Quantitative transcriptomic analysis of abscisic acid-induced and reactive oxygen species-dependent expression changes and proteomic profiling in Arabidopsis suspension cells

Plant Journal

Volumn 67, Issue 1, 2011, Pages 105-118

  Böhmer, Maik ^a   Schroeder, Julian I ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

abscisic acid; quantitative proteomics; reactive oxygen species

Indexed keywords

ABA SIGNALING; ABA-INDUCED GENES; ABSCISIC ACID; ARABIDOPSIS; DATA SETS; DIMETHYLTHIOUREA; EXTRACELLULAR; GLUCOSINOLATES; MARKER GENES; PROTEIN LEVEL; PROTEOMIC PROFILING; QUANTITATIVE PROTEOMICS; RAPID CHANGES; REACTIVE OXYGEN; REACTIVE OXYGEN SPECIES; SUSPENSION CELL; TRANSCRIPT LEVEL;

GENES; MOLECULAR BIOLOGY; OXYGEN; SUSPENSIONS (FLUIDS);

PROTEINS;

1,3-DIMETHYLTHIOUREA; ABSCISIC ACID; ARABIDOPSIS PROTEIN; DIMETHYLTHIOUREA; DRUG DERIVATIVE; GLUCOSINOLATE; MESSENGER RNA; PHYTOHORMONE; PLANT RNA; PROTEIN SERINE THREONINE KINASE; REACTIVE OXYGEN METABOLITE; SNRK2 PROTEIN, ARABIDOPSIS; THIOUREA;

ARABIDOPSIS; ARTICLE; CULTURE TECHNIQUE; DNA MICROARRAY; DRUG EFFECT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; METHODOLOGY; MUTATION; PROTEOMICS; RESPIRATORY BURST; SIGNAL TRANSDUCTION;

ABSCISIC ACID; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL CULTURE TECHNIQUES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GLUCOSINOLATES; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLANT GROWTH REGULATORS; PROTEIN-SERINE-THREONINE KINASES; PROTEOMICS; REACTIVE OXYGEN SPECIES; RESPIRATORY BURST; RNA, MESSENGER; RNA, PLANT; SIGNAL TRANSDUCTION; THIOUREA;

ARABIDOPSIS;

EID: 79959744765     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2011.04579.x     Document Type: Article

References (74)

1. Ache, P., Becker, D., Ivashikina, N., Dietrich, P., Roelfsema, M.R., and, Hedrich, R., (2000) GORK, a delayed outward rectifier expressed in guard cells of Arabidopsis thaliana, is a K(+)-selective, K(+)-sensing ion channel. FEBS Lett. 486, 93-98.
2. Axelos, M., (1992) A protocol for transient gene expression in Arabidopsis thaliana protoplasts isolated from cell suspension cultures. Plant Physiol. Biochem. 30, 123.
3. Bartling, D., Seedorf, M., Mithöfer, A., and, Weiler, E.W., (1992) Cloning and expression of an Arabidopsis nitrilase which can convert indole-3-acetonitrile to the plant hormone, indole-3-acetic acid. Eur. J. Biochem. 205, 417-424.
4. Bonaldi, T., Straub, T., Cox, J., Kumar, C., Becker, P.B., and, Mann, M., (2008) Combined use of RNAi and quantitative proteomics to study gene function in Drosophila. Mol. Cell, 31, 762-772.
5. Brault, M., Amiar, Z., Pennarun, A.M., Monestiez, M., Zhang, Z.S., Cornel, D., Dellis, O., Knight, H., Bouteau, F.O., and, Rona, J.P., (2004) Plasma membrane depolarization induced by abscisic acid in Arabidopsis suspension cells involves reduction of proton pumping in addition to anion channel activation, which are both Ca2+ dependent. Plant Physiol. 135, 231-243. (Pubitemid 38653671)
6. Chen, Y., Hoehenwarter, W., and, Weckwerth, W., (2010) Comparative analysis of phytohormone-responsive phosphoproteins in Arabidopsis thaliana using TiO2-phosphopeptide enrichment and mass accuracy precursor alignment. Plant J. 63, 1-17.
7. Christie, P.J., Alfenito, M.R., and, Walbot, V., (1994) Impact of low-temperature stress on general phenylpropanoid and anthocyanin pathways: enhancement of transcript abundance and anthocyanin pigmentation in maize seedlings. Planta, 194, 541-549. (Pubitemid 2145719)
8. Cutler, S.R., Rodriguez, P.L., Finkelstein, R.R., and, Abrams, S.R., (2010) Abscisic acid: emergence of a core signaling network. Annu. Rev. Plant Biol. 61, 651-679.
9. Falk, K.L., Tokuhisa, J.G., and, Gershenzon, J., (2007) The effect of sulfur nutrition on plant glucosinolate content: physiology and molecular mechanisms. Plant Biol. 9, 573-581. (Pubitemid 47507819)
10. Finkelstein, R., and, Somerville, C., (1989) Abscisic acid or high osmoticum promote accumulation of long-chain fatty acids in developing embryos of Brassica napus. Plant Sci. 61, 213-217.
11. Fujii, H., and, Zhu, J.K., (2009) Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress. Proc. Natl Acad. Sci. USA, 106, 8380-8385.
12. Fujita, Y., Nakashima, K., Yoshida, T., et al. (2009) Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis. Plant Cell Physiol. 50, 2123-2132.
13. Geiger, D., Scherzer, S., Mumm, P., et al. (2009) Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair. Proc. Natl Acad. Sci. USA, 106, 21425-21430.
14. Ghelis, T., Dellis, O., Jeannette, E., Bardat, F., Cornel, D., Miginiac, E., Rona, J.P., and, Sotta, B., (2000) Abscissic acid specific expression of RAB18 involves activation of anion channels in Arabidopsis thaliana suspension cells. FEBS Lett. 474, 43-47. (Pubitemid 30320829)
15. Grimplet, J., Deluc, L., Tillett, R., Wheatley, M., Schlauch, K., Cramer, G., and, Cushman, J., (2007) Tissue-specific mRNA expression profiling in grape berry tissues. BMC Genomics, 8, 187.
16. Gygi, S.P., Rist, B., Gerber, S.A., Turecek, F., Gelb, M.H., and, Aebersold, R., (1999) Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat. Biotechnol. 17, 994-999. (Pubitemid 29474856)
17. Hancock, J.T., and, Jones, O.T., (1987) The inhibition by diphenyleneiodonium and its analogues of superoxide generation by macrophages. Biochem. J. 242, 103-107. (Pubitemid 17015451)
18. + channel GORK is involved in regulation of stomatal movements and plant transpiration. Proc. Natl Acad. Sci. USA, 100, 5549-5554. (Pubitemid 36542742)
19. Hoth, S., Morgante, M., Sanchez, J.-P., Hanafey, M.K., Tingey, S.V., and, Chua, N.-H., (2002) Genome-wide gene expression profiling in Arabidopsis thaliana reveals new targets of abscisic acid and largely impaired gene regulation in the abi1-1 mutant. J. Cell Sci. 115, 4891-4900. (Pubitemid 36054641)
20. Huang da, W., Sherman, B.T., and, Lempicki, R.A., (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57.
21. Islam, M.M., Tani, C., Watanabe-Sugimoto, M., Uraji, M., Jahan, M.S., Masuda, C., Nakamura, Y., Mori, I.C., and, Murata, Y., (2009) Myrosinases, TGG1 and TGG2 redundantly function in ABA and MeJA signaling in Arabidopsis guard cells. Plant Cell Physiol. 50, 1171-1175.
22. Janowitz, T., Trompetter, I., and, Piotrowski, M., (2009) Evolution of nitrilases in glucosinolate-containing plants. Phytochemistry, 70, 1680-1686.
23. Keller, A., Eng, J., Zhang, N., Li, X.J., and, Aebersold, R., (2005) A uniform proteomics MS/MS analysis platform utilizing open XML file formats. Mol. Syst. Biol. 1, 2005.0017.
24. 2+ signalling. Annu. Rev. Plant Biol. 61, 13.1-13.31.
25. Kline, K.G., Barrett-Wilt, G.A., and, Sussman, M.R., (2010) In planta changes in protein phosphorylation induced by the plant hormone abscisic acid. Proc. Natl Acad. Sci. USA, 107, 15986-15991.
26. Kobayashi, M., Ohura, I., Kawakita, K., Yokota, N., Fujiwara, M., Shimamoto, K., Doke, N., and, Yoshioka, H., (2007) Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell, 19, 1065-1080. (Pubitemid 46953247)
27. Kwak, J.M., Murata, Y., Baizabal-Aguirre, V.M., Merrill, J., Wang, M., Kemper, A., Hawke, S.D., Tallman, G., and, Schroeder, J.I., (2001) Dominant negative guard cell K+ channel mutants reduce inward-rectifying K+ currents and light-induced stomatal opening in arabidopsis. Plant Physiol. 127, 473-485. (Pubitemid 32996750)
28. Kwak, J.M., Mori, I.C., Pei, Z.M., Leonhardt, N., Torres, M.A., Dangl, J.L., Bloom, R.E., Bodde, S., Jones, J.D., and, Schroeder, J.I., (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J. 22, 2623-2633. (Pubitemid 36712360)
29. Lahm, H.W., and, Langen, H., (2000) Mass spectrometry: a tool for the identification of proteins separated by gels. Electrophoresis, 21, 2105-2114. (Pubitemid 30435810)
30. Lee, S.C., Lan, W., Buchanan, B.B., and, Luan, S., (2009) A protein kinase-phosphatase pair interacts with an ion channel to regulate ABA signaling in plant guard cells. Proc. Natl Acad. Sci. USA, 106, 21419-21424.
31. Leonhardt, N., Kwak, J.M., Robert, N., Waner, D., Leonhardt, G., and, Schroeder, J.I., (2004) Microarray expression analyses of Arabidopsis guard cells and isolation of a recessive abscisic acid hypersensitive protein phosphatase 2C mutant. Plant Cell, 16, 596-615. (Pubitemid 38335273)
32. Li, Y., Lee, K.K., Walsh, S., Smith, C., Hadingham, S., Sorefan, K., Cawley, G., and, Bevan, M.W., (2006) Establishing glucose- and ABA-regulated transcription networks in Arabidopsis by microarray analysis and promoter classification using a relevance vector machine. Genome Res. 16, 414-427. (Pubitemid 43327511)
33. Lohse, M., Nunes-Nesi, A., Kruger, P., et al. (2010) Robin: an intuitive wizard application for R-based expression microarray quality assessment and analysis. Plant Physiol. 153, 642-651.
34. Ma, Y., Szostkiewicz, I., Korte, A., Moes, D., Yang, Y., Christmann, A., and, Grill, E., (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science, 324, 1064-1068.
35. Meyer, S., Mumm, P., Imes, D., Endler, A., Weder, B., Al-Rasheid, K.A.S., Geiger, D., Marten, I., Martionia, E., and, Hedrich, R., (2010) ATALMT12 represents an R-type anion channel required for stomatal movement in Arabidopsis guard cells. Plant J. 63, 1054-1062.
36. Miao, Y., Lv, D., Wang, P., Wang, X.-C., Chen, J., Miao, C., and, Song, C.-P., (2006) An Arabidopsis glutathione peroxidase functions as both a redox transducer and a scavenger in abscisic acid and drought stress responses. Plant Cell, 18, 2749-2766. (Pubitemid 44749901)
37. 2+ permeable channels and stomatal closure. PLoS Biol. 4, e327.
38. 2+ channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1-1 and abi2-1 protein phosphatase 2C mutants. Plant Cell, 13, 2513-2523. (Pubitemid 33146113)
39. Mustilli, A.C., Merlot, S., Vavasseur, A., Fenzi, F., and, Giraudat, J., (2002) Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell, 14, 3089-3099. (Pubitemid 36029134)
40. Nakashima, K., Fujita, Y., Kanamori, N., et al. (2009) Three Arabidopsis SnRK2 protein kinases, SRK2D/SnRK2.2, SRK2E/SnRK2.6/OST1 and SRK2I/SnRK2.3, involved in ABA signaling are essential for the control of seed development and dormancy. Plant Cell Physiol. 50, 1345-1363.
41. Nesvizhskii, A.I., Keller, A., Kolker, E., and, Aebersold, R., (2003) A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 75, 4646-4658. (Pubitemid 37082259)
42. Nishimura, N., Sarkeshik, A., Nito, K., et al. (2010) PYR/PYL/RCAR family members are major in-vivo ABI1 protein phosphatase 2C-interacting proteins in Arabidopsis. Plant J. 61, 290-299.
43. O'Brien, R.N., Shen, Z., Tachikawa, K., Lee, P.J., and, Briggs, S.P., (2010) Quantitative proteome analysis of pluripotent cells by iTRAQ mass tagging reveals post-transcriptional regulation of proteins required for ES cell self-renewal. Mol. Cell Proteomics, 9, 2238-2251.
44. Oda, Y., Huang, K., Cross, F.R., Cowburn, D., and, Chait, B.T., (1999) Accurate quantitation of protein expression and site-specific phosphorylation. Proc. Natl Acad. Sci. USA, 96, 6591-6596. (Pubitemid 29274927)
45. Okamoto, M., Tatematsu, K., Matsui, A., et al. (2010) Genome-wide analysis of endogenous abscisic acid-mediated transcription in dry and imbibed seeds of Arabidopsis using tiling arrays. Plant J. 62, 39-51.
46. Park, S.Y., Fung, P., Nishimura, N., et al. (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science, 324, 1068-1071.
47. Pei, Z.M., Murata, Y., Benning, G., Thomine, S., Klüsener, B., Allen, G.J., Grill, E., and, Schroeder, J.I., (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature, 406, 731-734.
48. Raghavendra, A.S., Gonugunta, V.K., Christmann, A., and, Grill, E., (2010) ABA perception and signalling. Trends Plant Sci. 15, 395-401.
49. Ramakers, C., Ruijter, J.M., Deprez, R.H., and, Moorman, A.F., (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci. Lett. 339, 62-66. (Pubitemid 36263221)
50. Romeis, T., Piedras, P., Zhang, S., Klessig, D.F., Hirt, H., and, Jones, J.D., (1999) Rapid Avr9- and Cf-9 -dependent activation of MAP kinases in tobacco cell cultures and leaves: convergence of resistance gene, elicitor, wound, and salicylate responses. Plant Cell, 11, 273-287.
51. Ross, P.L., Huang, Y.N., Marchese, J.N., et al. (2004) Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol. Cell Proteomics, 3, 1154-1169.
52. Rubio, S., Rodrigues, A., Saez, A., Dizon, M.B., Galle, A., Kim, T.H., Santiago, J., Flexas, J., Schroeder, J.I., and, Rodriguez, P.L., (2009) Triple loss of function of protein phosphatases type 2C leads to partial constitutive response to endogenous abscisic acid. Plant Physiol. 150, 1345-1355.
53. Santiago, J., Rodrigues, A., Saez, A., Rubio, S., Antoni, R., Dupeux, F., Park, S.Y., Marquez, J.A., Cutler, S.R., and, Rodriguez, P.L., (2009) Modulation of drought resistance by the abscisic acid receptor PYL5 through inhibition of clade A PP2Cs. Plant J. 60, 575-588.
54. Sasaki, T., Mori, I.C., Furuichi, T., Munemasa, S., Toyooka, K., Matsuoka, K., Murata, Y., and, Yamamoto, Y., (2010) Closing plant stomata requires a homolog of an aluminum-activated malate transporter. Plant Cell Physiol. 51, 354-365.
55. Seki, M., Ishida, J., Narusaka, M., et al. (2002) Monitoring the expression pattern of around 7,000 Arabidopsis genes under ABA treatments using a full-length cDNA microarray. Funct. Integr. Genomics, 2, 301.
56. Sirichandra, C., Gu, D., Hu, H.C., et al. (2009) Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase. FEBS Lett. 583, 2982-2986.
57. Suhita, D., Raghavendra, A.S., Kwak, J.M., and, Vavasseur, A., (2004) Cytoplasmic alkalization precedes reactive oxygen species production during methyl jasmonate- and abscisic acid-induced stomatal closure. Plant Physiol. 134, 1536-1545. (Pubitemid 38527363)
58. ++dependent protein kinase. Biochem. Biophys. Res. Commun. 135, 397-402. (Pubitemid 16049425)
59. Tate, R.M., Vanbenthuysen, K.M., Shasby, D.M., McMurtry, I.F., and, Repine, J.E., (1982) Oxygen-radical-mediated permeability edema and vasoconstriction in isolated perfused rabbit lungs. Am. Rev. Respir. Dis. 126, 802-806. (Pubitemid 13241060)
60. Thimm, O., Blasing, O., Gibon, Y., Nagel, A., Meyer, S., Kruger, P., Selbig, J., Muller, L.A., Rhee, S.Y., and, Stitt, M., (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J. 37, 914-939. (Pubitemid 38370342)
61. Tokimatsu, T., Sakurai, N., Suzuki, H., Ohta, H., Nishitani, K., Koyama, T., Umezawa, T., Misawa, N., Saito, K., and, Shibata, D., (2005) KaPPA-view: a web-based analysis tool for integration of transcript and metabolite data on plant metabolic pathway maps. Plant Physiol. 138, 1289-1300. (Pubitemid 43142077)
62. Trouverie, J., Vidal, G., Zhang, Z., Sirichandra, C., Madiona, K., Amiar, Z., Prioul, J.L., Jeannette, E., Rona, J.P., and, Brault, M., (2008) Anion channel activation and proton pumping inhibition involved in the plasma membrane depolarization induced by ABA in Arabidopsis thaliana suspension cells are both ROS dependent. Plant Cell Physiol. 49, 1495-1507.
63. Umezawa, T., Sugiyama, N., Mizoguchi, M., Hayashi, S., Myouga, F., Yamaguchi-Shinozaki, K., Ishihama, Y., Hirayama, T., and, Shinozaki, K., (2009) Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis. Proc. Natl Acad. Sci. USA, 106, 17588-17593.
64. Vahisalu, T., Puzorjova, I., Brosche, M., et al. (2010) Ozone-triggered rapid stomatal response involves the production of reactive oxygen species, and is controlled by SLAC1 and OST1. Plant J. 62, 442-453.
65. Vlad, F., Rubio, S., Rodrigues, A., Sirichandra, C., Belin, C., Robert, N., Leung, J., Rodriguez, P.L., Lauriere, C., and, Merlot, S., (2009) Protein phosphatases 2C regulate the activation of the Snf1-related kinase OST1 by abscisic acid in Arabidopsis. Plant Cell, 21, 3170-3184.
66. Vorwerk, S., Biernacki, S., Hillebrand, H., Janzik, I., Muller, A., Weiler, E.W., and, Piotrowski, M., (2001) Enzymatic characterization of the recombinant Arabidopsis thaliana nitrilase subfamily encoded by the NIT2/NIT1/NIT3-gene cluster. Planta, 212, 508-516. (Pubitemid 32235428)
67. Wang, W., Scali, M., Vignani, R., Spadafora, A., Sensi, E., Mazzuca, S., and, Cresti, M., (2003) Protein extraction for two-dimensional electrophoresis from olive leaf, a plant tissue containing high levels of interfering compounds. Electrophoresis, 24, 2369-2375. (Pubitemid 38089022)
68. Yang, Y., Costa, A., Leonhardt, N., Siegel, R.S., and, Schroeder, J.I., (2008) Isolation of a strong Arabidopsis guard cell promoter and its potential as a research tool. Plant Methods, 4, 6.
69. Yoshida, R., Hobo, T., Ichimura, K., Mizoguchi, T., Takahashi, F., Aronso, J., Ecker, J.R., and, Shinozaki, K., (2002) ABA-activated SnRK2 protein kinase is required for dehydration stress signaling in Arabidopsis. Plant Cell Physiol. 43, 1473-1483. (Pubitemid 36100984)
70. Yoshida, R., Umezawa, T., Mizoguchi, T., Takahashi, S., Takahashi, F., and, Shinozaki, K., (2006) The regulatory domain of SRK2E/OST1/SnRK2.6 interacts with ABI1 and integrates abscisic acid (ABA) and osmotic stress signals controlling stomatal closure in Arabidopsis. J. Biol. Chem. 281, 5310-5318. (Pubitemid 43847795)
71. Zalejski, C., Paradis, S., Maldiney, R., Habricot, Y., Miginiac, E., Rona, J.P., and, Jeannette, E., (2006) Induction of abscisic acid-regulated gene expression by diacylglycerol pyrophosphate involves Ca2+ and anion currents in Arabidopsis suspension cells. Plant Physiol. 141, 1555-1562. (Pubitemid 44223304)
72. Zhang, X., Zhang, L., Dong, F., Gao, J., Galbraith, D.W., and, Song, C.P., (2001) Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol. 126, 1438-1448. (Pubitemid 32752373)
73. Zhao, Z., Zhang, W., Stanley, B.A., and, Assmann, S.M., (2008) Functional proteomics of Arabidopsis thaliana guard cells uncovers new stomatal signaling pathways. Plant Cell, 20, 3210-3226.
74. Zhao, Z., Stanley, B.A., Zhang, W., and, Assmann, S.M., (2010) ABA-regulated G protein signaling in Arabidopsis guard cells: a proteomic perspective. J. Proteome Res. 9, 1637-1647.