Arabidopsis phosphatidylinositol monophosphate 5-kinase 2 is involved in root gravitropism through regulation of polar auxin transport by affecting the cycling of PIN proteins

Cell Research

Volumn 22, Issue 3, 2012, Pages 581-597

  Mei, Yu ^a   Jia, Wen Jing ^a   Chu, Yu Jia ^a   Xue, Hong Wei ^a  

^a INSTITUTE OF PLANT PHYSIOLOGY AND ECOLOGY   (China)

Author keywords

Arabidopsis; phosphatidylinositol monophosphate 5 kinase 2 (PIP5K2); polar auxin transport; root development; vesicle trafficking

Indexed keywords

1-PHOSPHATIDYLINOSITOL-4-PHOSPHATE 5-KINASE; ARABIDOPSIS PROTEIN; INDOLEACETIC ACID DERIVATIVE; PHOSPHATIDYLINOSITOL 4 PHOSPHATE KINASE; PHOSPHOTRANSFERASE; PIN2 PROTEIN, ARABIDOPSIS; PIN3 PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; ARTICLE; CHEMISTRY; ENZYMOLOGY; GRAVITROPISM; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY; PLANT ROOT; TRANSPORT AT THE CELLULAR LEVEL;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOLOGICAL TRANSPORT; GRAVITROPISM; INDOLEACETIC ACIDS; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PLANT ROOTS;

ARABIDOPSIS;

EID: 84857794081     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2011.150     Document Type: Article

References (76)

1. Stevenson JM, Perera IY, Heilmann I, Persson S, Boss WF. Inositol signaling and plant growth. Trends Plant Sci 2000; 5:252-258. (Pubitemid 30347751)
2. Xue HW, Chen X, Li G. Involvement of phospholipid signaling in plant growth and hormone effects. Curr Opin Plant Biol 2007; 10:483-489. (Pubitemid 47503878)
3. Xue HW, Chen X, Mei Y. Function and regulation of phospholipid signalling in plants. Biochem J 2009; 421:145-156.
4. Berridge MJ. Rapid accumulation of inositol trisphosphate reveals that agonists hydrolyse polyphosphoinositides instead of phosphatidylinositol. Biochem J 1983; 212:849-858. (Pubitemid 13056904)
5. Meijer HJ, Munnik T. Phospholipid-based signaling in plants. Annu Rev Plant Biol 2003; 54:265-306. (Pubitemid 37399995)
6. Wasteneys GO, Galway ME. Remodeling the cytoskeleton for growth and form: An overview with some new views. Annu Rev Plant Biol 2003; 54:691-722. (Pubitemid 37400010)
7. Wenk MR, De Camilli P. Protein-lipid interactions and phosphoinositide metabolism in membrane traffic: Insights from vesicle recycling in nerve terminals. Proc Natl Acad Sci USA 2004; 101:8262-8269. (Pubitemid 38736563)
8. Cote GG, Yueh YG, Crain RC. Phosphoinositide turnover and its role in plant signal transduction. Subcell Biochem 1996; 26:317-343.
9. Suh BC, Hille B. Regulation of ion channels by phosphatidylinositol 4,5-bisphosphate. Curr Opin Neurobiol 2005; 15:370-378. (Pubitemid 40806451)
10. Haucke V. Phosphoinositide regulation of clathrin-mediated endocytosis. Biochem Soc Trans 2005; 33:1285-1289. (Pubitemid 41779669)
11. Clague MJ, UrbéS, de Lartigue J. Phosphoinositides and the endocytic pathway. Exp Cell Res 2009; 315:1627-1631.
12. Yao HY, Xue HW. Signals and mechanisms affecting vesicular trafficking during root growth. Curr Opin Plant Biol 2011 Jul 15. doi:10.1016/j.pbi.2011.06. 009
13. Mueller-Roeber B, Pical C. Inositol phospholipid metabolism in Arabidopsis. Characterized and putative isoforms of inositol phospholipid kinase and phosphoinositide-specific phospholipase C. Plant Physiol 2002; 130:22-46.
14. Nishi M, Mizushima A, Nakagawara K, Takeshima H. Characterization of human junctophilin subtype genes. Biochem Biophys Res Commun 2000; 273:920-927. (Pubitemid 30481055)
15. Elge S, Brearley C, Xia HJ, Kehr J, Xue HW, Mueller-Roeber B. An Arabidopsis inositol phospholipid kinase strongly expressed in procambial cells: Synthesis of PtdIns(4,5)P2 and PtdIns(3,4,5)P3 in insect cells by 5-phosphorylation of precursors. Plant J 2001; 26:561-571. (Pubitemid 32692899)
16. Stenzel I, Ischebeck T, König S, et al. The type B phosphatidylinositol-4-phosphate 5-kinase 3 is essential for root hair formation in Arabidopsis thaliana. Plant Cell 2008; 20:124-141. (Pubitemid 352844038)
17. Ischebeck T, Stenzel I, Heilmann I. Type B phosphatidylinositol-4- phosphate 5-kinases mediate Arabidopsis and Nicotiana tabacum pollen tube growth by regulating apical pectin secretion. Plant Cell 2008; 20:3312-3330.
18. Zhao Y, Yan A, Feijo J, et al. Phosphoinositides regulate clathrin-dependent endocytosis at the tip of pollen tubes in Arabidopsis and Tobacco. Plant Cell 2010; 22:4031-4044.
19. Mikami K, Katagiri T, Iuchi S, Yamaguchi-Shinozaki K, Shinozaki K. A gene encoding phosphatidylinositol-4-phosphase 5-kinase is induced by water stress and abscisic acid in Arabidopsis thaliana. Plant J 1998; 15:563-568.
20. Kusano H, Testerink C, Vermeer JEM, et al. The Arabidopsis phosphatidylinositol phosphate 5-kinase PIP5K3 is a key regulator of root hair tip growth. Plant Cell 2008; 20:367-380. (Pubitemid 352844018)
21. Lee Y, Kim YW, Jeon BW, et al. Phosphatidylinositol 4, 5-bisphosphate is important for stomatal opening. Plant J 2007; 52:803-816. (Pubitemid 350157748)
22. Sousa E, Kost B, Malhó R. Arabidopsis phosphatidylinositol-4- monophosphate 5-kinase 4 regulates pollen tube growth and polarity by modulating membrane recycling. Plant Cell 2008; 20:3050-3064.
23. Lou Y, Gou JY, Xue HW. PIP5K9, an Arabidopsis phosphatidylinositol monophosphate kinase, interacts with a cytosolic invertase to negatively regulate sugar-mediated root growth. Plant Cell 2007; 19:163-181. (Pubitemid 46852709)
24. Casimiro I, Marchant A, Bhalerao RP, et al. Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell 2001; 13:843-852. (Pubitemid 32375905)
25. Nibau C, Gibbs DJ, Coates JC. Branching out in new directions: The control of root architecture by lateral root formation. New Phytol 2008; 179:595-614.
26. Boerjan W, Cervera MT, Delarue M, et al. Superroot, a recessive mutation in Arabidopsis, confers auxin overproduction. Plant Cell 1995; 7:1405-1419.
27. King JJ, Stimart DP, Fisher RH, Bleecker AB. A mutation altering auxin homeostasis and plant morphology in Arabidopsis. Plant Cell 1995; 7:2023-2037. (Pubitemid 2615563)
28. Laskowski MJ, Williams ME, Nusbaum HC, Sussex IM. Formation of lateral root meristems is a two-stage process. Development 1995; 121:3303-3310.
29. Ruegger M, Dewey E, Gray WM, Hobbie L, Turner J, Estelle M. The TIR1 protein of Arabidopsis functions in auxin response and is related to human SKP2 and yeast Grr1p. Genes Dev 1998; 12:198-207. (Pubitemid 28060450)
30. Marchant A, Bhalerao R, Casimiro I, et al. AUX1 promotes lateral root formation by facilitating indole-3-acetic acid distribution between sink and source tissues in the Arabidopsis seedling. Plant Cell 2002; 14:589-597. (Pubitemid 34299665)
31. Park JE, Park JY, Kim YS, et al. GH3-mediated auxin homeostasis links growth regulation with stress adaptation response in Arabidopsis. J Biol Chem 2007; 282:10036-10046.
32. Swarup K, Benkova E, Swarup R, et al. The auxin influx carrier LAX3 promotes lateral root emergence. Nat Cell Biol 2008; 10:946-954.
33. Bandyopadhyay A, Blakeslee JJ, Lee OR, et al. Interactions of PIN and PGP auxin transport mechanisms. Biochem Soc Trans 2007; 35:137-141.
34. Petrasek J, Mravec J, Bouchard R, et al. PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 2006; 312:914-918. (Pubitemid 43727324)
35. Zhang J, Vanneste S, Brewer PB, et al. Inositol trisphosphateinduced Ca2+ signaling modulates auxin transport and PIN polarity. Dev Cell 2011; 14:855-66.
36. Bennett MJ, Marchant A, Green HG, et al. Arabidopsis AUX1 gene: A permease-like regulator of root gravitropism. Science 1996; 273:948-950. (Pubitemid 26275169)
37. Müller A, Guan C, Gälweiler L, et al. AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J 1998; 17:6903-6911. (Pubitemid 28550284)
38. Li L, Xu J, Xu ZH, Xue HW. Brassinosteroids stimulate plant tropisms through modulation of polar auxin transport in Brassica and Arabidopsis. Plant Cell 2005; 17:2738-2753.
39. 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. (Pubitemid 34150504)
40. 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 USA 1999; 96:5838-5843. (Pubitemid 29234705)
41. 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. (Pubitemid 43956293)
42. Wang Y, Lin WH, Chen X, Xue HW. The role of Arabidopsis 5PTase 13 in root gravitropism through modulation of vesicle trafficking. Cell Res 2009; 19:1191-1204.
43. Geldner N, Anders N, Wolters H, et al. The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 2003; 112:219-230. (Pubitemid 36144111)
44. Jaillais Y, Fobis-Loisy I, Miege C, Rollin C, Gaude T. AtSNX1 defines an endosome for auxin-carrier trafficking in Arabidopsis. Nature 2006; 443:106-109. (Pubitemid 44344057)
45. Dhonukshe P, Aniento F, Hwang I, et al. Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Curr Biol 2007; 17:520-527. (Pubitemid 46420535)
46. Geldner N, Friml J, Stierhof YD, Jurgens G, Palme K. Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 2001; 413:425-428. (Pubitemid 32928597)
47. Men S, BouttéY, Ikeda Y, et al. Sterol-dependent endocytosis mediates post-cytokinetic acquisition of PIN2 auxin efflux carrier polarity. Nat Cell Biol 2008; 10:237-244. (Pubitemid 351194054)
48. Pan J, Fujioka S, Peng J, Chen J, Li G, Chen R. The E3 ubiquitin ligase SCFTIR1/AFB and membrane sterols play key roles in auxin regulation of endocytosis, recycling, and plasma membrane accumulation of the auxin efflux transporter PIN2 in Arabidopsis thaliana. Plant Cell 2009; 21:568-580.
49. Lin WH, Wang Y, Mueller-Roeber B, Brearley CA, Xu ZH, Xue HW. At5PTase13 modulates cotyledon vein development through regulating auxin homeostasis. Plant Physiol 2005; 139:1677-1691. (Pubitemid 43899810)
50. Li G, Xue HW. Arabidopsis PLDζ2 regulates vesicle trafficking and is required for auxin response. Plant Cell 2007; 19:281-295. (Pubitemid 46852717)
51. Zhang ZB, Yang G, Arana F, Chen Z, Li Y, Xia HJ. Arabidopsis inositol polyphosphate 6-/3-kinase (AtIpk2b) is involved in axillary shoot branching via auxin signaling. Plant Physiol 2007; 144:942-951. (Pubitemid 46944758)
52. Alonso JM, Stepanova AN, Leisse TJ, et al. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 2003; 301:653-657. (Pubitemid 36927950)
53. Zhang H, Jennings A, Barlow PW, Forde GB. Dual pathways for regulation of root branching by nitrate. Proc Natl Acad Sci USA 1999; 96:6529-6534. (Pubitemid 29256700)
54. DeWald DB, Ozaki S, Malaviya S, et al. Cellular calcium mobilization in response to phosphoinositide delivery. Cell Calcium 2005; 38:59-72. (Pubitemid 41150654)
55. Casimiro I, Beeckman T, Graham N, et al. Dissecting Arabidopsis lateral root development. Trends Plant Sci 2003; 8:165-171. (Pubitemid 36726458)
56. Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ. Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 1997; 9:1963-1971. (Pubitemid 28174069)
57. Rashotte AM, Brady SR, Reed RC, Ant SJ, Muday GK. Basipetal auxin transport is required for gravitropism in roots of Arabidopsis. Plant Physiol 2000; 122:481-490. (Pubitemid 30153116)
58. Perrin RM, Young LS, Murthy UMN, et al. Gravity signal transduction in primary roots. Ann Bot 2005; 96:737-743. (Pubitemid 41330543)
59. Palme K, Dovzhenko A, Ditengou FA. Auxin transport and gravitational research: Perspectives. Protoplasma 2006; 229:175-181. (Pubitemid 44974253)
60. Owen DJ, Collins BM, Evans PR. Adaptors for clathrin coats: Structure and function. Annu Rev Cell Dev Biol 2004; 20:153-191. (Pubitemid 39488636)
61. Bolte S, Talbot C, Boutte Y, Catrice O, Read ND, Satiat-Jeunemaitre B. FM-dyes as experimental probes for dissecting vesicle trafficking in living plant cells. J Microsc 2004; 214:159-173. (Pubitemid 38553612)
62. Nebenfuhr A, Ritzenthaler C, Robinson DG. Brefeldin A: Deciphering an enigmatic inhibitor of secretion. Plant Physiol 2002; 130:1102-1108. (Pubitemid 35352938)
63. Blakeslee JJ, Bandyopadhyay A, Lee OR, et al. Interactions among PIN-FORMED and P-glycoprotein auxin transporters in Arabidopsis. Plant Cell 2007; 1:131-147. (Pubitemid 46852707)
64. Rashotte A, Delong A, Muday G. Genetic and chemical reductions in protein phosphatase activity alter auxin transport, gravity response, and lateral root growth. Plant Cell 2001; 13:1683-1697. (Pubitemid 32675728)
65. 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. (Pubitemid 37470662)
66. Ottenschläger I, Wolff P, Wolverton C, et al. Gravity-regulated differential auxin transport from columella to lateral root cap cells. Proc Natl Acad Sci USA 2003; 100:2987-2991. (Pubitemid 36297610)
67. Yang X, Song L, Xue HW. Membrane steroid binding protein 1 (MSBP1) stimulates tropism by regulating vesicle trafficking and auxin redistribution. Mol Plant 2008; 1:1077-1087.
68. Abas L, Benjamins R, Malenica N, et al. Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat Cell Biol 2006; 8:249-256. (Pubitemid 43336066)
69. Camacho L, Smertenko AP, Pérez-Gómez J, Hussey PJ, Moore I. Arabidopsis Rab-E GTPases exhibit a novel interaction with a plasma-membrane phosphatidylinositol-4-phosphate 5-kinase. J Cell Sci 2009; 122:4383-4392.
70. Speth EB, Imboden L, Hauck P, He SY. Subcellular localization and functional analysis of the Arabidopsis GTPase RabE. Plant Physiol 2009; 149:1824-1837.
71. Benková E, Michniewicz M, Sauer M, et al. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 2003; 115:591-602. (Pubitemid 37506047)
72. Di Paolo G, De Camilli P. Phosphoinositides in cell regulation and membrane dynamics. Nature 2006; 443:651-657. (Pubitemid 44564702)
73. Clough SJ, Bent AF. Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 1998; 16:735-743.
74. Liu W, Xu ZH, Luo D, Xue HW. Roles of OsCKI1, a rice casein kinase I, in root development and plant hormone sensitivity. Plant J 2003; 36:189-202. (Pubitemid 37293060)
75. Kowalczyk M, Sandberg G. Quantitative analysis of indole-3-acetic acid metabolites in Arabidopsis. Plant Physiol 2001; 127:1845-1853. (Pubitemid 34050048)
76. Qi J, Qian Q, Bu Q, et al. Mutation of the rice Narrow leaf1 gene, which encodes a novel protein, affects vein patterning and polar auxin transport. Plant Physiol 2008; 147:1947-1959. (Pubitemid 352844234)