2003; 100:2987-91.
11. Lewis D, et al. Separating the roles of acropetal and basipetal auxin transport on gravitropism with mutations in two Arabidopsis multidrug resistance-like ABC transporter genes. Plant Cell 2007; 19:1838-50.
12. Harrison B, Masson P. ARL2, ARG1 and PIN3 define a gravity signal transduction pathway in root statocytes. Plant J 2008; 53:380-92.
13. Friml J, et al. Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 2005; 415:806-9.
14. Paciorek T, et al. Auxin inhibits endocytosis and promotes its own efflux from cells. Nature 2005; 435:1251-6.
15. Aloni R, et al. Role of cytokinin in the regulation of root gravitropism. Planta 2004; 220:177-82.
16. Sack F. Plastids and gravitropic sensing. Planta 1997; 203:63-8.
17. Tsugeki R, Fedoroff N. Genetic ablation of root cap cells in Arabidopsis. Proc Natl Acad Sci USA 1999; 96:12941-6.
18. Tanaka A, et al. Positional effect of cell inactivation on root gravitropism using heavy-ion microbeams. J Exp Bot 2002; 53:683-7.
19. Blancaflor E, et al. Mapping the functional roles of cap cells in the response of Arabidopsis primary roots to gravity. Plant Physiol 1998; 116:213-22.
20. Kuznetsov O, Hasenstein K. Intracellular magnetophoresis of amyloplasts and induction of root curvature. Planta 1996; 198:87-94.
21. Ma Z, Hasenstein K. The onset of gravisensitivity in the embryonic root of flax. Plant Physiol 2006; 140:159-66.
22. Vitha S, et al. Gravitropism in starch-excess mutant of Arabidopsis thaliana. Am J Bot 2007; 94:590-8.
23. Kato T, et al. SGR2, a phospholipase-like protein, and ZIG/SGR4, a SNARE, are involved in the shoot gravitropism of Arabidopsis. Plant Cell 2002; 14:33-46.
24. Yano D, et al. A SNARE complex containing SGR3/ AtVAM3 and ZIG/VTI11 in gravity-sensing cells is important for Arabidopsis shoot gravitropism. Proc Natl Acad Sci USA 2003; 100:8589-94.
25. Morita M, et al. Inovolvement of the vacuoles of the endodermis in the early process of shoot gravitropism in Arabidopsis. Plant Cell 2002; 14:47-56.
26. Tasaka M, et al. Genetic regulation of gravitropism in higher plants. Int Rev Cytol 2001; 206:135-54.
27. Silady R, et al. The GRV2/RME-8 protein of Arabidopsis functions in the late endocytic pathway and is required for vacuolar membrane flow. Plant J 2007; 53:29-41.
28. Wolverton C, et al. Root gravitropism in response to a signal originating outside of the cap. Planta 2002; 215:153-7.
29. Staves M, et al. Hydrostatic pressure mimics gravitational pressure in characean cells. Protoplasma 1992; 168:141-52.
30. Staves M, et al. The effect of external medium on the gravitropic curvature of rice (Oryza sativa, Poaceae) roots. Am J Bot 1997; 84:1522-9.
31. Mancuso S, et al. Actin turnover-mediated gravity response in maize root apices. Gravitropism of decapped roots implicates gravisensing outside of the root cap. Plant Signal Behav 2006; 1:52-8.
32. Miller N, et al. Computer-vision analysis of seedling responses to light and gravity. Plant J 2007; 52:374-81.
33. Caspar T, Pickard B. Gravitropism in a starchless mutant of Arabidopsis: implications for the starchstatolith theory of gravity sensing. Planta 1989; 177:185-97.
34. Kiss J, et al. Amyloplasts are necessary for full gravitropic sensitivity in roots of Arabidopsis thaliana. Planta 1989; 177:198-206.
35. Sinclair W, Trewavas A. Calcium in gravitropism: A re-examination. Planta 1997; 203:85-90.
36. Fasano J, et al. Ionic signaling in plant responses to gravity and touch. J Plant Growth Reg 2002; 21:71-88.
37. Monshausen G, et al. Touch sensing and thigmotropism. In Plant Tropisms. Gilroy S, Masson P, (eds.,) Blackwell Publishing 2008; 5:91-122.
38. Plieth C, Trewavas A. Reorientation of seedlings in the Earth's gravitational field induces cytosolic calcium transients. Plant Physiol 2002; 129:786-96.
39. Toyota M, et al. Cytoplasmic calcium increases in response to changes in the gravity vector in hypocotyls and petioles of Arabidopsis seedlings. Plant Physiol 2008; 146:505-14.
40. Toyota M, et al. Critical consideration on the relationship between auxin transport and calcium transients in gravity perception of Arabidopsis seedlings. Plant Signal Behav 2009; 3:521-4.
41. Haswell E, Meyerowitz E. MscS-like proteins control plastid size and shape in Arabidopsis thaliana. Curr Biol 2006; 16:1-11.
42. Haswell E, et al. Two MscS homologs provide mechanosensitive channel activities in the Arabidopsis root. Curr Biol 2008; 18:730-4.
43. Nakagawa Y, et al. Arabidopsis plasma membrane protein crucial for Ca2+ influx and touch sensing in roots. Proc Natl Acad Sci USA 2007; 104:3639-44.
44. Mikoshiba K. The IP3 receptor/Ca2+ channel an its cellular function. Biochem Soc Symp 2007; 74:9-22.
45. Perera I, et al. Transient and sustained increases in inositol-1,4,5-trisphosphate precede the differential growth response in gravistimulated maize pulvini. Proc Natl Acad Sci USA 1999; 96:5838-43.
46. Perera I, et al. A role for inositol 1,4,5-trisphosphate in gravitropic signaling and the retention of coldperceived gravistimulation of oat shoot pulvini. Plant Physiol 2001; 125:1499-507.
47. Perera I, et al. Phosphoinositide signaling and plant gravitropism. Grav Space Biol Bull 2003; 17:102.
48. Perera I, et al. A universal role for inositol 1,4,5-trisphosphate-mediated signaling in plant gravitropism. Plant Physiol 2006; 140:746-60.
49. Fasano J, et al. Changes in root cap pH are required for the gravity response of the Arabidopsis root. Plant Cell 2001; 13:907-21.
50. Scott A, Allen N. Changes in cytosolic pH within Arabidposis root columella cells play a key role in the early signaling pathway for root gravitropism. Plant Physiol 1999; 121:1291-8.
51. Leitz G, et al. Statolith sedimentation kinetics and force transduction to the cortical endoplasmic reticulum in gravity-sensing Arabidopsis columella cells. Plant Cell 2009; 21:843-60.
52. Staves M. Cytoplasmic streaming and gravity sensing in Chara internodal cells. Planta 1997; 203:79-84.
53. Perbal G, et al. The dose-response curve of the gravitropic reaction: a re-analysis. Physiol Plant 2002; 114:336-42.
54. Yoder T, et al. Amyloplast sedimentation dynamics in maize columella cells support a new model for the gravity-sensing apparatus of roots. Plant Physiol 2001; 125:1045-60.
55. Hou G, et al. 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; 39:113-25.
56. Yamamoto K, Kiss J. Disruption of the actin cytoskeleton results in the promotion of gravitropism in inflorescence stems and hypocotyls of Arabidopsis. Plant Physiol 2002; 128:669-81.
57. Hou G, et al. Enhanced gravitropism of roots with a disrupted cap actin cytoskeleton. Plant Physiol 2003; 131:1360-73.
58. Bowman J, et al. Green genes-comparative genomics of the green branch of life. Cell 2007; 129:229-34.
59. Limbach C, et al. How to activate a plant gravireceptor. Early mechanisms of gravity sensing studied in Characean rhizoids during parabolic flights. Plant Physiol 2005; 139:1030-40.
60. Stanga J, et al. A role for the TOC complex in Arabidopsis root gravitropism. Plant Physiol 2009; 149:1896-905.
61. Sedbrook J, et al. ARG1 (Altered Response to Gravity) encodes a DnaJ-like protein that potentially interacts with the cytoskeleton. Proc Natl Acad Sci USA 1999; 96:1140-5.
62. Guan C, et al. The ARG1-LIKE2 (ARL2) gene of Arabidopsis thaliana functions in a gravity signal transduction pathway that is genetically distinct from the PGM pathway. Plant Physiol 2003; 133:100-12.
63. Mayer M, Bukau B. Hsp70 chaperones: cellular functions and molecular mechanisms. Cell Mol Life Sci 2005; 62:670-84.
64. Lupas A. Coiled coils: new structures and new functions. Trends Biochem Sci 1996; 21:375-82.
65. Li J, et al. Arabidopsis H+-PPase AVP1 regulates auxin-mediated organ development. Science 2005; 310:121-5.
66. Waegemann K, Söll J. Characterization of the protein import apparatus in isolated outer envelopes of chloroplasts. Plant J 1991; 191:149-58.
67. Perry L, Keegstra K. Envelope membrane proteins that interact with chloroplastic precursor proteins. Plant Cell 1994; 6:93-105.
68. Kessler F, et al. Identification of two GTP-binding proteins in the chloroplast protein import machinery. Science 1994; 266:1035-9.
69. Vojta A, et al. The protein translocon of the plastid envelopes. J Biol Chem 2004; 279:21401-5.
70. Martin W, et al. Evolutionary analysis of Arabidopsis, cyanobacterial and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc Natl Acad Sci USA 2002; 99:12246-51.
71. May T, Soll J. 14-3-3-proteins form a guidance complex with chloroplast precursor proteins in plants. Plant Cell 2000; 12:53-64.
72. Soll J, Schleiff E. Protein import into chloroplasts. Nature Rev Mol Cell Biol 2004; 5:198-208.
73. Kouranov A, et al. Tic22 is targeted to intermembrane space of chloroplasts by a novel pathway. J Biol Chem 1999; 274:25181-6.
74. Becker T, et al. Toc12, a novel subunit of the intermembrane space preprotein translocon of chloroplasts. Mol Cell Biol 2004; 15:5130-44.
75. Tu S, et al. Import pathways of chloroplast interior proteins and the outer-membrane protein OEP14 converge at Toc75. Plant Cell 2004; 16:2078-88.
76. Hust B, et al. Analysis of the subunit composition of TOC protein import complexes from chloroplasts in Arabidopsis thaliana reveals distinct complex subtypes. 2008; Submitted.
77. Schleiff E, et al. Characterization of the translocon of the outer envelope of chloroplasts. J Cell Biol 2003; 160:541-51.
78. Schleiff E, et al. Prediction of the plant β-barrel proteome: A case study of the chloroplast outer envelope. Protein Sci 2003; 12:748-59.
79. Sveshnikova N, et al. Toc34 is a preprotein receptor regulated by GTP and phosphorylation. Proc Natl Acad Sci USA 2000; 97:4973-8.
80. Baldwin A, et al. A molecular-genetic study of the Arabidopsis Toc75 gene family. Plant Physiol 2005; 138:715-33.
81. Kubis S, et al. Functional specialization amongst the Arabidopsis Toc159 family of chloroplast protein import receptors. Plant Cell 2004; 16:2059-77.
82. Ivanova Y, et al. Members of the Toc159 import receptor family represent distinct pathways for protein targeting to plastids. Mol Biol Cell 2004; 15:3379-92.
83. Chen K, et al. Initial binding of preproteins involving the Toc159 receptor can be bypassed during protein import into chloroplasts. Plant Physiol 2000; 122:813-22.
84. Bauer J, et al. The major protein import receptor of plastids is essential for chloroplast biogenesis. Nature 2000; 403:203-7.
85. Ma Y, et al. Two components of the chloroplast protein import apparatus, IAP86 and IAP75, interact with the transit sequence during the recognition and translocation or precursor proteins at the outer envelope. J Cell Biol 1996; 134:315-27.
86. Jackson-Constan D, Keegstra K. Arabidopsis genes encoding components of chloroplastic protein import apparatus. Plant Physiol 2001; 125:1567-76.
87. Gutensohn M, et al. Functional analysis of the two Arabidopsis homologues of Toc34, a component of the chloroplast protein import apparatus. Plant J 2000; 23:771-83.
88. Jelic M, et al. Two Toc34 homologues with different properties. Biochemistry 2003; 42:5906-16.
89. Kubis S, et al. The Arabidopsis ppi1 mutant is specifically defective in the expression, chloroplast import and accumulation of photosynthetic proteins. Plant Cell 2003; 15:1859-71.
90. Constan D, et al. An outer envelope membrane component of the plastid protein import apparatus plays an essential role in Arabidopsis. Plant J 2004; 38:93-106.
91. Kessler F, Schnell D. The function and diversity of plastid protein import pathways: a multilane GTPase highway into plastids. Traffic 2006; 7:248-57.
92. Li H, Chen L. Protein targeting and integration signal for the chloroplastic outer envelope membrane. Plant Cell 1996; 8:2117-26.
93. Jarvis P. Organellar proteomics: chloroplasts in the spotlight. Curr Biol 2004; 14:317-9.
94. Miras S, et al. Toc159-and Toc75-independent import of a transit sequence-less precursor into the inner envelope of chloroplasts. J Biol Chem 2007; 282:29482-92.
95. Nada A, Soll J. Inner envelope protein 32 is imported into chloroplasts by a novel pathway. J Cell Sci 2004; 117:3975-82.
96. Radhamony R, Theg S. Evidence for an ER to Golgi to chloroplast protein transport pathway. Trends Cell Biol 2006; 16:385-7.
97. Neuhaus H, Emes M. Nonphotosynthetic metabolism in plastids. Ann Rev Plant Physiol Plant Mol Biol 2000; 51:111-40.
98. Nomura H, et al. Evidence for chloroplast control of external Ca2+-induced cytosolic Ca2+ transients and stomatal closure. Plant J 2008; 53:988-98.