Hydroponics on a chip: Analysis of the Fe deficient Arabidopsis thylakoid membrane proteome

Journal of Proteomics

Volumn 72, Issue 3, 2009, Pages 397-415

  Laganowsky, Arthur ^a   Gómez, Stephen M ^b   Whitelegge, Julian P ^c   Nishio, John N ^a  

^a CALIFORNIA STATE UNIVERSITY   (United States)

^b Central New Mexico Community College   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Arabidopsis thaliana; Chloroplast; Hydroponics; Hydroponics on a chip; Intact mass proteomics; Iron deficiency; Proteomics; Thylakoids

Indexed keywords

ANTIOXIDANT; IRON; LIGHT HARVESTING COMPLEX IIB PROTEIN LHCB1; LIGHT HARVESTING COMPLEX IIB PROTEIN LHCB2; PHOTOSYSTEM II OXYGEN EVOLVING COMPLEX PSBH; PROTEOME; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ARABIDOPSIS; ARTICLE; CHLOROPLAST; HYDROPONICS; HYDROPONICS ON A CHIP; ISOTOPE LABELING; LIGHT HARVESTING SYSTEM; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; PHOTOSYSTEM II; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PROCESSING; THYLAKOID MEMBRANE;

ARABIDOPSIS; ELECTRON TRANSPORT; HYDROPONICS; IRON; MASS SPECTROMETRY; PROTEOME; PROTEOMICS; THYLAKOIDS;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 63549131287     PISSN: 18743919     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jprot.2009.01.024     Document Type: Article

References (107)

1. Gibeaut D.M., Hulett J., Cramer G.R., and Seemann J.R. Maximal biomass of Arabidopsis thaliana using a simple, low-maintenance hydroponics method and favorable environmental conditions. Plant Physiol 115 (1997) 317-319
2. Taji T., Seki M., Satou M., Sakurai T., Kobayashi M., Ishiyama K., et al. Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis Microarray. Plant Physiol 135 (2004) 1697-1709
3. Schlesier B., Bréton F., and Mock H.P. A hydroponic culture system for growing Arabidopsis thaliana plantlets under sterile conditions. Plant Mol Biol Rept 21 (2003) 449-456
4. Arteca R.N., and Arteca J.M. A novel method for growing Arabidopsis thaliana plants hydroponically. Physiol Plant 108 (2000) 188-193
5. +-ATPase gene expression by affecting FER (or FER-like) gene activity. J Exp Bot 57 (2006) 4145-4154
6. Tocquin P., Corbesier L., Havelange A., Pieltain A., Kurtem E., Bernier G., et al. A novel high efficiency, low maintenance, hydroponic system for synchronous growth and flowering of Arabidopsis thaliana. BMC Plant Biol 3 (2003) 2
7. Hoagland DR, Arnon DI. The water-culture method for growing plants without soil. In The College of Agriculture, ed, California Agricultural Experiment Station Circular 347, Revised January 1950. University of California, Berkeley; 1950.
8. Bindschedler L.V., Palmblad M., and Cramer R. Hydroponic isotope labeling of entire plants (HILEP) for quantitative proteomics; an oxidative stress study. Phytochemistry 69 (2008) 1962-1972
9. Huttlin E.L., Hegeman A.D., Harms A.C., and Sussman M.R. Comparison of full versus partial metabolic labeling for quantitative proteomic analysis in Arabidopsis thaliana. Mol Cell Prot 6 (2007) 860-881
10. Bartels A., Mock H.P., and Papenbrock J. Differential expression of Arabidopsis sulfurtransferases under various growth conditions. Plant Physiol Biochem 45 (2007) 178-187
11. Kolář J., and Seňková J. Reduction of mineral nutrient availability accelerates flowering of Arabidopsis thaliana. J Plant Physiol 165 (2008) 1601-1609
12. Sweetlove L.J., Taylor N.L., and Leaver C.L. Isolation of intact, functional mitochondria from the model plant Arabidopsis thaliana. Methods Mol Biol 372 (2007) 125-136
13. Whitelegge J.P., Gundersen C.B., and Faull K.F. Electrospray-ionization mass spectrometry of intact intrinsic membrane proteins. Protein Sci 7 (1998) 1423-1430
14. Fromme P., and Grotjohann I. Structure of photosystems I and II. Results Probl Cell Differ 45 (2008) 33-72
15. Zouni A., Horst-Tobias W., Kern J., Fromme P., Krauss N., Saenger W., et al. Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409 (2000) 739-743
16. Ben-Shem A., Frolow F., and Nelson N. Crystal structure of plant photosystem I. Nature 426 (2003) 630-635
17. 6f complex for its charge transfer pathways. Biochim Biophys Acta 1757 (2006) 339-345
18. 6f complex of oxygenic photosynthesis: tuning the cavity. Science 302 (2003) 1009-1014
19. McCarty R.E., Evron Y., and Johnson E.A. The chloroplast ATP synthase: a rotary enzyme?. Annu Rev Plant Physiol Plant Mol Biol 51 (2000) 83-109
20. Richter M.L., Samra H.S., He F., Giessel A.J., and Kuczera K.K. Coupling proton movement to ATP synthesis in the chloroplast ATP synthase. J Bioenerg Biomembr 37 (2005) 467-473
21. Gómez S.M., Nishio J.N., Faull K.F., and Whitelegge J.P. The chloroplast grana proteome defined by intact mass measurements from liquid chromatography mass spectrometry. Mol Cell Prot 1 (2002) 46-59
22. Gómez S.M., Bil K.Y., Aguilera R., Nishio J.N., Faull K.F., and Whitelegge J.P. Transit peptide cleavage sites of integral thylakoid membrane proteins. Mol Cell Prot 2 (2003) 1068-1085
23. Zolla L., Rinalducci S., and Timperio A.M. Proteomic analysis of photosystem I components from different plant species. Proteomics 7 (2007) 1866-1876
24. Whitelegge J.P., Laganowsky A., Nishio J., Souda P., Zhang H., and Cramer W.A. Sequencing covalent modifications of membrane proteins. J Expt Bot 57 (2006) 1515-1522
25. Arteca R.N., and Arteca J.M. A novel method for growing Arabidopsis thaliana plants hydroponically. Physiol Plant 108 (2000) 188-193
26. 3 buffer system for studying the Fe efficiency response in Sugar Beet (Beta vulgaris L.). J Plant Nutr 23 (2000) 741-757
27. Nishio J.N., and Whitmarsh J. Dissipation of the proton electrochemical potential in intact and lysed chloroplasts. I. The electrical potential. Plant Physiol 95 (1991) 522-528
28. Lichtenthaler H.K. Chlorophylls and carotenoids, the pigments of photosynthetic biomembranes. In: Douce R., and Packer L. (Eds). Methods Enzymol. vol. 148 (1987), Academic Press Inc., New York 350-382
29. Nishio J.N., Abadía J., and Terry N. Chlorophyll-proteins and electron transport during iron-nutrition mediated chloroplast development. Plant Physiol l78 (1985) 296-299
30. 6f complex from spinach and the cyanobacterium, M. laminosus. Mol Cell Prot 1 (2002) 816-827
31. Whitelegge J.P., le Coutre J., Lee J.C., Engel C.K., Privé G.G., Faull K.F., et al. Toward the bilayer proteome, electro-spray-ionization mass spectrometry of large intact transmembrane proteins. Proc Natl Acad Sci USA 96 (1999) 10695-10698
32. Saleeba J.A., and Guerinot M.L. Induction of ferric reductase activity in response to iron deficiency in Arabidopsis. Biometals 8 (1995) 297-300
33. Moog P.R., van der Kooij T.A.W., Bruggemann W., Schiefelbein J.W., and Kuiper P.J.C. Responses to iron deficiency in Arabidopsis thaliana: the turbo iron reductase does not depend on the formation of root hairs and transfer cells. Planta 195 (1995) 505-513
34. Susín S., Albián J., Sánchez-Baeza F., Peleato M.L., Abadía A., Gelpí E., et al. Riboflavin 3′- and 5′-sulfate, two novel flavins accumulating in the roots of iron-deficient sugar beet (Beta vulgaris). J Biol Chem 268 (1993) 20958-20965
35. Abadía J. Leaf responses to Fe deficiency. A review. J Plant Nutr 15 (1992) 1699-1713
36. Nishio J.N., Taylor S.E., and Terry N. Changes in thylakoid galactolipids and proteins during iron nutrition-mediated chloroplast development. Plant Physiol 77 (1985) 705-711
37. Kiss A.Z., Ruban A.V., and Horton P. The PsbS protein controls the organization of the photosystem II antenna in higher plant thylakoid membranes. J Biol Chem 283 (2008) 3972-3978
38. Anwaruzzaman M., Chin B.L., Li X.P., Lohr M., Martinez D.A., and Niyoqi K.K. Genomic analysis of mutants affecting xanthopyhll biosynthesis and regulation of photosynthetic light harvesting in Chlamydomonas reinhardtii. Photosynth Res 82 (2004) 265-276
39. Sugimoto I., and Takahashi Y. Evidence that the PsbK polypeptide is associated with the photosystem II core antenna complex CP43. J Biol Chem 278 (2003) 45004-45010
40. Ohnishi N., and Takahashi Y. Chloroplast-encoded PsbT is required for efficient biogenesis of photosystem II complex in the green alga Chlamydomonas reinhardtii. Photosynth Res 98 (2008) 315-322
41. Ohnishi N., Kashino Y., Satoh K., Ozawa S., and Takahashi Y. Chloroplast-encoded polypeptide PsbT is involved in the repair of primary electron acceptor QA of photosystem II during photoinhibition in Chlamydomonas reinhardtii. J Biol Chem 282 (2007) 7107-7115
42. Singh A.K., and Sherman L.A. Reflections on the function of IsiA, a cyanobacterial stress-inducible, Chl-binding protein. Photosynth Res 93 (2007) 17-25
43. Timperio A.M., D'Amic G.M., Barta C., Loreto F., and Zolla L. Proteomics, pigment composition, and organization of thylakoid membranes in iron-deficient spinach leaves. J Exp Bot 58 (2007) 3695-3710
44. Iwai M., Katayama M., and Ikeuchi M. Absence of the psbH gene product destabilizes the Photosystem II complex and prevents association of the Photosystem II-X protein in the thermophilic cyanobacterium Thermosynechococcus elongatus BP-1. Photosynth Res 87 (2006) 313-322
45. Mayes S.R., Dubbs J.M., Vass I., Hideg E., Nagy L., and Barber J. Further characterization of the psbH locus of Synechocystis sp. PCC 6803: inactivation of the psbH impairs QA to QB electron transport in photosystem 2. Biochemistry 32 (1993) 1454-1465
46. Summer E.J., Schmid V.H., Bruns B.U., and Schmidt G.W. Requirement for the H phosphoprotein in photosystem II of Chlamydomonas reinhardtii. Plant Physiol 113 (1997) 1359-1368
47. Carlberg I., and Anderson B. Phosphatase activities in spinach thylakoid membranes-effectores, regulation and location. Photosynth Res 47 (1996) 145-156
48. Funk C., Schröder W.P., Napiwotzki A., Tjus S.E., Renger G., and Andersson B. The PSII-S protein of higher plants: a new type of pigment-binding protein. Biochemistry 34 (1995) 11133-11141
49. Peterson R.B., and Havir E.A. Photosynthetic properties of Arabidopsis thaliana mutant possessing a defective PsbS gene. Planta 214 (2001) 142-152
50. Li X., Muller-Moule P., Glimore A.M., and Niyogi K.K. PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition. Proc Natl Acad Sci USA 99 (2002) 15222-15227
51. Naver H., Haldrup A., and Scheller H.V. Cosuppression of photosystem I subunit PSI-H in Arabidopsis thaliana. J Biol Chem 274 (1999) 10784-10789
52. Chitnis V.P., and Chitnis P.R. PsaL subunit is required for the formation of photosystem I trimers in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett 336 (1993) 330-334
53. Fromme P., Jordan P., and Krauβ N. Structure of photosystem I. Biochim Biophys Acta 1507 (2001) 5-31
54. Chitnis V.P., Ke A., and Chitnis P.R. The PsaD subunit of photosystem I. Mutations in the basic domain reduce the levels of PsaD in the membranes. Plant Physiol 115 (1997) 1699-1705
55. Lotan C., Cohen Y., Michaeli D., and Nechushtai R. High levels of photosystem I subunit II (PsaD) mRNA result in the accumulation of the PSAD polypeptide only in the presence of light. J Biol Chem 268 (1993) 16185-16489
56. Naumann B., Busch A., Allmer J., Ostendorf E., Zeller M., Kirchhoff H., et al. Comparative quantitative proteomics to investigate the remodeling of bioenergetic pathways under iron deficiency in Chalmydomonas reinhardtii. Proteomics 7 (2007) 3964-3979
57. Ihnatowicz A., Pesaresi P., Varotto C., Richly E., Schneider A., Jahns P., et al. Mutants for photosystem I subunit D of Arabidopsis thaliana: effects on photosynthesis, photosystem I stability and expression of nuclear genes for chloroplast functions. Plant J 37 (2004) 839-852
58. Joyard J., Teyssier E., Miege C., Berny-Seigneurin D., Marechal E., Block M.A., et al. The biochemical machinery of plastid envelope membranes. Plant Physiol 118 (1998) 715-723
59. Winder T.L., and Nishio J.N. Early iron deficiency stress response in leaves of sugar beet. Plant Physiol 108 (1995) 1487-1494
60. Cottrelle P., Cool M., Thuriaux P., Prive V., Theile D., Buhler J., et al. Either one of the two yeast EF-1a genes if required for cell viability. Curr Genet 9 (1985) 693-697
61. Song J.M., Picologlou S., Grant C.M., Firoozan M., Tuite M.F., and Liebman S. Elongation factor EF-1a gene dosage alters translational fidelity in Saccharomyces cerevisiae. Mol Cell Biol 9 (1989) 4571-4575
62. Nishio J.N., and Terry N. Iron nutrition-mediated chloroplast development. Plant Physiol 71 (1983) 688-691
63. Arulanantham A.R., Rao I.M., and Terry N. Limiting factors in photosynthesis. VI. Regeneration of Ribulose-1,5-Bisphosphate limits photosynthesis at low photochemical capacity. Plant Physiol 93 (1989) 1466-1475
64. Andaluz S., Lopez-Millan A., Rivas J., Aro E.M., Abadía J., and Abadía A. Proteomic profiles of thylakoid membranes and changes in response to iron deficiency. Photosynth Res 89 (2006) 141-155
65. Murgia I., Tarantino D., Vannini C., Bracale M., Carravieri S., and Soave C. Arabidopsis thaliana plants overexpressing thylakoidal ascorbate peroxidase show increased resistance to Paraquat-induced photooxdative stress and to nitric oxide-induced cell death. Plant J 38 (2004) 940-953
66. Krieger-Liszkay A. Singlet oxygen production in photosynthesis. J Exp Bot 56 (2005) 337-346
67. 2 in chloroplasts of Arabidopsis thaliana overexpressing glycolate oxidase as an inducible system to study oxidative stress. Plant Physiol 10 (2008) 1104:108.126789
68. König J., Baier M., Horling F., Kahmann U., Harris G., Schürmann, et al. The plant-specific function of 2-Cys peroxiredoxin-mediated detoxification of peroxides in the redox-heirarchy of photosynthetic electron flux. Proc Natl Acad Sci USA 8 (2002) 5738-5743
69. Lamkemeyer P., Laxa M., Collin V., Li W., Finkemeier I., Schöttler M.A., et al. Peroxiredoxin Q of Arabidopsis thaliana is attached to the thylakoids and functions in context of photosynthesis. Plant J 45 (2006) 968-981
70. Jing L., Chen S., Guo X., Zhang H., and Zhao Y. Overexpression of a chloroplast-located peroxiredoxin Q gene, ssPrxQ, increases the salt and low-temperature tolerance of Arabidopsis. J Integrat Plant Biol 48 (2006) 1244-1249
71. Pérez-Ruiz J.M., Spínola M.C., Kirchsteiger K., Moreno J., Sahrawy M., and Cejudo F.J. Rice NTRC is a high-efficiency redox system for chloroplast protection against oxidative damage. Plant Cell 18 (2006) 2356-2368
72. Pushnik J.C., and Miller G.W. The effect of iron and light treatment on chloroplast composition and ultrastructure in iron-deficient barley leaves. J Plant Nutr 5 (1982) 311-321
73. Eberhard S., Finazzi G., and Wollman F.A. The dynamics of photosynthesis. Annu Rev Genet 42 (2008) 463-515
74. Boardman K., and Highkin H.R. Studies on a barley mutant lacking chlorophyll b. Photochemical activity of isolated chloroplasts. Biochim Biophys Acta 126 (1966) 189-199
75. Thornber J.P., and Highkin H.R. Composition of the photosynthetic apparatus of normal barley leaves and a mutant lacking chlorophyll b. Eur J Biochem 41 (1974) 109-116
76. Waldron G.C., and Anderson J.M. Chlorophyll-protein complexes from thylakoids of a mutant barley lacking chlorophyll b. Eur J Biochem 102 (1979) 357-362
77. Bellemare G., Bartlett S.G., and Chua N. Biosynthesis of chlorophyll a/b-binding polypeptides in wild type and the chlorina f2 mutant of barley. J Biol Chem 257 (1982) 7762-7767
78. Preiss S., and Thornber J.P. Stability of the apoproteins of light-harvesting complex I and II during biogenesis of thylakoids in the chlorophyll b-less barley mutant chlorina f2. Plant Physiol 107 (1995) 709-717
79. Darr S.C., Somerville S.C., and Arntzen C.J. Monoclonal antibodies to the light-harvesting chlorophyll a/b protein complex of photosystem II. J Cell Biol 103 (1986) 163-172
80. Harrison M.A., and Melis A. Organization and stability of polypeptides associated with the chlorophyll a-b light-harvesting complex of photosystem-II. Plant Cell Physiol 33 (1992) 627-637
81. Peter G.F., and Thornber J.P. Biochemical composition and organization of higher plant photosystem II light-harvesting pigment-proteins. J Biol Chem 266 (1991) 16745-16754
82. White M.J., and Green B.R. Intermittent-light chloroplasts are not developmentally equivalent to chlorina f2 chloroplasts in barley. Photosynth Res 15 (1988) 195-203
83. Baker N.R., Webber A.N., Bradbury M., Markwell J.P., BAker M.G., and Thornber J.P. Development of photochemical competence during the growth of the wheat leaf. UCLA Symp Mol Cell Biol New Ser 14 (1984) 237-255
84. Dreyfuss B.W., and Thornber J.P. Assembly of the light-harvesting complexes (LHCs) of photosystem II: Monomeric LHC Ilb complexes are intermediates in the formation of oligomeric LHC Ilb complexes. Plant Physiol 106 (1994) 829-839
85. Dreyfuss B.W., and Thornber J.P. Organization of the light-harvesting complex of photosystem I and its assembly during plastid development. Plant Physiol 106 (1994) 841-848
86. Hörtensteiner S., and Feller U. Nitrogen metabolism and remobilization during senescence. J Exp Bot 53 (2002) 927-937
87. Rosiak-Figielek B., and Jackowski G. The disappearance kinetics of Lhcb polypeptides during dark-induced senescence of leaves. Aust J Plant Physiol 27 (2000) 245-251
88. Jackowski G., and Elisko A. Lhca polypeptides are maintained during dark-induced senescence of leaves. Acta Physiol Plant 23 (2001) 437-442
89. Thomas H., and Howarth C.J. Five ways to stay green. J Exp Bot 51 (2001) 329-337
90. Lu C., Lu Q., Zhang J., and Kuang T. Characterization of photosynthetic pigment composition, photosystem II photochemistry and thermal energy dissipation during leaf senescence of wheat plants grown in the field. J Exp Bot 52 (2001) 1805-1810
91. Humbeck K., and Krupinska K. The abundance of minor chlorophyll a/b-binding proteins CP29 and LHCI of barley (Hordeum vulgare L.) during leaf senescence is controlled by light. J Exp Bot 54 (2003) 375-383
92. Morales F., Abadía A., and Abadía J. Characterization of the xanthophyll cycle and other photosynthetic pigment changes induced by iron deficiency in sugar beet (Beta vulgaris L.). Plant Physiol 94 (1990) 607-613
93. Lee A.I.c., and Thornber J.P. Analysis of the pigment stoichiometry of pigment-protein complexes from barley (Hordeum vulgare): the xanthophyll cycle intermediates occur mainly in the light-harvesting complexes of photosystem I and photosystem II. Plant Physiol 107 (1995) 565-574
94. Yamamoto H.Y., and Bassi R. Carotenoids: localization and function. In: Ort D.R., and Yocum C.F. (Eds). Oxygenic Photosynthesis: The Light Reactions (1996), Kluwer Academic Publishers, Dordrecht 539-563
95. Kim S., Sandusky P., Bowlby N.R., Aebersold R., Green B.R., Vlahakis S., et al. Characterization of a spinach psbS cDNA encoding the 22 kDa protein of photosystem II. FEBS Lett 314 (1992) 67-71
96. Wedel N., Kelin R., Ljungberg U., Andersson B., and Herrmann R.G. The single-copy gene psbS codes for a phylogeneteically intriguing 22 kDa polypeptide of photosystem II. FEBS Lett 314 (1992) 61-66
97. Aspinall-O'Dea M., Wentworth M., Pascal A., Robert B., Ruban A., and Horton P. In vitro reconstitution of the activated zeaxanthin state associated with energy dissipation in plants. Proc Natl Acad Sci USA 99 (2002) 16331-16335
98. Li X.P., Gilmore A.M., Caffarri S., Bassi R., Golan T., Kramer D., et al. Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein. J Biol Chem 279 (2004) 22866-22874
99. Niyogi K.K., Li X.P., Rosenberg V., and Jung H.S. Is PsbS the site of non-photochemical quenching in photosynthesis?. J Exp Bot 58 (2004) 375-382
100. Gómez S.M., and Chitnis P.R. Light-harvesting antennas in plants. In: Yunus M., Pathre U., and Mohanty P. (Eds). Probing photosynthesis: mechanisms, regulation and adaptation (2000), Taylor and Francis, London 51-69
101. Green B.R., Pichersky E., and Kloppstech K. Chlorophyll a/b-binding proteins: an extended family. Trends Biochem Sci 16 (1991) 181-186
102. Thornber J.P., Cogdell R.J., Chitnis P.R., Morishige D.T., Peter G.F., Gómez S.M., et al. Antenna pigment-protein complexes of higher plants and purple bacteria. In: Bittar E.E., and Barber J. (Eds). Advances in Molecular and Cell Biology Vol. 10: Molecular Processes of Photosynthesis (1994), JAI Press, Greenwich, Conn 55-118
103. Maiwald D., Dietzmann A., Jahns P., Pesaresi P., Joliot P., Joliot A., et al. Knock-out of the genes coding for the Rieske protein and the ATP-synthase delta-subunit of Arabidopsis. Effects on photosynthesis, thylakoid protein composition, and nuclear chloroplast gene expression. Plant Physiol 133 (2003) 191-202
104. Friso G., Giacomelli L., Ytterburg A.J., Pelteir J.B., Rudella A., Sun Q., et al. In-depth analysis of the thylakoid membrane proteome of Arabidopsis thaliana chloroplasts; new proteins, new functions and a plastid proteome database. Plant Cell 16 (2004) 478-499
105. Kim S.A., and Guerinot M.L. Mining iron: iron uptake and transport in plants. FEBS Letters 581 (2007) 2273-2280
106. Jeong J., Cohu C., Kerkeb L., Pilon M., Connolly E.L., and Guerinot M.L. Chloroplast Fe(III) chelate reductase activity is essential for seedling viability under iron limiting conditions. Proc Nat Acad Sci 105 (2008) 10619-10624
107. Walker E.L., and Connolly E.L. Time to pump iron: iron-deficiency-signaling mechanisms of higher plants. Cur Opin Plant Biol 11 (2008) 530-535