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Protoplasma

, Volume 253, Issue 2, pp 403–415 | Cite as

Peroxisomal NADP-isocitrate dehydrogenase is required for Arabidopsis stomatal movement

  • Marina Leterrier
  • Juan B. Barroso
  • Raquel Valderrama
  • Juan C. Begara-Morales
  • Beatriz Sánchez-Calvo
  • Mounira Chaki
  • Francisco Luque
  • Benjamin Viñegla
  • José M. Palma
  • Francisco J. CorpasEmail author
Original Article

Abstract

Peroxisomes are subcellular organelles characterized by a simple morphological structure but have a complex biochemical machinery involved in signaling processes through molecules such as hydrogen peroxide (H2O2) and nitric oxide (NO). Nicotinamide adenine dinucleotide phosphate (NADPH) is an essential component in cell redox homeostasis, and its regeneration is critical for reductive biosynthesis and detoxification pathways. Plants have several NADPH-generating dehydrogenases, with NADP-isocitrate dehydrogenase (NADP-ICDH) being one of these enzymes. Arabidopsis contains three genes that encode for cytosolic, mitochondrial/chloroplastic, and peroxisomal NADP-ICDH isozymes although the specific function of each of these remains largely unknown. Using two T-DNA insertion lines of the peroxisomal NADP-ICDH designated as picdh-1 and picdh-2, the data show that the peroxisomal NADP-ICDH is involved in stomatal movements, suggesting that peroxisomes are a new element in the signaling network of guard cells.

Keywords

Nitric oxide Hydrogen peroxide NADP-isocitrate dehydrogenase Peroxisomes Stomata Guard cells 

Notes

Acknowledgments

ML acknowledges a JAE-Doc contract from CSIC. Microscopy analyses were carried out at the Technical Services of the University of Granada and Estación Experimental del Zaidín (CSIC). Special thanks are given to Mr. Carmelo Ruíz-Torres for his excellent technical support. T-DNA insertion mutant seeds were provided by the Nottingham Arabidopsis Stock Centre, UK. This work was supported by ERDF-cofinanced grants from the Ministry of Economy and Competitiveness (BIO2012-33904) and Junta de Andalucía (groups BIO192 and BIO 286).

Conflict of interest

The authors declare that they have no conflict of interests.

Supplementary material

709_2015_819_MOESM1_ESM.ppt (166 kb)
ESM 1 (PPT 165 kb)
709_2015_819_MOESM2_ESM.doc (37 kb)
ESM 2 (DOC 37 kb)

References

  1. Agurla S, Gayatri G, Raghavendra AS (2014) Nitric oxide as a secondary messenger during stomatal closure as a part of plant immunity response against pathogens. Nitric Oxide 43:89–96PubMedCrossRefGoogle Scholar
  2. Allen GJ, Chu SP, Schumacher K, Shimazaki CT, Vafeados D, Kemper A, Hawke SD, Tallman G, Tsien RY, Harper JF, Chory J, Schroeder JI (2000) Alteration of stimulus-specific guard cell calcium oscillations and stomatal closing in Arabidopsis det3 mutant. Science 289:2338–2342PubMedCrossRefGoogle Scholar
  3. An Z, Jing W, Liu Y, Zhang W (2008) Hydrogen peroxide generated by copper amine oxidase is involved in abscisic acid-induced stomatal closure in Vicia faba. J Exp Bot 59(4):815–825PubMedCrossRefGoogle Scholar
  4. Attucci S, Rivoal J, Brouquisse R, Carde JP, Pradet A, Raymond P (1994) Characterization of a mitochondrial NADP-dependent isocitrate dehydrogenase in axes of germinating sunflower seeds. Plant Sci 102:49–59CrossRefGoogle Scholar
  5. Barroso JB, Corpas FJ, Carreras A, Sandalio LM, Valderrama R, Palma JM, Lupiáñez JA, del Río LA (1999) Localization of nitric-oxide synthase in plant peroxisomes. J Biol Chem 274:36729–36733PubMedCrossRefGoogle Scholar
  6. Beevers H (1979) Microbodies in higher-plants. Annu Rev Plant Physiol Plant Mol Biol 30:159–193CrossRefGoogle Scholar
  7. Begara-Morales JC, Chaki M, Sánchez-Calvo B, Mata-Pérez C, Leterrier M, Palma JM, Barroso JB, Corpas FJ (2013) Protein tyrosine nitration in pea roots during development and senescence. J Exp Bot 64(4):1121–1134PubMedPubMedCentralCrossRefGoogle Scholar
  8. Bolwell GP (1999) Role of active oxygen species and NO in plant defence responses. Curr Opin Plant Biol 2:287–294PubMedCrossRefGoogle Scholar
  9. Bright J, Desikan R, Hancock JT, Weir IS, Neill SJ (2006) ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. Plant J 45:113–122PubMedCrossRefGoogle Scholar
  10. Bunkelmann JR, Trelease RN (1996) Ascorbate peroxidase. A prominent membrane protein in oilseed glyoxysomes. Plant Physiol 110:589–598PubMedPubMedCentralCrossRefGoogle Scholar
  11. Canino S, Nieri B, Pistelli L, Alpi A, DeBellis L (1996) NADP-isocitrate dehydrogenase in germinating cucumber cotyledons: purification and characterization of a cytosolic isoenzyme. Physiol Plant 98:13–19CrossRefGoogle Scholar
  12. Chai MF, Wei PC, Chen QJ, An R, Chen J, Yang S, Wang XC (2006) NADK3, a novel cytoplasmic source of NADPH, is required under conditions of oxidative stress and modulates abscisic acid responses in Arabidopsis. Plant J 47:665–674PubMedCrossRefGoogle Scholar
  13. Chen RD (1998) Plant NADP-dependent isocitrate dehydrogenases are predominantly localized in the cytosol. Planta 207:280–285PubMedCrossRefGoogle Scholar
  14. Chen Z, Gallie DR (2004) The ascorbic acid redox state controls guard cell signaling and stomatal movement. Plant Cell 16:1143–1162PubMedPubMedCentralCrossRefGoogle Scholar
  15. Chen R, Lemarechal P, Vidal J, Jacquot JP, Gadal P (1988) Purification and comparative properties of the cytosolic isocitrate dehydrogenases (NADP) from pea (Pisum sativum) roots and green leaves. Eur J Biochem 175:565–572PubMedCrossRefGoogle Scholar
  16. Chen RD, Bismuth E, Champigny ML, Gadal P (1989) Chromatographic and immunological evidence that chloroplastic and cytosolic pea (Pisum sativum) NADP-isocitrate dehydrogenases are distinct isoenzymes. Planta 178:157–163PubMedCrossRefGoogle Scholar
  17. Comstock J, Ehleringer JR (1992) Correlating genetic variation in carbon isotopic composition with complex climatic gradients. Proc Natl Acad Sci U S A 89:7747–7751PubMedPubMedCentralCrossRefGoogle Scholar
  18. Corpas FJ, Barroso JB (2014a) Functional implications of peroxisomal nitric oxide (NO) in plant. Front Plant Sci 5:97PubMedPubMedCentralCrossRefGoogle Scholar
  19. Corpas FJ, Barroso JB (2014b) NADPH-generating dehydrogenases: their role in the mechanism of protection against nitro-oxidative stress induced by adverse environmental conditions. Front Environ Sci 2:55CrossRefGoogle Scholar
  20. Corpas FJ, Barroso JB (2014c) Peroxynitrite (ONOO) is endogenously produced in arabidopsis peroxisomes and is overproduced under cadmium stress. Ann Bot 113(1):87–96PubMedPubMedCentralCrossRefGoogle Scholar
  21. Corpas FJ, Trelease RN (1998) Differential expression of ascorbate peroxidase and a putative molecular chaperone in the boundary membrane of differentiating cucumber seedling peroxisomes. J Plant Physiol 153:332–338CrossRefGoogle Scholar
  22. Corpas FJ, Bunkelmmann J, Trelease RN (1994) Identification and immunocharacterization of a family of peroxisome membrane proteins (PMPs) in oilseed glyoxysomes. Eur J Cell Biol 65:280–290Google Scholar
  23. Corpas FJ, de la Colina C, Sánchez-Rasero F, del Río LA (1997) A role for leaf peroxisomes in the catabolism of purines. J Plant Physiol 151:246–250Google Scholar
  24. Corpas FJ, Barroso JB, Sandalio LM, Palma JM, Lupiáñez JA, del Río LA (1999) Peroxisomal NADP-dependent isocitrate dehydrogenase. Characterization and activity regulation during natural senescence. Plant Physiol 121:921–928PubMedPubMedCentralCrossRefGoogle Scholar
  25. Corpas FJ, Hayashi M, Mano S, Nishimura M, Barroso JB (2009) Peroxisomes are required for in vivo nitric oxide accumulation in the cytosol following salinity stress of Arabidopsis plants. Plant Physiol 151:2083–2094PubMedPubMedCentralCrossRefGoogle Scholar
  26. Corpas FJ, Barroso JB, Carreras A, Quirós M, León AM, Romero-Puertas MC, Esteban FJ, Valderrama R, Palma JM, Sandalio LM, Gómez M, del Río LA (2004) Cellular and subcellular localization of endogenous nitric oxide in young and senescent pea plants. Plant Physiol 136:2722–2733Google Scholar
  27. Curry RA, Ting IP (1976) Purification, properties, and kinetic observations on isoenzymes of NADP isocitrate dehydrogenase of maize. Arch Biochem Biophysics 176:501–509CrossRefGoogle Scholar
  28. Daszkowska-Golec A, Szarejko I (2013) Open or close the gate—stomata action under the control of phytohormones in drought stress conditions. Front Plant Sci 4:138PubMedPubMedCentralCrossRefGoogle Scholar
  29. Dat JF, Lopez-Delgado H, Foyer CH, Scott IM (2000) Effects of salicylic acid on oxidative stress and thermotolerance in tobacco. J Plant Physiol 156:659–665CrossRefGoogle Scholar
  30. del Río LA (2011) Peroxisomes as a cellular source of reactive nitrogen species signal molecules. Arch Biochem Biophys 506:1–11PubMedCrossRefGoogle Scholar
  31. del Río LA, Sandalio LM, Corpas FJ, Palma JM, Barroso JB (2006) Reactive oxygen species and reactive nitrogen species in peroxisomes. Production, scavenging, and role in cell signaling. Plant Physiol 141:330–335Google Scholar
  32. Desikan R, Griffiths R, Hancock J, Neill S (2002) A new role for an old enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana. Proc Natl Acad Sci U S A 99:16314–16318PubMedPubMedCentralCrossRefGoogle Scholar
  33. Desikan R, Cheung MK, Bright J, Henson D, Hancock JT, Neill SJ (2004) ABA, hydrogen peroxide and nitric oxide signalling in stomatal guard cells. J Exp Bot 55:205–212PubMedCrossRefGoogle Scholar
  34. Dghim AA, Mhamdi A, Vaultier MN, Hasenfratz-Sauder MP, Le Thiec D, Dizengremel P, Noctor G, Jolivet Y (2013) Analysis of cytosolic isocitrate dehydrogenase and glutathione reductase 1 in photoperiod-influenced responses to ozone using Arabidopsis knockout mutants. Plant Cell Environ 36:1981–1991PubMedGoogle Scholar
  35. Donaldson RP (1982) Nicotinamide cofactors (NAD and NADP) in glyoxysomes, mitochondria, and plastids isolated from castor bean endosperm. Arch Biochem Biophys 215:274–279PubMedCrossRefGoogle Scholar
  36. Eubel H, Meyer EH, Taylor NL, Bussell JD, O’Toole N, Heazlewood JL, Castleden I, Small I, Smith SM, Millar AH (2008) Novel proteins, putative membrane transporters, and an integrated metabolic network are revealed by quantitative proteomic analysis of Arabidopsis cell culture peroxisomes. Plant Physiol 148:1809–1829PubMedPubMedCentralCrossRefGoogle Scholar
  37. Fieuw S, Mullerrober B, Galvez S, Willmitzer L (1995) Cloning and expression analysis of the cytosolic NADP-dependent isocitrate dehydrogenase from potato—implications for nitrogen-metabolism. Plant Physiol 107:905–913PubMedPubMedCentralCrossRefGoogle Scholar
  38. Foyer CH, Noctor G, Hodges M (2011) Respiration and nitrogen assimilation: targeting mitochondria-associated metabolism as a means to enhance nitrogen use efficiency. J Exp Bot 62:1467–1482PubMedCrossRefGoogle Scholar
  39. Gallardo F, Gálvez S, Gadal P, Canovas FM (1995) Changes in NADP-linked isocitrate dehydrogenase during tomato fruit ripening—characterization of the predominant cytosolic enzyme from green and ripe pericarp. Planta 196:148–154CrossRefGoogle Scholar
  40. Gálvez S, Gadal P (1995) On the function of the nadp-dependent isocitrate dehydrogenase isoenzymes in living organisms. Plant Sci 105:1–14CrossRefGoogle Scholar
  41. Gálvez S, Bismuth E, Sarda C, Gadal P (1994) Purification and characterization of chloroplastic NADP-isocitrate dehydrogenase from mixotrophic tobacco cells—comparison with the cytosolic isoenzyme. Plant Physiol 105:593–600PubMedPubMedCentralGoogle Scholar
  42. Gálvez S, Hodges M, Bismuth E, Samson I, Teller S, Gadal P (1995) Purification and characterization of a fully active recombinant tobacco cytosolic NADP-dependent isocitrate dehydrogenase in Escherichia coli—evidence for a role for the N-terminal region in enzyme-activity. Arch Biochem Biophys 323:164–168PubMedCrossRefGoogle Scholar
  43. Gálvez S, Roche O, Bismuth E, Brown S, Gadal P, Hodges M (1998) Mitochondrial localization of a NADR-dependent isocitrate dehydrogenase isoenzyme by using the green fluorescent protein as a marker. Proc Natl Acad Sci U S A 95:7813–7818PubMedPubMedCentralCrossRefGoogle Scholar
  44. Gálvez S, Lancien M, Hodges M (1999) Are isocitrate dehydrogenases and 2-oxoglutarate involved in the regulation of glutamate synthesis? Trends Plant Sci 4:484–490PubMedCrossRefGoogle Scholar
  45. García-Mata C, Lamattina L (2001) Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiol 126:1196–1204PubMedCrossRefGoogle Scholar
  46. García-Mata C, Lamattina L (2002) Nitric oxide and abscisic acid cross talk in guard cells. Plant Physiol 128:790–792PubMedPubMedCentralCrossRefGoogle Scholar
  47. García-Mata C, Lamattina L (2007) Abscisic acid (ABA) inhibits light-induced stomatal opening through calcium- and nitric oxide-mediated signaling pathways. Nitric Oxide Biol Chem 17:143–151CrossRefGoogle Scholar
  48. Gayatri G, Agurla S, Raghavendra AS (2013) Nitric oxide in guard cells as an important secondary messenger during stomatal closure. Front Plant Sci 4:425PubMedPubMedCentralCrossRefGoogle Scholar
  49. Geisbrecht BV, Gould SJ (1999) The human PICD gene encodes a cytoplasmic and peroxisomal NADP-dependent isocitrate dehydrogenase. J Biol Chem 274:30527–30533PubMedCrossRefGoogle Scholar
  50. Gray GR, Villarimo AR, Whitehead CL, McIntosh L (2004) Transgenic tobacco (Nicotiana tabacum L.) plants with increased expression levels of mitochondrial NADP-dependent isocitrate dehydrogenase: evidence implicating this enzyme in the redox activation of the alternative oxidase. Plant Cell Physiol 45:1413–1425PubMedCrossRefGoogle Scholar
  51. Hao F, Zhao S, Dong H, Zhang H, Sun L, Miao C (2010) Nia1 and Nia2 are involved in exogenous salicylic acid-induced nitric oxide generation and stomatal closure in Arabidopsis. J Integr Plant Biol 52:298–307PubMedCrossRefGoogle Scholar
  52. He JM, Xu H, She XP, Song XG, Zhao WM (2005) The role and the interrelationship of hydrogen peroxide and nitric oxide in the UV-B-induced stomatal closure in broad bean. Funct Plant Biol 32:237–247CrossRefGoogle Scholar
  53. Heazlewood JL, Tonti-Filippini JS, Gout AM, Day DA, Whelan J, Millar AH (2004) Experimental analysis of the Arabidopsis mitochondrial proteome highlights signaling and regulatory components, provides assessment of targeting prediction programs, and indicates plant-specific mitochondrial proteins. Plant Cell 16:241–256PubMedPubMedCentralCrossRefGoogle Scholar
  54. Hjelm U, Ögren E (2004) Photosynthetic responses to short-term and long-term light variation in Pinus sylvestris and Salix dasyclados. Trees 18:622–629CrossRefGoogle Scholar
  55. Hodges M, Flesch V, Galvez S, Bismuth E (2003) Higher plant NADP(+)-dependent isocitrate dehydrogenases, ammonium assimilation and NADPH production. Plant Physiol Biochem 41:577–585CrossRefGoogle Scholar
  56. Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35:W585–W587PubMedPubMedCentralCrossRefGoogle Scholar
  57. Hu J, Aguirre M, Peto C, Alonso J, Ecker J, Chory J (2002) A role for peroxisomes in photomorphogenesis and development of Arabidopsis. Science 297:405–409PubMedCrossRefGoogle Scholar
  58. Hu J, Baker A, Bartel B, Linka N, Mullen RT, Reumann S, Zolman BK (2012) Plant peroxisomes: biogenesis and function. Plant Cell 24:2279–2303PubMedPubMedCentralCrossRefGoogle Scholar
  59. Igamberdiev AU, Gardestrom P (2003) Regulation of NAD- and NADP-dependent isocitrate dehydrogenases by reduction levels of pyridine nucleotides in mitochondria and cytosol of pea leaves. Biochimica Et Biophysica Acta-Bioenergetics 1606:117–125CrossRefGoogle Scholar
  60. Jones HG (1992) Plants and microclimate: a quantitative approach to environmental plant physiology. Cambridge University Press, CambridgeGoogle Scholar
  61. Kwak JM, Mori IC, Pei Z-M, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Boddle S, Jones JDG, Schroeder JI (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS dependent ABA signaling in Arabidopsis. EMBO J 22:2623–2633PubMedPubMedCentralCrossRefGoogle Scholar
  62. Lee S, Choi H, Suh S, Doo IS, Oh KY, Choi EJ, Taylor ATS, Low PS, Lee Y (1999) Oligogalacturonic acid and chitosan reduce stomatal aperture by inducing the evolution of reactive oxygen species from guard cells of tomato and Commelina communis. Plant Physiol 121:147–152PubMedPubMedCentralCrossRefGoogle Scholar
  63. Leterrier M, Corpas FJ, Barroso JB, Sandalio LM, del Río LA (2005) Peroxisomal monodehydroascorbate reductase. Genomic clone characterization and functional analysis under environmental stress conditions. Plant Physiol 138:2111–2123PubMedPubMedCentralCrossRefGoogle Scholar
  64. Leterrier M, del Río LA, Corpas FJ (2007) Cytosolic NADP-isocitrate dehydrogenase of pea plants: genomic clone characterization and functional analysis under abiotic stress conditions. Free Radic Res 41:191–199PubMedCrossRefGoogle Scholar
  65. Leterrier M, Barroso JB, Valderrama R, Palma JM, Corpas FJ (2012) NADP-dependent isocitrate dehydrogenase (NADP-ICDH) from Arabidopsis roots contributes in the mechanism of defence against the nitro-oxidative stress induced by salinity. Sci World J 2012:694740CrossRefGoogle Scholar
  66. Li JH, Liu YQ, Lu P, Lin HF, Bai Y, Wang XC, Chen YL (2009) A signaling pathway linking nitric oxide production to heterotrimeric g protein and hydrogen peroxide regulates extracellular calmodulin induction of Stomatal closure in Arabidopsis. Plant Physiol 150:114–124PubMedPubMedCentralCrossRefGoogle Scholar
  67. Lum HK, Butt YKC, Lo SCL (2002) Hydrogen peroxide induces a rapid production of nitric oxide in mung bean (Phaseolus aureus). Nitric Oxide Biol Chem 6:205–213CrossRefGoogle Scholar
  68. Mateos RM, Bonilla-Valverde D, del Río LA, Palma JM, Corpas FJ (2009) NADP-dehydrogenases from pepper fruits: effect of maturation. Physiol Plant 135:130–139PubMedCrossRefGoogle Scholar
  69. McKinnon DJ, Brzezowski P, Wilson KE, Gray GR (2009) Mitochondrial and chloroplastic targeting signals of NADP-dependent isocitrate dehydrogenase. Biochem Cell Biol Biochimie Et Biologie Cellulaire 87:963–974PubMedCrossRefGoogle Scholar
  70. Mhamdi A, Nocto G (2014) Analysis of the roles of the Arabidopsis peroxisomal isocitratedehydrogenase in leaf metabolism and oxidative stress. Environ Exp Bot. doi: 10.1016/j.envexpbot.2014.07.002 Google Scholar
  71. Mhamdi A, Mauve C, Gouia H, Saindrenan P, Hodges M, Noctor G (2010) Cytosolic NADP-dependent isocitrate dehydrogenase contributes to redox homeostasis and the regulation of pathogen responses in Arabidopsis leaves. Plant Cell Environ 33:1112–1123PubMedGoogle Scholar
  72. Moller IM, Rasmusson AG (1998) The role of NADP in the mitochondrial matrix. Trends Plant Sci 3:21–27CrossRefGoogle Scholar
  73. Moschou PN, Sanmartin M, Andriopoulou AH, Rojo E, Sanchez-Serrano JJ, Roubelakis-Angelakis KA (2008) Bridging the gap between plant and mammalian polyamine catabolism: a novel peroxisomal polyamine oxidase responsible for a full back-conversion pathway in Arabidopsis. Plant Physiol 147:1845–1857PubMedPubMedCentralCrossRefGoogle Scholar
  74. Neill SJ, Desikan R, Clarke A, Hancock JT (2002) Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cells. Plant Physiol 128:13–16PubMedPubMedCentralCrossRefGoogle Scholar
  75. Neill S, Barros R, Bright J, Desikan R, Hancock J, Harrison J, Morris P, Ribeiro D, Wilson I (2008) Nitric oxide, stomatal closure, and abiotic stress. J Exp Bot 59:165–176PubMedCrossRefGoogle Scholar
  76. Nekrutenko A, Hillis DM, Patton JC, Bradley RD, Baker RJ (1998) Cytosolic isocitrate dehydrogenase in humans, mice, and voles and phylogenetic analysis of the enzyme family. Mol Biol Evol 15:1674–1684PubMedCrossRefGoogle Scholar
  77. Neuberger G, Maurer-Stroh S, Eisenhaber B, Hartig A, Eisenhaber F (2003a) Prediction of peroxisomal targeting signal 1 containing proteins from amino acid sequence. J Mol Biol 328:581–592PubMedCrossRefGoogle Scholar
  78. Neuberger G, Maurer-Stroh S, Eisenhaber B, Hartig A, Eisenhaber F (2003b) Motif refinement of the peroxisomal targeting signal 1 and evaluation of taxon-specific differences. J Mol Biol 328:567–579PubMedCrossRefGoogle Scholar
  79. Palma JM, Corpas FJ, del Rio LA (2009) Proteome of plant peroxisomes: new perspectives on the role of these organelles in cell biology. Proteomics 9:2301–2312PubMedCrossRefGoogle Scholar
  80. Palomo J, Gallardo F, Suarez MF, Canovas FM (1998) Purification and characterization of NADP(+)-linked isocitrate dehydrogenase from Scots pine—evidence for different physiological roles of the enzyme in primary development. Plant Physiol 118:617–626PubMedPubMedCentralCrossRefGoogle Scholar
  81. Pascual MB, Molina-Rueda JJ, Canovas FM, Gallardo F (2008) Spatial distribution of cytosolic NADP(+)-isocitrate dehydrogenase in pine embryos and seedlings. Tree Physiol 28:1773–1782PubMedCrossRefGoogle Scholar
  82. Pei ZM, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406:731–734PubMedCrossRefGoogle Scholar
  83. Popova TN, Rakhmanova TI, Appenroth KJ (2002) Cytosolic and chloroplastic NADP-dependent isocitrate dehydrogenases in Spirodela polyrhiza. I. Regulation of activity by metabolites in vitro. J Plant Physiol 159:231–237CrossRefGoogle Scholar
  84. Proost S, Van Bel M, Sterck L, Billiau K, Van Parys T, Van de Peer Y, Vandepoele K (2009) PLAZA: a comparative genomics resource to study gene and genome evolution in plants. Plant Cell 21:3718–3731PubMedPubMedCentralCrossRefGoogle Scholar
  85. Quan S, Yang P, Cassin-Ross G, Kaur N, Switzenberg R, Aung K, Li J, Hu J (2013) Proteome analysis of peroxisomes from etiolated Arabidopsis seedlings identifies a peroxisomal protease involved in β-oxidation and development. Plant Physiol 163:1518–1538PubMedPubMedCentralCrossRefGoogle Scholar
  86. Rasmusson AG, Moller IM (1990) NADP-utilizing enzymes in the matrix of plant-mitochondria. Plant Physiol 94:1012–1018PubMedPubMedCentralCrossRefGoogle Scholar
  87. Reumann S (2011) Toward a definition of the complete proteome of plant peroxisomes: where experimental proteomics must be complemented by bioinformatics. Proteomics 11:1764–1779PubMedCrossRefGoogle Scholar
  88. Reumann S, Ma CL, Lemke S, Babujee L (2004) AraPerox. A database of putative Arabidopsis proteins from plant peroxisomes. Plant Physiol 136:2587–2608PubMedPubMedCentralCrossRefGoogle Scholar
  89. Reumann S, Babujee L, Ma CL, Wienkoop S, Siemsen T, Antonicelli GE, Rasche N, Luder F, Weckwerth W, Jahn O (2007) Proteome analysis of Arabidopsis leaf peroxisomes reveals novel targeting peptides, metabolic pathways, and defense mechanisms. Plant Cell 19:3170–3193PubMedPubMedCentralCrossRefGoogle Scholar
  90. Reumann S, Quan S, Aung K, Yang P, Manandhar-Shrestha K, Holbrook D, Linka N, Switzenberg R, Wilkerson CG, Weber AP, Olsen LJ, Hu J (2009) In-depth proteome analysis of Arabidopsis leaf peroxisomes combined with in vivo subcellular targeting verification indicates novel metabolic and regulatory functions of peroxisomes. Plant Physiol 150:125–143PubMedPubMedCentralCrossRefGoogle Scholar
  91. Romero-Puertas MC, Corpas FJ, Sandalio LM, Leterrier M, Rodríguez-Serrano M, Del Río LA, Palma JM (2006) Glutathione reductase from pea leaves: response to abiotic stress and characterization of the peroxisomal isozyme. New Phytol 170(1):43–52PubMedCrossRefGoogle Scholar
  92. Sagi M, Fluhr R (2006) Production of reactive oxygen species by plant NADPH oxidases. Plant Physiol 141:336–340PubMedPubMedCentralCrossRefGoogle Scholar
  93. Sankaran B, Chavan AJ, Haley BE (1996) Identification of adenine binding domain peptides of the NADP(+) active site within porcine heart NADP(+)-dependent isocitrate dehydrogenase. Biochemistry 35:13501–13510PubMedCrossRefGoogle Scholar
  94. Scheible WR, Krapp A, Stitt M (2000) Reciprocal diurnal changes of phosphoenolpyruvate carboxylase expression and cytosolic pyruvate kinase, citrate synthase and NADP-isocitrate dehydrogenase expression regulate organic acid metabolism during nitrate assimilation in tobacco leaves. Plant Cell Environ 23:1155–1167CrossRefGoogle Scholar
  95. Shi YC, Fu YP, Liu WQ (2012) NADPH oxidase in plasma membrane is involved in stomatal closure induced by dehydroascorbate. Plant Physiol Biochem 51:26–30PubMedCrossRefGoogle Scholar
  96. Shorrosh BS, Dixon RA (1992) Molecular characterization and expression of an isocitrate dehydrogenase from alfalfa (Medicago sativa L). Plant Mol Biol 20:801–807PubMedCrossRefGoogle Scholar
  97. Song XG, She XP, Wang J, Sun YC (2011) Ethylene inhibits darkness-induced stomatal closure by scavenging nitric oxide in guard cells of Vicia faba. Funct Plant Biol 38:767–777CrossRefGoogle Scholar
  98. Sulpice R, Sienkiewicz-Porzucek A, Osorio S, Krahnert I, Stitt M, Fernie AR, Nunes-Nesi A (2010) Mild reductions in cytosolic NADP-dependent isocitrate dehydrogenase activity result in lower amino acid contents and pigmentation without impacting growth. Amino Acids 39:1055–1066PubMedPubMedCentralCrossRefGoogle Scholar
  99. Uraji M, Katagiri T, Okuma E, Ye W, Hossain MA, Masuda C, Miura A, Nakamura Y, Mori II, Shinozaki K, Murata Y (2012) Cooperative function of PLDδ and PLDα1 in ABA-induced stomatal closure in Arabidopsis. Plant Physiol 159:450–460PubMedPubMedCentralCrossRefGoogle Scholar
  100. Waller JC, Dhanoa PK, Schumann U, Mullen RT, Snedden WA (2010) Subcellular and tissue localization of NAD kinases from Arabidopsis: compartmentalization of de novo NADP biosynthesis. Planta 231:305–317PubMedCrossRefGoogle Scholar
  101. Wang P, Du Y, Hou Y, Zhao Y, Hsu C, Yuan F, Zhu X, Tao WA, Song C, Zhu J (2014) Nitric oxide negatively regulates abscisic acid signaling in guard cells by S-nitrosylation of OST1. Proc Natl Acad Sci U S A 112:613–618PubMedPubMedCentralCrossRefGoogle Scholar
  102. Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007) An “electronic fluorescent pictograph” browser for exploring and analyzing large-scale biological data sets. Plos One 2Google Scholar
  103. Yu M, Xie Y, Zhang X (2005) Quantification of intrinsic water use efficiency along a moisture gradient in northeastern China. J Environ Qual 34:1311–1318PubMedCrossRefGoogle Scholar
  104. Yu G, Song X, Wang Q, Liu Y, Guan D, Yan J, Sun X, Zhang L, Wen X (2008) Water-use efficiency of forest ecosystems in eastern China and its relations to climatic variables. New Phytol 177:927–937PubMedCrossRefGoogle Scholar
  105. Zhang W, Fan LM, Wu WH (2007) Osmo-sensitive and stretch-activated calcium-permeable channels in Vicia faba guard cells are regulated by actin dynamics. Plant Physiol 143:1140–1151Google Scholar
  106. Zhang X, Zhang L, Dong FC, Gao JF, Galbraith DW, Song CP (2001) Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol 126:1438–1448PubMedPubMedCentralCrossRefGoogle Scholar
  107. Zhang Y, Zhu H, Zhang Q, Li M, Yan M, Wang R, Wang L, Welti R, Zhang W, Wang X (2009) Phospholipase dalpha1 and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis. Plant Cell 21:2357–2377PubMedPubMedCentralCrossRefGoogle Scholar
  108. Zybailov B, Rutschow H, Friso G, Rudella A, Emanuelsson O, Sun Q, van Wijk KJ (2008) Sorting signals, N-terminal modifications and abundance of the chloroplast proteome. Plos One 3Google Scholar

Copyright information

© Springer-Verlag Wien 2015

Authors and Affiliations

  • Marina Leterrier
    • 1
  • Juan B. Barroso
    • 2
  • Raquel Valderrama
    • 2
  • Juan C. Begara-Morales
    • 2
  • Beatriz Sánchez-Calvo
    • 2
  • Mounira Chaki
    • 1
  • Francisco Luque
    • 2
  • Benjamin Viñegla
    • 3
  • José M. Palma
    • 1
  • Francisco J. Corpas
    • 1
    Email author
  1. 1.Group of Antioxidants, Free Radicals and Nitric Oxide in Biotechnology, Food and Agriculture, Department of Biochemistry, Cell and Molecular Biology of PlantsEstación Experimental del Zaidín, CSICGranadaSpain
  2. 2.Group of Biochemistry and Cell Signaling in Nitric Oxide, Department of Biochemistry and Molecular BiologyUniversity of JaénJaénSpain
  3. 3.Departamento de Biología Animal, Biología Vegetal y Ecología (Ecología), Facultad de Ciencias ExperimentalesUniversidad de JaénJaénSpain

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