A proteomic approach to analyzing responses of Arabidopsis thaliana root cells to different gravitational conditions using an agravitropic mutant, pin2 and its wild type

Proteome Science

Volumn 9, Issue , 2011, Pages

  Tan, Chao ^a   Wang, Hui ^a,b   Zhang, Yue ^a   Qi, Bin ^a   Xu, Guoxin ^a   Zheng, Huiqiong ^a  

^a INSTITUTE OF PLANT PHYSIOLOGY AND ECOLOGY   (China)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Annexin; Arabidopsis thaliana; Clinorotation; Hypergravity; Pin2 mutant; Proteomics; Root tip

Indexed keywords

ARABIDOPSIS PROTEIN; AUXIN; MUTANT PROTEIN; PROTEIN PIN2; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; AUXIN TRANSPORT; COMPARATIVE STUDY; GRAVITROPISM; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PLANT CELL; PLANT ROOT; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEOMICS; ROOT GROWTH; ROOT LENGTH; SIGNAL TRANSDUCTION; WILD TYPE;

ARABIDOPSIS; ARABIDOPSIS THALIANA; COLUMELLA;

EID: 81055138784     PISSN: None     EISSN: 14775956     Source Type: Journal    
DOI: 10.1186/1477-5956-9-72     Document Type: Article

References (73)

1. Chen R, Rosen E, Masson PH. Gravitropism in higher plants. Plant Physiol 1999, 120:343-350. 10.1104/pp.120.2.343, 1539215, 11541950.
2. Morita MT, Tasaka M. Gravity sensing and signaling. Curr Opion Plant Biol 2004, 7:712-718.
3. Zheng HQ, Wei N, Chen AD, Wang LF, Zheng WB, Zhang T. Live imaging technique for studies of growth and development of Chinese cabbage under microgravity in a recoverable satellite (SJ-8). Micrograv Sci Tech 2008, 20:137-143.
4. Wei N, Tan C, Qi B, Zhang Y, Xu G, Zheng HQ. Changes in gravitational forces induce the modification of Arabidopsis thaliana silique pedicel positioning. J Expl Bot 2010, 61:3874-3884.
5. Sack FD. Plant gravity sensing. Int Rev Cyt 1991, 127:193-252.
6. 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. 10.1104/pp.125.1.252, 61007, 11154334.
7. Blancaflor EB, Masson PH. Plant gravitropism: unraveling the ups and downs of a complex process. Plant Physiol 2003, 113:1677-1690.
8. Perbal G, Driss-Ecole D. Mechanotransduction in gravisensing cells. Trends Plant Sci 2003, 8:498-504. 10.1016/j.tplants.2003.09.005, 14557047.
9. Leitz G, Kang B-H, Schoewaelder M, 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. 10.1105/tpc.108.065052, 2671718, 19276442.
10. Muday GK. Auxins and tropisms. J Plant Growth Regul 2001, 20:226-243. 10.1007/s003440010027, 12033223.
11. Friml J. Auxin transport: shaping the plant. Curr Opin Plant Biol 2003, 6:7-12. 10.1016/S1369526602000031, 12495745.
12. Morita MT. Directional gravity sensing in gravitropism. Ann Rev Plant Biol 2010, 61:705-720.
13. Bennett MJ, Marchant A, Green HG, May ST, Ward SP, Millner PA, Walker AR, Schulz B, Feldmann KA. Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science 1996, 273:948-950. 10.1126/science.273.5277.948, 8688077.
14. Chen R, Hilson P, Sedbrook J, Rosen E, Caspar T, Masson PH. The Arabidopsis thaliana AGRAVITROPIC(AGR1) gene encodes a component of the polar auxin-transport efflux carrier. Proc Natl Acad Sci USA 1998, 95:15112-15117. 10.1073/pnas.95.25.15112, 24584, 9844024.
15. Luschnig C, Gaxiola RA, Grisafi P, Fink GR. EIR1, A root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Gen Dev 1998, 12:2175-2187.
16. Müller A, Guan G, Gälweiler L, Tänzler P, Huijser P, Marchant A, Parry G, Bennett M, Wisman E, Palme K. AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J 1998, 17:6903-6911. 10.1093/emboj/17.23.6903, 1171038, 9843496.
17. Moore I. Gravitropism: lateral thinking in auxin transport. Curr Biol 2002, 12:R452-R454. 10.1016/S0960-9822(02)00943-0, 12121635.
18. Abas L, Benjamins R, Malenica N, Paciorek T, Wiśniewska 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. 10.1038/ncb1369, 16489343.
19. Hoshino T, Miyamoto K, Ueda J. 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. J Plant Res 2007, 120:619-628. 10.1007/s10265-007-0103-2, 17712525.
20. Peer WA, Blakeslee JJ, Yang H, Murphy AS. Seven things we think we know about auxin transport. Mol Plant 2011, 4:487-504. 10.1093/mp/ssr034, 21505044.
21. Palme K, Gäweiler L. PIN-pointing the molecular basis of auxin transport. Curr Opin Plant Biol 1999, 2:375-381. 10.1016/S1369-5266(99)00008-4, 10508762.
22. Palme K, Dovzhenko A, Ditengou FA. Auxin transport and gravitational research: perspectives. Protoplasma 2006, 229:175-181. 10.1007/s00709-006-0216-9, 17180499.
23. Sukumar P, Edwards KS, Rahman A, Delong A, Muday GK. PINOD kinase regulates root gravitropism through modulation of PIN2-dependent basipetal auxin transport in Arabidopsis. Plant Physiol 2009, 150:722-735. 10.1104/pp.108.131607, 2689958, 19363095.
24. 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 USA 2003, 100:2987-2991. 10.1073/pnas.0437936100, 151453, 12594336.
25. Paponov I, Teale WD, Trebar M, Blilou I, Palme K. The PIN auxin efflux facilitators: evolutionary and functional perspectives. Trends Plant Sci 2005, 10:170-177. 10.1016/j.tplants.2005.02.009, 15817418.
26. Kleine-Vehn J, Ding Z, Jones AR, Tasaka M, Morita M, Friml J. Gravity-induced PIN transcytosis for polarizaion of auxin fluxes in gravity-sensing root cells. Proc Natl Acad Sci USA 2010, 107:22344-22349. 10.1073/pnas.1013145107, 3009804, 21135243.
27. Utsuno K, Shikanai T, Yamada Y, Hashimoto T. Agr, an Agravitropic locus of Arabidopsis thaliana, encodes a novel membrane-protein family member. Plant Cell Physiol 1998, 39:1111-1118.
28. Rashotte AM, Brady SR, Reed RC, Ante SJ, Muday GK. Basipetal auxin transport is required for gravitropism in roots of Arabidopsis. Plant Physiol 2000, 122:481-490. 10.1104/pp.122.2.481, 58885, 10677441.
29. Rahman A, Takahashi M, Shibasaki K, Wu S, Inaba T, Tsurumi S, Baskin TI. Gravitropism of Arabidopsis thaliana roots requires the polarization of PIN2 toward the root tip in meristematic cortical cells. Plant Cell 2010, 22:1762-1776. 10.1105/tpc.110.075317, 2910985, 20562236.
30. Gälweiler L, Guan C, Muller A, Wisman E, Mendgen K, Yephremov A, Palme K. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 1998, 282:2226-2230.
31. Kleine-Vehn J, Leitner J, Zwiewka M, Sauer M, Abas L, Luchnig C, Friml J. Differential degradation of PIN2 auxin efflux carrier by retromer-dependent vacuolar targeting. Proc Natl Acad Sci USA 2008, 105:17812-17817. 10.1073/pnas.0808073105, 2584678, 19004783.
32. Miyamoto K, Oka M, Yamamoto R, Masuda Y, Hoson T, Kamisaka S, Ueda J. Auxin polar transport in Arabidopsis under simulated microgravity conditions-relevance to growth and development. Adv Space Res 1999, 23:2033-2036. 10.1016/S0273-1177(99)00344-0, 11710387.
33. Moseyko N, Zhu T, Chang H-S, Wang X, Feldman LJ. Transcription profiling of the early grvitropic response in Arabidopsis using high-density oligonucleotide probe microarrays. Plant Physiol 2002, 130:720-728. 10.1104/pp.009688, 166601, 12376639.
34. Centis-Aubay S, Gasset G, Mazars C, Ranjeva R, Graziana A. Changes in gravitational forces induce modifications of gene expression in A. thaliana seedlings. Planta 2003, 218:179-185. 10.1007/s00425-003-1103-7, 13680230.
35. Martzivanou M, Hampp R. Hyper-gravity effects on the Arabidopsis transcriptome. Physiol Plant 2003, 118:221-231. 10.1034/j.1399-3054.2003.00092.x, 14552351.
36. Kimbrough JM, Salinas-Mondragon R, Boss WF, Brown CS, Sederoff HW. The fast and transient transcriptional network of gravity and mechanical stimulation in the Arabidopsis root apex. Plant Physiol 2004, 136:2790-2805. 10.1104/pp.104.044594, 523342, 15347791.
37. Martzivanou M, Babbick M, Cogoli-Greuter M, Hampp R. Microgravity-related changes in gene expression after short-term exposure of Arabidopsis thaliana cell cultures. Protoplasma 2006, 229:155-162. 10.1007/s00709-006-0203-1, 17180497.
38. Kamada M, Higashitani A, Ishioka N. Proteomic analysis of Arabidopsis root gravitropism. Biol Sci Space 2005, 19:148-154.
39. Barjaktarović Z, Nordheim A, Lamkemeyer T, Fladerer C, Madlung J, Hampp R. Time-course of changes in amounts of specific proteins upon exposure to hyper-g, 2-D clinorotation, and 3-D random positioning of Arabidopsis cell cultures. J Exp Bot 2007, 58:4357-4363. 10.1093/jxb/erm302, 18182437.
40. Wang H, Zheng HQ, Sha W, Zeng R, Xia QC. A proteomic approach to analysing responses of Arabidopsis thaliana callus cells to clinostat rotation. J Exp Bot 2006, 57:827-835. 10.1093/jxb/erj066, 16449375.
41. Hampp R, Hoffmann E, Schönherr K, Johann P, Filippis LD. Fusion and metabolism of plant cells as affected by microgravity. Planta 1997, 203:S42-S53. 10.1007/PL00008114, 9299795.
42. Obenland DM, Brown DS. The influence of altered gravity on carbohydrate metabolism in excised wheat leaves. J Plant Physiol 1994, 144:696-699.
43. Swarup R, Kramer EM, Perry P, Knox K, Leyser HM, Haseloff J, Beemster GT, Bhalerao R, Bennett MJ. Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal. Nat Cell Biol 2005, 7:1057-1065.
44. Himmelspach R, Nick P, Schäfer E, Ehmann B. Developmental and light-dependent changes of the cytosolic chaperonin containing TCP-1(CCT) subunits in maize seedlings, and the localization in coleoptiles. Plant J 1997, 12:1299-1310. 10.1046/j.1365-313x.1997.12061299.x, 9450343.
45. Nick P, Heuing A, Ehmann B. Plant chaperonins: a role in microtubule-dependent wall formation?. Protoplasma 2000, 211:234-244.
46. Cordier H, Karst F, Bergès T. Heterologous expression in Saccharomyces cerevisiae of an Arabidopsis thaliana cDNA encoding mevalonate diphosphate decarboxylase. Plant Mol Biol 1999, 39:953-967. 10.1023/A:1006181720100, 10344201.
47. Kotchoni SO, Kuhns C, Ditzer A, Kirch H-H, Bartels D. Over-expression of different aldehyde dehydrogenas genes in Arabidopsis thaliana confers tolerance to abiotic stress and protects plants against lipid peroxidation and oxidative stress. Plant Cell Env 2006, 29:1033-1048.
48. Gaina V, ŠvegČdiene D, Raklevičiene D, Koryzniene D, Stanevičiene R, Laurinavičius R. Kinetics of amyloplast movement in cress root statocytes under different gravitational loads. Adv Space Res 2003, 31:2275-2281. 10.1016/S0273-1177(03)00255-2, 14686443.
49. Fitzelle KJ, Kiss JZ. Restoration of gravitropic sensitivity in starch-deficient mutants of Arabidopsis by hypergravity. J Exp Bot 2001, 52:265-275. 10.1093/jexbot/52.355.265, 11283171.
50. Popova AF. Comparative characteristic of mitochondria ultrastructural organization in Chlorella cells under altered gravity conditions. Adv Space Res 2003, 31:2253-2259. 10.1016/S0273-1177(03)00252-7, 14686440.
51. Perera I, Heilmann I, Chang S, Boss W, Kaufman P. 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. 10.1104/pp.125.3.1499, 65627, 11244128.
52. Plieth C, Trewavas AJ. Reorientation of seedlings in the earth's gravitational field induces cytosolic calcium transients. Plant Physiol 2002, 129:786-796. 10.1104/pp.011007, 161701, 12068119.
53. Boonsirichai K, Sedbrook JC, Chen R, Gilroy S, Masson PH. ARG1 is a peripheral membrane protein that modulates gravity-induced cytoplasmic alkalinization and lateral auxin transport in plant statocytes. Plant Cell 2003, 15:2612-2625. 10.1105/tpc.015560, 280565, 14507996.
54. Harrison BR, Masson PH. ARL2, ARG1 and PIN3 define a gravity signal transduction pathway in root statocytes. Plant J 2008, 53:380-392.
55. Li P, Wind JJ, Shi X, Zhang H, Hanson J, Smeekens SC, Teng S. Fructose sensitivity is suppressed in Arabidopsis by the transcription factor ANAC089 lacking the membrane-bound domain. Proc Natl Acad Sci USA 2010, 108:3436-3441.
56. Moore BD. Bifunctional and moonlighting enzymes: lighting the way to regulatory control. Trends Plant Sci 2004, 9:221-228. 10.1016/j.tplants.2004.03.005, 15130547.
57. Hancock JT, Henson D, Nyirenda M, Desikan R, Harrison J, Lewis M, Hughes J, Neill SJ. Proteomic identification of glyceraldehydes 3-phosphate dehydrogenase as an inhibitory target of hydrogen peroxide in Arabidopsis. Plant Physiol Biochem 2005, 43:828-835. 10.1016/j.plaphy.2005.07.012, 16289945.
58. Sergeant N, Wattez A, Galván-Valencia M, Ghestem A, David J-P, Lemoine J, Sautiére P-E, Dachary J, Mazat J-P, Michalski J-C, Velours J, Mena-López R, Delacourte A. Association of ATP syntase α-chain with neurofibrillary degeneration in alzheimer's disease. Neurosci 2003, 117:293-303.
59. Singh S, Khar A. Differential gene expression during apoptosis induced by a serum factor: role of mitochondrial F0-F1 ATP synthase complex. Apotosis 2005, 10:1469-1482.
60. Dunand C, Crèvecoeur M, Penel C. Distribution of superoxide and hydrogen peroxide in Arabidopsis root and their influence on root development: possible interaction with peroxidases. New Phytologist 2007, 174:332-341. 10.1111/j.1469-8137.2007.01995.x, 17388896.
61. Joo JH, Bae YS, Lee JS. Role of auxin-induced reactive oxygen species in root gravitropism. Plant Physiol 2001, 126:1055-1060. 10.1104/pp.126.3.1055, 116462, 11457956.
62. Lange PR, Geserick C, Tischendorf G, Zrenner R. Functions of chloroplastic adenylate kinases in Arabidopsis. Plant Physiol 2008, 146:492-504. 2245825, 18162585.
63. Meng G, Zhai R, Liu B, Zheng X. Identification of a novel nuclear-localized adenylate kinase from Drosophila melanogaster. Biochemistry (Moscow) 2008, 73:38-43.
64. Carrari F, Coll-Garcia D, Schauer N, Lytovhenko A, Palacios-Rojas N, Balbo I, Rosso M, Fernie AR. Deficiency of a plastidial adenylate kinase in Arabidopsis results in elevated photosynthetic amino acid biosynthesis and enhance growth. Plant Physiol 2005, 137:70-82. 10.1104/pp.104.056143, 548839, 15618410.
65. Salekdeh GH, Siopongco J, Wade LJ, Ghareyazie B, Bennett J. A proteomic approach to analyzing drought- and salt-responsiveness in rice. Field Crops Res 2002, 76:199-219.
66. Weber H, Engelmann S, Becher D, Hecker M. Oxidative stress triggers thiol oxidation in the glyceraldehyde-3-phosphate dehydrogenase of Staphylococcus aureus. Mol Microbiol 2004, 52:133-140. 10.1111/j.1365-2958.2004.03971.x, 15049816.
67. Young L-S, Harrison BR, Murthy N, Moffatt BA, Gilroy S, Masson PH. Adenosine kinase modulates root gravitropism and cap morphogenesis in Arabidopsis. Plant Physiol 2006, 142:564-573. 10.1104/pp.106.084798, 1586050, 16891550.
68. 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. 10.1111/j.1365-313X.2004.02114.x, 15200646.
69. Hou G, Mohamalawari DR, Blancaflor EB. Enhanced gravitropism of roots with a disrupted cap actin cytoskeleton. Plant Physiol 2003, 131:1360-1373. 10.1104/pp.014423, 166895, 12644685.
70. Murashige T, Skoog F. A revised medium for rapid growth and bio assays with tobacco tissue culture. Physiol Plant 1962, 15:473-497.
71. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254. 10.1016/0003-2697(76)90527-3, 942051.
72. Yu LR, Shao XX, Jiang WL, Xu D, Chang YC, Xu YH, Xia QC. Proteome alterations in human hepatoma cells transfected with antisense epidermal growth factor receptor sequence. Electrophoresis 2001, 22:3001-3008. 10.1002/1522-2683(200108)22:14<3001::AID-ELPS3001>3.0.CO;2-5, 11565794.
73. Clough SJ, Bent AF. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabiopsis thaliana. Plant J 1998, 16:735-743. 10.1046/j.1365-313x.1998.00343.x, 10069079.