Plant Molecular Biology

, Volume 70, Issue 5, pp 547–563 | Cite as

Arabidopsis mutants reveal multiple singlet oxygen signaling pathways involved in stress response and development

  • Aiswarya Baruah
  • Klára Šimková
  • Klaus Apel
  • Christophe Laloi
Article

Abstract

Shortly after the release of singlet oxygen (1O2) in chloroplasts drastic changes in nuclear gene expression occur in the conditional flu mutant of Arabidopsis that reveal a rapid transfer of signals from the plastid to the nucleus. Factors involved in this retrograde signaling were identified by mutagenizing a transgenic flu line expressing a 1O2-responsive reporter gene. The reporter gene consisted of the luciferase open reading frame and the promoter of an AAA-ATPase gene (At3g28580) that was selectively activated by 1O2 but not by superoxide or hydrogen peroxide. A total of eight second-site mutants were identified that either constitutively activate the reporter gene and the endogenous AAA-ATPase irrespectively of whether 1O2 was generated or not (constitutive activators of AAA-ATPase, caa) or abrogated the 1O2-dependent up-regulation of these genes as seen in the transgenic parental flu line (non-activators of AAA-ATPase, naa). The characterization of the mutants strongly suggests that 1O2-signaling does not operate as an isolated linear pathway but rather forms an integral part of a signaling network that is modified by other signaling routes and impacts not only stress responses of plants but also their development.

Keywords

Arabidopsis Oxidative stress Singlet oxygen Signaling flu mutant AAA-ATPase 

Supplementary material

11103_2009_9491_MOESM1_ESM.pdf (193 kb)
Supplementary material 1 (PDF 192 kb)

References

  1. Anthony JR, Warczak KL, Donohue TJ (2005) A transcriptional response to singlet oxygen, a toxic byproduct of photosynthesis. Proc Natl Acad Sci USA 102:6502–6507. doi:10.1073/pnas.0502225102 PubMedCrossRefGoogle Scholar
  2. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399. doi:10.1146/annurev.arplant.55.031903.141701 PubMedCrossRefGoogle Scholar
  3. Asada K (1999) The water–water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639. doi:10.1146/annurev.arplant.50.1.601 PubMedCrossRefGoogle Scholar
  4. Asada K, Kiso K, Yoshikawa K (1974) Univalent reduction of molecular oxygen by spinach chloroplasts on illumination. J Biol Chem 249:2175–2181PubMedGoogle Scholar
  5. Babbs CF, Pham JA, Coolbaugh RC (1989) Lethal hydroxyl radical production in paraquat-treated plants. Plant Physiol 90:1267–1270. doi:10.1104/pp.90.4.1267 PubMedCrossRefGoogle Scholar
  6. Baier M, Dietz KJ (2005) Chloroplasts as source and target of cellular redox regulation: a discussion on chloroplast redox signals in the context of plant physiology. J Exp Bot 56:1449–1462. doi:10.1093/jxb/eri161 PubMedCrossRefGoogle Scholar
  7. Ball L, Accotto GP, Bechtold U, Creissen G, Funck D, Jimenez A, Kular B, Leyland N, Mejia-Carranza J, Reynolds H, Karpinski S, Mullineaux PM (2004) Evidence for a direct link between glutathione biosynthesis and stress defense gene expression in Arabidopsis. Plant Cell 16:2448–2462. doi:10.1105/tpc.104.022608 PubMedCrossRefGoogle Scholar
  8. Beck CF (2005) Signaling pathways from the chloroplast to the nucleus. Planta 222:743–756. doi:10.1007/s00425-005-0021-2 PubMedCrossRefGoogle Scholar
  9. Cao H, Bowling SA, Gordon AS, Dong X (1994) Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6:1583–1592PubMedCrossRefGoogle Scholar
  10. Danon A, Miersch O, Felix G, Camp RG, Apel K (2005) Concurrent activation of cell death-regulating signaling pathways by singlet oxygen in Arabidopsis thaliana. Plant J 41:68–80. doi:10.1111/j.1365-313X.2004.02276.x PubMedCrossRefGoogle Scholar
  11. Dunkley TP, Hester S, Shadforth IP, Runions J, Weimar T, Hanton SL, Griffin JL, Bessant C, Brandizzi F, Hawes C, Watson RB, Dupree P, Lilley KS (2006) Mapping the Arabidopsis organelle proteome. Proc Natl Acad Sci USA 103:6518–6523. doi:10.1073/pnas.0506958103 PubMedCrossRefGoogle Scholar
  12. Fischer BB, Krieger-Liszkay A, Hideg E, Snyrychova I, Wiesendanger M, Eggen RI (2007) Role of singlet oxygen in chloroplast to nucleus retrograde signaling in Chlamydomonas reinhardtii. FEBS Lett 581:5555–5560. doi:10.1016/j.febslet.2007.11.003 PubMedCrossRefGoogle Scholar
  13. Flors C, Fryer MJ, Waring J, Reeder B, Bechtold U, Mullineaux PM, Nonell S, Wilson MT, Baker NR (2006) Imaging the production of singlet oxygen in vivo using a new fluorescent sensor, singlet oxygen sensor green (R). J Exp Bot 57:1725–1734. doi:10.1093/jxb/erj181 PubMedCrossRefGoogle Scholar
  14. Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446. doi:10.1038/nature01485 PubMedCrossRefGoogle Scholar
  15. Foyer CH, Noctor G (2000) Oxygen processing in photosynthesis: regulation and signalling. New Phytol 146:359–388. doi:10.1046/j.1469-8137.2000.00667.x CrossRefGoogle Scholar
  16. Foyer CH, Noctor G (2003) Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant 119:355–364. doi:10.1034/j.1399-3054.2003.00223.x CrossRefGoogle Scholar
  17. Gadjev I, Vanderauwera S, Gechev TS, Laloi C, Minkov IN, Shulaev V, Apel K, Inze D, Mittler R, Van Breusegem F (2006) Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol 141:436–445. doi:10.1104/pp.106.078717 PubMedCrossRefGoogle Scholar
  18. Gechev TS, Van Breusegem F, Stone JM, Denev I, Laloi C (2006) Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. Bioessays 28:1091–1101. doi:10.1002/bies.20493 PubMedCrossRefGoogle Scholar
  19. Gollnick K (1968) Type 2 photosensitized oxygenation reactions. Adv Chem Ser 77:78–101CrossRefGoogle Scholar
  20. Gorman AA, Rodgers MAJ (1992) Current perspectives of singlet oxygen detection in biological environments. J Photochem Photobiol B 14:159–176. doi:10.1016/1011-1344(92)85095-C PubMedCrossRefGoogle Scholar
  21. Heiber I, Stroher E, Raatz B, Busse I, Kahmann U, Bevan MW, Dietz KJ, Baier M (2007) The redox imbalanced mutants of Arabidopsis differentiate signaling pathways for redox regulation of chloroplast antioxidant enzymes. Plant Physiol 143:1774–1788. doi:10.1104/pp.106.093328 PubMedCrossRefGoogle Scholar
  22. Hetherington SE, He J, Smillie RM (1989) Photoinhibition at low-temperature in chilling-sensitive and chilling-resistant plants. Plant Physiol 90:1609–1615. doi:10.1104/pp.90.4.1609 PubMedCrossRefGoogle Scholar
  23. Hideg E, Kalai T, Hideg K, Vass I (1998) Photoinhibition of photosynthesis in vivo results in singlet oxygen production detection via nitroxide-induced fluorescence quenching in broad bean leaves. Biochemistry 37:11405–11411. doi:10.1021/bi972890+ PubMedCrossRefGoogle Scholar
  24. Hideg E, Kalai T, Hideg K, Vass I (2000) Do oxidative stress conditions impairing photosynthesis in the light manifest as photoinhibition? Philos Trans R Soc Lond B Biol Sci 355:1511–1516. doi:10.1098/rstb.2000.0711 PubMedCrossRefGoogle Scholar
  25. Hideg E, Barta C, Kalai T, Vass I, Hideg K, Asada K (2002) Detection of singlet oxygen and superoxide with fluorescent sensors in leaves under stress by photoinhibition or UV radiation. Plant Cell Physiol 43:1154–1164. doi:10.1093/pcp/pcf145 PubMedCrossRefGoogle Scholar
  26. Hideg E, Kalai T, Kos PB, Asada K, Hideg K (2006) Singlet oxygen in plants- Its significance and possible detection with double (fluorescent and spin) indicator reagents. Photochem Photobiol 82:1211–1218. doi:10.1562/2006-02-06-RA-797 PubMedCrossRefGoogle Scholar
  27. Keogh RC, Deverall BJ, Mcleod S (1980) Comparison of histological and physiological-responses to phakopsora-pachyrhizi in resistant and susceptible soybean. Trans Br Mycol Soc 74:329–333CrossRefGoogle Scholar
  28. Keren N, Berg A, van Kan PJ, Levanon H, Ohad I (1997) Mechanism of photosystem II photoinactivation and D1 protein degradation at low light: the role of back electron flow. Proc Natl Acad Sci USA 94:1579–1584. doi:10.1073/pnas.94.4.1579 PubMedCrossRefGoogle Scholar
  29. Klotz LO, Kroncke KD, Sies H (2003) Singlet oxygen-induced signaling effects in mammalian cells. Photochem Photobiol Sci 2:88–94. doi:10.1039/b210750c PubMedCrossRefGoogle Scholar
  30. Kochevar IE, Bouvier J, Lynch M, Lin CW (1994) Influence of dye and protein location on photosensitization of the plasma membrane. Biochim Biophys Acta 1196:172–180. doi:10.1016/0005-2736(94)00236-3 PubMedCrossRefGoogle Scholar
  31. Koncz C, Martini N, Szabados L, Hrouda M, Bachmair A, Schell J (1994) Specialized vectors for gene tagging and expression studies. Plant Mol Biol Man B2:1–22Google Scholar
  32. Koussevitzky S, Nott A, Mockler TC, Hong F, Sachetto-Martins G, Surpin M, Lim J, Mittler R, Chory J (2007) Signals from chloroplasts converge to regulate nuclear gene expression. Science 316:715–719. doi:10.1126/science.1140516 PubMedCrossRefGoogle Scholar
  33. Kozaki A, Takeba G (1996) Photorespiration protects C3 plants from photooxidation. Nature 384:557–560. doi:10.1038/384557a0 CrossRefGoogle Scholar
  34. Krieger-Liszkay A, Fufezan C, Trebst A (2008) Singlet oxygen production in photosystem II and related protection mechanism. Photosynth Res 98:551–564. doi:10.1007/s11120-008-9349-3 PubMedCrossRefGoogle Scholar
  35. Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JD, Schroeder JI (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22:2623–2633. doi:10.1093/emboj/cdg277 PubMedCrossRefGoogle Scholar
  36. Laloi C, Apel K, Danon A (2004) Reactive oxygen signalling: the latest news. Curr Opin Plant Biol 7:323–328. doi:10.1016/j.pbi.2004.03.005 PubMedCrossRefGoogle Scholar
  37. Laloi C, Przybyla D, Apel K (2006) A genetic approach towards elucidating the biological activity of different reactive oxygen species in Arabidopsis thaliana. J Exp Bot 57:1719–1724. doi:10.1093/jxb/erj183 PubMedCrossRefGoogle Scholar
  38. Laloi C, Stachowiak M, Pers-Kamczyc E, Warzych E, Murgia I, Apel K (2007) Cross-talk between singlet oxygen- and hydrogen peroxide-dependent signaling of stress responses in Arabidopsis thaliana. Proc Natl Acad Sci USA 104:672–677. doi:10.1073/pnas.0609063103 PubMedCrossRefGoogle Scholar
  39. Ledford HK, Chin BL, Niyogi KK (2007) Acclimation to singlet oxygen stress in Chlamydomonas reinhardtii. Eukaryot Cell 6:919–930. doi:10.1128/EC.00207-06 PubMedCrossRefGoogle Scholar
  40. Lee KP, Kim C, Landgraf F, Apel K (2007) EXECUTER1- and EXECUTER2-dependent transfer of stress-related signals from the plastid to the nucleus of Arabidopsis thaliana. Proc Natl Acad Sci USA 104:10270–10275. doi:10.1073/pnas.0702061104 PubMedCrossRefGoogle Scholar
  41. Leisinger U, Rufenacht K, Fischer B, Pesaro M, Spengler A, Zehnder AJ, Eggen RI (2001) The glutathione peroxidase homologous gene from Chlamydomonas reinhardtii is transcriptionally up-regulated by singlet oxygen. Plant Mol Biol 46:395–408. doi:10.1023/A:1010601424452 PubMedCrossRefGoogle Scholar
  42. Long SP, Humphries S, Falkowski PG (1994) Photoinhibition of photosynthesis in nature. Annu Rev Plant Physiol Plant Mol Biol 45:633–662. doi:10.1146/annurev.pp.45.060194.003221 CrossRefGoogle Scholar
  43. Medina J, Rodriguez-Franco M, Penalosa A, Carrascosa MJ, Neuhaus G, Salinas J (2005) Arabidopsis mutants deregulated in RCI2A expression reveal new signaling pathways in abiotic stress responses. Plant J 42:586–597. doi:10.1111/j.1365-313X.2005.02400.x PubMedCrossRefGoogle Scholar
  44. Melzer S, Majewski DM, Apel K (1990) Early changes in gene expression during the transition from vegetative to generative growth in the long-day plant sinapis alba. Plant Cell 2:953–961PubMedCrossRefGoogle Scholar
  45. Meskauskiene R, Nater M, Goslings D, Kessler F, op den Camp R, Apel K (2001) FLU: a negative regulator of chlorophyll biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 104(98):12826–12831. doi:10.1073/pnas.221252798 CrossRefGoogle Scholar
  46. Millar AJ, Carre IA, Strayer CA, Chua NH, Kay SA (1995) Circadian clock mutants in Arabidopsis identified by luciferase imaging. Science 267:1161–1163. doi:10.1126/science.7855595 PubMedCrossRefGoogle Scholar
  47. Miller G, Suzuki N, Rizhsky L, Hegie A, Koussevitzky S, Mittler R (2007) Double mutants deficient in cytosolic and thylakoid ascorbate peroxidase reveal a complex mode of interaction between reactive oxygen species, plant development, and response to abiotic stresses. Plant Physiol 144:1777–1785. doi:10.1104/pp.107.101436 PubMedCrossRefGoogle Scholar
  48. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498. doi:10.1016/j.tplants.2004.08.009 PubMedCrossRefGoogle Scholar
  49. Mochizuki N, Tanaka R, Tanaka A, Masuda T, Nagatani A (2008) The steady-state level of Mg-protoporphyrin IX is not a determinant of plastid-to-nucleus signaling in Arabidopsis. Proc Natl Acad Sci USA 105:15184–15189. doi:10.1073/pnas.0803245105 PubMedCrossRefGoogle Scholar
  50. Mogk A, Haslberger T, Tessarz P, Bukau B (2008) Common and specific mechanisms of AAA + proteins involved in protein quality control. Biochem Soc Trans 36:120–125. doi:10.1042/BST0360120 PubMedCrossRefGoogle Scholar
  51. Moulin M, McCormac AC, Terry MJ, Smith AG (2008) Tetrapyrrole profiling in Arabidopsis seedlings reveals that retrograde plastid nuclear signaling is not due to Mg-protoporphyrin IX accumulation. Proc Natl Acad Sci USA 105:15178–15183. doi:10.1073/pnas.0803054105 PubMedCrossRefGoogle Scholar
  52. Muller P, Li XP, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566. doi:10.1104/pp.125.4.1558 PubMedCrossRefGoogle Scholar
  53. Mullineaux P, Karpinski S (2002) Signal transduction in response to excess light: getting out of the chloroplast. Curr Opin Plant Biol 5:43–48. doi:10.1016/S1369-5266(01)00226-6 PubMedCrossRefGoogle Scholar
  54. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497. doi:10.1111/j.1399-3054.1962.tb08052.x CrossRefGoogle Scholar
  55. Murgia I, Tarantino D, Vannini C, Bracale M, Carravieri S, Soave C (2004) Arabidopsis thaliana plants overexpressing thylakoidal ascorbate peroxidase show increased resistance to Paraquat-induced photooxidative stress and to nitric oxide-induced cell death. Plant J 38:940–953. doi:10.1111/j.1365-313X.2004.02092.x PubMedCrossRefGoogle Scholar
  56. Nemhauser JL, Hong F, Chory J (2006) Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell 126:467–475. doi:10.1016/j.cell.2006.05.050 PubMedCrossRefGoogle Scholar
  57. Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50:333–359. doi:10.1146/annurev.arplant.50.1.333 PubMedCrossRefGoogle Scholar
  58. Nott A, Jung HS, Koussevitzky S, Chory J (2006) Plastid-to-nucleus retrograde signaling. Annu Rev Plant Biol 57:739–759. doi:10.1146/annurev.arplant.57.032905.105310 PubMedCrossRefGoogle Scholar
  59. Ochsenbein C, Przybyla D, Danon A, Landgraf F, Gobel C, Imboden A, Feussner I, Apel K (2006) The role of EDS1 (enhanced disease susceptibility) during singlet oxygen-mediated stress responses of Arabidopsis. Plant J 47:445–456. doi:10.1111/j.1365-313X.2006.02793.x PubMedCrossRefGoogle Scholar
  60. op den Camp RG, Przybyla D, Ochsenbein C, Laloi C, Kim C, Danon A, Wagner D, Hideg E, Gobel C, Feussner I, Nater M, Apel K (2003) Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell 15:2320–2332PubMedCrossRefGoogle Scholar
  61. Overmyer K, Brosche M, Kangasjarvi J (2003) Reactive oxygen species and hormonal control of cell death. Trends Plant Sci 8:335–342PubMedCrossRefGoogle Scholar
  62. Petit JM, Briat JF, Lobreaux S (2001) Structure and differential expression of the four members of the Arabidopsis thaliana ferritin gene family. Biochem J 359:575–582PubMedCrossRefGoogle Scholar
  63. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45PubMedCrossRefGoogle Scholar
  64. Pfannschmidt T (2003) Chloroplast redox signals: how photosynthesis controls its own genes. Trends Plant Sci 8:33–41PubMedCrossRefGoogle Scholar
  65. Przybyla D, Gobel C, Imboden A, Hamberg M, Feussner I, Apel K (2008) Enzymatic, but not non-enzymatic, 1O2-mediated peroxidation of polyunsaturated fatty acids forms part of the EXECUTER1-dependent stress response program in the flu mutant of Arabidopsis thaliana. Plant J 54:236–248PubMedCrossRefGoogle Scholar
  66. Rama Devi S, Chen X, Oliver DJ, Xiang C (2006) A novel high-throughput genetic screen for stress-responsive mutants of Arabidopsis thaliana reveals new loci involving stress responses. Plant J 47:652–663PubMedCrossRefGoogle Scholar
  67. Redmond RW, Kochevar IE (2006) Spatially resolved cellular responses to singlet oxygen. Photochem Photobiol 82:1178–1186PubMedCrossRefGoogle Scholar
  68. Regenberg B, Grotkjaer T, Winther O, Fausboll A, Akesson M, Bro C, Hansen LK, Brunak S, Nielsen J (2006) Growth-rate regulated genes have profound impact on interpretation of transcriptome profiling in Saccharomyces cerevisiae. Genome Biol 7:R107PubMedCrossRefGoogle Scholar
  69. Rizhsky L, Liang H, Mittler R (2003) The water–water cycle is essential for chloroplast protection in the absence of stress. J Biol Chem 278:38921–38925PubMedCrossRefGoogle Scholar
  70. Rizhsky L, Davletova S, Liang H, Mittler R (2004) The zinc finger protein Zat12 is required for cytosolic ascorbate peroxidase 1 expression during oxidative stress in Arabidopsis. J Biol Chem 279:11736–11743PubMedCrossRefGoogle Scholar
  71. Rodermel S (2001) Pathways of plastid-to-nucleus signaling. Trends Plant Sci 6:471–478PubMedCrossRefGoogle Scholar
  72. Runge S, van Cleve B, Lebedev N, Armstrong G, Apel K (1995) Isolation and classification of chlorophyll-deficient xantha mutants of Arabidopsis thaliana. Planta 197:490–500PubMedCrossRefGoogle Scholar
  73. Shao N, Krieger-Liszkay A, Schroda M, Beck CF (2007) A reporter system for the individual detection of hydrogen peroxide and singlet oxygen: its use for the assay of reactive oxygen species produced in vivo. Plant J 50:475–487PubMedCrossRefGoogle Scholar
  74. Sies H, Menck CFM (1992) Singlet oxygen induced DNA damage. Mutat Res 275:367–375PubMedGoogle Scholar
  75. Stelling J, Sauer U, Szallasi Z, Doyle FJ 3rd, Doyle J (2004) Robustness of cellular functions. Cell 118:675–685PubMedCrossRefGoogle Scholar
  76. Strand A, Asami T, Alonso J, Ecker JR, Chory J (2003) Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrinIX. Nature 421:79–83PubMedCrossRefGoogle Scholar
  77. Sullivan JA, Gray JC (1999) Plastid translation is required for the expression of nuclear photosynthesis genes in the dark and in roots of the pea lip1 mutant. Plant Cell 11:901–910PubMedCrossRefGoogle Scholar
  78. Surpin M, Larkin RM, Chory J (2002) Signal transduction between the chloroplast and the nucleus. Plant Cell 14:S327–S338PubMedGoogle Scholar
  79. Taylor WC (1989) Regulatory interactions between nuclear and plastid genomes. Annu Rev Plant Physiol Plant Mol Biol 40:211–233CrossRefGoogle Scholar
  80. Toth R, Kevei E, Hall A, Millar AJ, Nagy F, Kozma-Bognar L (2001) Circadian clock-regulated expression of phytochrome and cryptochrome genes in Arabidopsis. Plant Physiol 127:1607–1616PubMedCrossRefGoogle Scholar
  81. Triantaphylides C, Krischke M, Hoeberichts FA, Ksas B, Gresser G, Havaux M, Van Breusegem F, Mueller MJ (2008) Singlet oxygen is the major reactive oxygen species involved in photooxidative damage to plants. Plant Physiol 148:960–968PubMedCrossRefGoogle Scholar
  82. Wagner D, Przybyla D, Op den Camp R, Kim C, Landgraf F, Lee KP, Wursch M, Laloi C, Nater M, Hideg E, Apel K (2004) The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana. Science 306:1183–1185PubMedCrossRefGoogle Scholar
  83. Wise RR, Naylor AW (1987) Chilling-enhanced photooxidation—evidence for the role of singlet oxygen and superoxide in the breakdown of pigments and endogenous antioxidants. Plant Physiol 83:278–282PubMedCrossRefGoogle Scholar
  84. Woodson JD, Chory J (2008) Coordination of gene expression between organellar and nuclear genomes. Nat Rev Genet 9:383–395PubMedCrossRefGoogle Scholar
  85. Yoshioka H, Numata N, Nakajima K, Katou S, Kawakita K, Rowland O, Jones JD, Doke N (2003) Nicotiana benthamiana gp91phox homologs NbrbohA and NbrbohB participate in H2O2 accumulation and resistance to Phytophthora infestans. Plant Cell 15:706–718PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Aiswarya Baruah
    • 1
    • 2
  • Klára Šimková
    • 1
  • Klaus Apel
    • 1
    • 2
  • Christophe Laloi
    • 1
  1. 1.Institute of Plant Sciences, ETH ZurichZurichSwitzerland
  2. 2.Boyce Thompson Institute for Plant ResearchIthacaUSA

Personalised recommendations