Light intensity-dependent retrograde signalling in higher plants

Journal of Plant Physiology

Volumn 170, Issue 17, 2013, Pages 1501-1516

  Szechyńska Hebda, Magdalena ^a,b   Karpiński, Stanisław ^b  

^a THE FRANCISZEK GÓRSKI INSTITUTE OF PLANT PHYSIOLOGY   (Poland)

^b WARSAW UNIVERSITY OF LIFE SCIENCES   (Poland)

Author keywords

Antioxidative enzymes; Chloroplast retrograde signalling; Intra and inter cellular signalling; Light intensity; Photo electrochemical signalling

Indexed keywords

EMBRYOPHYTA; TRACHEOPHYTA;

PHYTOHORMONE; PLASTOQUINONE; REACTIVE OXYGEN METABOLITE;

ACCLIMATIZATION; ANTIOXIDATIVE ENZYMES; APOPTOSIS; ARABIDOPSIS; ARTICLE; CELL AGING; CHLOROPLAST; CHLOROPLAST RETROGRADE SIGNALLING; CYTOLOGY; EEE; ELECTRON TRANSPORT; EXCESS EXCITATION ENERGY; GROWTH, DEVELOPMENT AND AGING; GSH AND GSSH; INTRA- AND INTER-CELLULAR SIGNALLING; INTRACELLULAR MEMBRANE; LIGHT; LIGHT INTENSITY; META ANALYSIS; METABOLISM; NONPHOTOCHEMICAL QUENCHING; NPQ; OXIDATIVE STRESS; PCD; PET; PHOTO-ELECTROCHEMICAL SIGNALLING; PHOTOSYNTHETIC ELECTRON TRANSPORT; PHOTOSYSTEMS I AND II; PHOTOTRANSDUCTION; PHYSIOLOGY; PLANT LEAF; PQ; PSI AND PSII; RADIATION EXPOSURE; REDUCED AND OXIDISED GLUTATHIONE FORMS; ROS; SAA; SAR; SYSTEMIC ACQUIRED ACCLIMATION; SYSTEMIC ACQUIRED RESISTANCE.; ULTRASTRUCTURE;

ANTIOXIDATIVE ENZYMES; CHLOROPLAST RETROGRADE SIGNALLING; EEE; EXCESS EXCITATION ENERGY; GSH AND GSSH; INTRA- AND INTER-CELLULAR SIGNALLING; LIGHT INTENSITY; NONPHOTOCHEMICAL QUENCHING; NPQ; PCD; PET; PHOTO-ELECTROCHEMICAL SIGNALLING; PHOTOSYNTHETIC ELECTRON TRANSPORT; PHOTOSYSTEMS I AND II; PLASTOQUINONE; PQ; PROGRAMMED CELL DEATH; PSI AND PSII; REACTIVE OXYGEN SPECIES; REDUCED AND OXIDISED GLUTATHIONE FORMS; ROS; SAA; SAR; SYSTEMIC ACQUIRED ACCLIMATION; SYSTEMIC ACQUIRED RESISTANCE.;

ACCLIMATIZATION; ARABIDOPSIS; CELL AGING; CHLOROPLASTS; ELECTRON TRANSPORT; INTRACELLULAR MEMBRANES; LIGHT; LIGHT SIGNAL TRANSDUCTION; OXIDATIVE STRESS; PLANT GROWTH REGULATORS; PLANT LEAVES; REACTIVE OXYGEN SPECIES;

EID: 84884976690     PISSN: 01761617     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jplph.2013.06.005     Document Type: Article

References (169)

1. Adamiec M., Drath M., Jackowski G. Redox state of plastoquinone pool regulates expression of Arabidopsis thaliana genes in response to elevated irradiance. Acta Biochim Pol 2008, 55:161-173.
2. Alboresi A., Dallosto L., Aprile A., Carillo P., Roncaglia E., Cattivelli L., et al. Reactive oxygen species and transcript analysis upon excess light treatment in wild-type Arabidopsis thaliana vs a photosensitive mutant lacking zeaxanthin and lutein. BMC Plant Biol 2011, 11:62-83.
3. Andersson M.X., Goksör M., Sandelius A.S. Optical manipulation reveals strong attracting forces at membrane contact sites between endoplasmic reticulum and chloroplasts. J Biol Chem 2007, 282:1170-1174.
4. Apel K., Hirt H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 2004, 55:373-399.
5. Armbruster U., Pesaresi P., Pribil M., Hertle A., Leister D. Update on chloroplast research: new tools, new topics, and new trends. Mol Plant 2010, 1-16. 10.1093/mp/ssq060.
6. Asada K. Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 2006, 141:391-396.
7. Asada K. The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 1999, 50:601-639.
8. Aseeva E., Ossenbühl F., Sippel C., Cho W.K., Stein B., Eichacker L.A., et al. Vipp1 is required for basic thylakoid membrane formation but not for the assembly of thylakoid protein complexes. Plant Physiol Biochem 2007, 45:119-128.
9. Bae G., Choi G. Decoding of light signals by plant phytochromes and their interacting proteins. Annu Rev Plant Biol 2008, 59:281-311.
10. Baena-González E., Sheen J. Convergent energy and stress signaling. Trends Plant Sci 2008, 13:474-482.
11. Baier M., Dietz K.J. Chloroplasts as source and target of cellular redox regulation: a discussion on chloroplast redox signals in the context of plant physiology. J Exp Bot 2005, 56:1449-1462.
12. Baier M., Noctor G., Foyer C.H., Dietz K.J. Antisense suppression of 2-cysteine peroxiredoxin in Arabidopsis specifically enhances the activities and expression of enzymes associated with ascorbate metabolism but not glutathione metabolism. Plant Physiol 2000, 120:823-832.
13. Beale S.I. Chloroplast signaling: retrograde regulation revelations. Curr Biol 2011, 24:391-393.
14. Bedard J., Jarvis P. Recognition and envelope translocation of chloroplast preproteins. J Exp Bot 2005, 56:2287-2320.
15. Bhattacharjee S. The language of reactive oxygen species signaling in plants. J Bot 2012, 10.1155/2012/985298.
16. Biello D. How the first plant came to be. A genetic analysis reveals the ancient, complex - and symbiotic - roots of photosynthesis in plants. Nature 2012, 10.1038/nature.2012.10048.
17. Biswal B., Mohapatra P.K., Biswal U.C., Raval M.K. Leaf senescence and transformation of chloroplasts to gerontoplasts photosynthesis. Adv Photosynth Respir 2012, 34:217-230.
18. Bläsing O.E., Gibon Y., Günther M., Höhne M., Morcuende R., Osuna D., et al. Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis. Plant Cell 2005, 17:3257-3281.
19. Bock R. Structure, function, and inheritance of plastid genomes. Top Curr Genet 2007, 19:29-63.
20. Bonardi V., Pesaresi P., Becker T., Schleiff E., Wagner R., Pfannschmidt T., et al. Photosystem II core phosphorylation and photosynthetic acclimation require two different protein kinases. Nature 2005, 437:1179-1182.
21. Bowler C., Van Montagu M., Inze D. Superoxide dismutase and stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 1992, 43:83-116.
22. Bräutigam K., Dietzel L., Kleine T., Ströher E., Wormuth D., Dietz K.J., et al. Dynamic plastid redox signals integrate gene expression and metabolism to induce distinct metabolic states in photosynthetic acclimation in Arabidopsis. Plant Cell 2009, 21:2715-2732.
23. Bräutigam K., Dietzel L., Pfannschmidt T. Hypothesis - a binary redox control mode as universal regulator of photosynthetic light acclimation. Plant Signal Behav 2010, 5:81-85.
24. Brouwer B., Ziolkowska A., Bagard M., Keech O., Gardeström P. The impact of light intensity on shade-induced leaf senescence. Plant Cell Environ 2012, 35:1084-1098.
25. Burch-Smith T.M., Brunkard J.O., Choi Y.G., Zambryski P.C. Organelle-nucleus cross-talk regulates plant intercellular communication via plasmodesmata. Proc Natl Acad Sci USA 2011, 108:1451-1460.
26. Burch-Smith T.M., Zambryski P.C. Loss of INCREASED SIZE EXCLUSION LIMIT (ISE)1 or ISE2 increases the formation of secondary plasmodesmata. Curr Biol 2010, 20:989-993.
27. Cai G., Cresti M. Organelle motility in the pollen tube: a tale of 20 years. J Exp Bot 2009, 60:495-508.
28. Chang C.C.C., Slesak I., Jorda L., Sotnikov A., Melzer M., Miszalski Z., et al. Arabidopsis chloroplastic glutathione peroxidases play a role in cross talk between photooxidative stress and immune responses. Plant Physiol 2009, 150:670-683.
29. Chatterjee M., Sparvoli S., Edmunds C., Garosi P., Findlay K., Martin C. DAG, a gene required for chloroplast differentiation and palisade development in Antirrhinum majus. EMBO J 1996, 15:4194-4207.
30. Cheminant S., Wild M., Bouvier F., Pelletier S., Renou J.P., Erhardt M., et al. DELLAs regulate chlorophyll and carotenoid biosynthesis to prevent photooxidative damage during seedling deetiolation in Arabidopsis. Plant Cell 2011, 23:1849-1860.
31. Cottage A., Mott E.K., Kempster J.A., Gray J.C. The Arabidopsis plastid-signaling mutant gun1 (genomes uncoupled1) shows altered sensitivity to sucrose and abscisic acid and alterations in early seedling development. J Exp Bot 2010, 61:3773-3786.
32. Cruz J.A., Sacksteder C.A., Kanazawa A., Kramer D.M. Contribution of electric field (Dy) to steady-state transthylakoid proton motive force (pmf) in vitro and in vivo. Control of pmf parsing into Dy and DpH by ionic strength. Biochemistry 2001, 40:1226-1237.
33. Dietz K.J., Jacob S., Oelze M.L., Laxa M., Tognetti V., Nunes de Miranda S.M., et al. The function of peroxiredoxins in plant organelle redox metabolism. J Exp Bot 2006, 57:1697-1709.
34. Dietz K.J., Pfannschmidt T. Novel regulators in photosynthetic redox control of plant metabolism and gene expression. Plant Physiol 2011, 155:1477-1485.
35. Dixon D.P., Davis B.G., Edwards R. Functional divergence in the glutathione transferase superfamily in plants. Identification of two classes with putative functions in redox homeostasis in Arabidopsis thaliana. J Biol Chem 2002, 277:30859-30869.
36. Dong H., Deng Y., Mu J., Lu Q., Wang Y., Xu Y., et al. The Arabidopsis spontaneous cell death1 gene, encoding a z-carotene desaturase essential for carotenoid biosynthesis, is involved in chloroplast development, photoprotection and retrograde signaling. Cell Res 2007, 17:458-470.
37. Eckardt N.A. Retrograde signaling: a new candidate signaling molecule. Plant Cell 2011, 23:3870.
38. Eltayeb A.E., Yamamoto S., Habora M.E.E., Yin L., Tsujimoto H., Tanaka K. Transgenic potato overexpressing Arabidopsis cytosolic AtDHAR1 showed higher tolerance to herbicide, drought and salt stresses. Breed Sci 2011, 61:3-10.
39. Estavillo G.M., Crisp P.A., Pornsiriwong W., Wirtz M., Collinge D., Carrie C., et al. Evidence for a SAL1-PAP chloroplast retrograde pathway that functions in drought and high light signaling in Arabidopsis. Plant Cell 2011, 23:3992-4012.
40. Fernandez A.P., Strand A. Retrograde signalling and plant stress: plastid signals initiate cellular stress responses. Curr Opin Plant Biol 2008, 11:509-513.
41. Ferro M., Brugière S., Salvi D., Seigneurin-Berny D., Court M., Moyet L., et al. AT_CHLORO, a comprehensive chloroplast proteome database with subplastidial localization and curated information on envelope proteins. Mol Cell Proteomics 2010, 9:1063-1084.
42. Fischer B.B., Krieger-Liszkay A., Eggen R.L. Photosensitizers neutral red (type I) and rose bengal (type II) cause light-dependent toxicity in Chlamydomonas reinhardtii and induce the Gpxh gene via increased singlet oxygen formation. Environ Sci Technol 2004, 38:6307-6313.
43. Fischer B.B., Krieger-Liszkay A., Hideg E., Šnyrychová I., Wiesendanger M., Eggen R.I.L. Role of singlet oxygen in chloroplast to nucleus retrograde signaling in Chlamydomonas reinhardtii. FEBS Lett 2007, 581:5555-5560.
44. Fischer B.B., Wiesendanger M., Eggen R.I.L. Growth condition-dependent sensitivity, photodamage and stress response of Chlamydomonas reinhardtii exposed to high light conditions. Plant Cell Physiol 2006, 47:1135-1145.
45. Foyer C.H., Neukermans J., Queval G., Noctor G., Harbinson J. Photosynthetic control of electron transport and the regulation of gene expression. J Exp Bot 2012, 63:1637-1661.
46. Foyer C.H., Noctor G. Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 2011, 155:2-18.
47. Foyer C.H., Noctor G. Redox regulation in photosynthetic organisms: signaling, acclimation and practical implications. Antioxid Redox Signal 2009, 11:861-905.
48. Foyer C.H., Shigeoka S. Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol 2011, 155:93-100.
49. Fryer M.J., Ball L., Oxborough K., Karpiński S., Mullineaux P.M., Baker N.R. Control of ascorbate peroxidase 2 expression by hydrogen peroxide and leaf water status during excess light stress reveals a functional organization of Arabidopsis leaves. Plant J 2003, 33:691-705.
50. Gawroński P., Górecka M., Bederska M., Rusaczonek A., Ślesak I., Kruk J., et al. ISOCHORISMATE SYNTHASE 1 is required for thylakoid organization, optimal plastoquinone redox status and state transitions in Arabidopsis thaliana. J Exp Bot 2013.
51. Ghassemian M., Lutes J., Tepperman J.M., Chang H.S., Zhu T., Wang X., et al. Integrative analysis of transcript and metabolite profiling data sets to evaluate the regulation of biochemical pathways during photomorphogenesis. Arch Biochem Biophys 2006, 448:45-59.
52. 2*(1δ), in aqueous micellar systems. Photochem Photobiol 1976, 23:399-403.
53. Grabowski E., Miao Y., Mulisch M., Krupinska K. Single-stranded DNA-binding protein Whirly1 in barley leaves is located in plastids and the nucleus of the same cell. Plant Physiol 2008, 147:1800-1804.
54. Grieco M., Tikkanen M., Paakkarinen V., Kangasjärvi S., Aro E.M. Steady-state phosphorylation of light-harvesting complex II proteins preserves photosystem I under fluctuating white light. Plant Physiol 2012, 160:1896-1910.
55. Hanson M.R., Sattarzadeh A. Dynamic morphology of plastids and stromules in angiosperm plants. Plant Cell Environ 2008, 31:646-657.
56. Herbette S., Lenne C., Leblanc N., Julien J.L., Drevet J.R., Roeckel-Drevet P. Two GPX-like proteins from Lycopersicon esculentum and Helianthus annuus are antioxidant enzymes with phospholipid hydroperoxide glutathione peroxidase and thioredoxin peroxidase activities. Eur J Biochem 2002, 269:2414-2420.
57. Horling F., König J., Dietz K.J. Type II peroxiredoxin C, a member of the peroxiredoxin family of Arabidopsis thaliana: its expression and activity in comparison with other peroxiredoxins. Plant Physiol Biochem 2002, 40:491-499.
58. Hörtensteiner S., Feller U. Nitrogen metabolism and remobilization during senescence. J Exp Bot 2002, 53:927-937.
59. Hosler J.P., Yocum C.F. Regulation of cyclic photophosphorylation during ferredoxin-mediated electron transport: effect of DCMU and the NADPH/NADP ratio. Plant Physiol 1987, 83:965-969.
60. Inaba T., Schnell D.J. Protein trafficking to plastids: one theme, many variations. Biochem J 2008, 413:15-28.
61. Inaba T. Bilateral communication between plastid and the nucleus: plastid protein import and plastid-to-nucleus retrograde signaling. Biosci Biotechnol Biochem 2010, 74:471-476.
62. Jarvis P. Targeting of nucleus-encoded proteins to chloroplasts in plants. New Phytol 2008, 179:257-285.
63. Jung H.S., Chory J. Signaling between chloroplasts and the nucleus: can a systems biology approach bring clarity to a complex and highly regulated pathway?. Plant Physiol 2010, 152:453-459.
64. Kakizaki T., Yazu F., Nakayama K., Ito-Inaba Y., Inaba T. Plastid signalling under multiple conditions is accompanied by a common defect in RNA editing in plastids. J Exp Bot 2012, 63:251-260.
65. Kanervo E., Singh M., Suorsa M., Paakkarinen V., Aro E., Battchikova N., et al. Expression of protein complexes and individual proteins upon transition of etioplasts to chloroplasts in pea (Pisum sativum). Plant Cell Physiol 2008, 49:396-410.
66. Kangasjärvi S., Lepistö A., Hännikäinen K., Piippo M., Luomala E.M., Aro E.M., et al. Diverse roles for chloroplast stromal and thylakoid-bound ascorbate peroxidases in plant stress responses. Biochem J 2008, 412:275-285.
67. Kangasjärvi S., Nurmi M., Tikkanen M., Aro E.M. Cell-specific mechanisms and systemic signalling as emerging themes in light acclimation of C3 plants. Plant Cell Environ 2009, 32:1230-1240.
68. Karpiński S., Reynolds H., Karpinska B., Wingsle G., Creissen G., Mullineaux P. Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 1999, 284:654-657.
69. Karpiński S., Gabryś H., Karpińska B., Mullineaux P. Light perception in plant disease defence mechanisms. Curr Opin Plant Biol 2003, 6:390-396.
70. Karpiński S., Szechyńska-Hebda M., Wituszyńska W., Burdiak P. Light acclimation, retrograde signalling, cell death and immune defences in plants. Plant Cell Environ 2013, 36:736-744.
71. Karpiński S., Szechyńska-Hebda M. Secret life of plants: from memory to intelligence. Plant Behav Signal 2010, 5:1391-1394.
72. 2-mediated retrograde signaling during late embryogenesis predetermines plastid differentiation in seedlings by recruiting abscisic acid. Proc Natl Acad Sci USA 2009, 106:9920-9924.
73. Kindgren P., Kremnev D., Blanco N.E., Lopez J.D.B., Fernandez A.P., Tellgren-Roth C., et al. The plastid redox insensitive 2 mutant of Arabidopsis is impaired in PEP activity and high light-dependent plastid redox signalling to the nucleus. Plant J 2012, 70:279-291.
74. Kleine T., Kindgren P., Benedict C., Hendricksen L., Strand Å. Genome wide gene expression analysis reveals a critical role for CRYPTOCHROME1 in the response of Arabidopsis to high irradiance. Plant Physiol 2007, 144:1391-1406.
75. Kleine T., Maier U.G., Leister D. DNA transfer from organelles to the nucleus: the idiosyncratic genetics of endosymbiosis. Annu Rev Plant Biol 2009, 60:115-138.
76. Köhler R.H., Cao J., Zipfel W.R., Webb W.W., Hanson M.R. Exchange of protein molecules through connections between higher plant plastids. Science 1997, 276:2039-2042.
77. Köhler R.H., Schwille P., Webb W.W., Hanson M.R. Active protein transport through plastid tubules: velocity quantified by fluorescence correlation spectroscopy. J Cell Sci 2000, 113:3921-3930.
78. Koussevitzky S., Nott A., Mockler T.C., Hong F., Sachetto-Martins G., Surpin M., et al. Signals from chloroplasts converge to regulate nuclear gene expression. Science 2007, 316:715-719.
79. Krause K., Kilbienski I., Mulisch M., Rödiger A., Schäfer A., Krupinska K. DNA-binding proteins of the Whirly family in Arabidopsis thaliana are targeted to the organelles. FEBS Lett 2005, 579:3707-3712.
80. Krause K., Oetke S., Krupinska K. Dual targeting and retrograde translocation: regulators of plant nuclear gene expression can be sequestered by plastids. Int J Mol Sci 2012, 13:11085-11101.
81. Krupinska K., Mulisch M., Hollmann J., Tokarz K., Zschiesche W., Kage H., et al. An alternative strategy of dismantling of the chloroplasts during leaf senescence observed in a high-yield variety of barley. Physiol Plant 2012, 144:189-200.
82. Kuo W.Y., Huang C.H., Liu A.C., Cheng C.P., Li S.H., Chang W.C., et al. CHAPERONIN 20 mediates iron superoxide dismutase (FeSOD) activity independent of its co-chaperonin role in Arabidopsis chloroplasts. New Phytol 2013, 197:99-110.
83. Kwok E.Y., Hanson M.R. Plastids and stromules interact with the nucleus and cell membrane in vascular plants. Plant Cell Rep 2004, 23:188-195.
84. Kwok E.Y., Hanson M.R. GFP-labelled Rubisco and aspartate aminotransferase are present in plastid stromules and traffic between plastids. J Exp Bot 2004, 55:595-604.
85. Lake J.A., Quick W.P., Beerling D.J., Woodward F.I. Plant development - signals from mature to new leaves. Nature 2001, 411:154.
86. Laloi C., Stachowiak M., Pers-Kamczyc E., Warzych E., Murgia I., Apel K Cross-talk between singlet oxygen- and hydrogen peroxide-dependent signaling of stress responses in Arabidopsis thaliana. Proc Natl Acad Sci USA 2007, 104:672-677.
87. Lee K.P., Kim C., Landgraf F., Apel K. EXECUTER1- and EXECUTER2-dependent transfer of stress-related signals from the plastid to the nucleus of Arabidopsis thaliana. Proc Natl Acad Sci USA 2007, 104:10270-10275.
88. Lepistö A., Kangasjärvi S., Luomala E.M., Brader G., Sipari N., Keränen M., et al. Chloroplast NADPH-thioredoxin reductase interacts with photoperiodic development in Arabidopsis. Plant Physiol 2009, 149:1261-1276.
89. Lepistö A., Rintamäki E. Coordination of plastid and light signaling pathways upon development of Arabidopsis leaves under various photoperiods. Mol Plant 2012, 5:799-816.
90. Leterrier M., Corpas F.J., Barroso J.B., Sandalio L.M., del Rio L.A. Peroxisomal monodehydroascorbate reductase genomic clone characterization and functional analysis under environmental stress conditions. Plant Physiol 2005, 138:2111-2123.
91. Li Z., Wakao S., Fischer B.B., Niyogi K.K. Sensing and responding to excess light. Annu Rev Plant Biol 2009, 60:239-260.
92. Lim P.O., Kim H.J., Nam H.G. Leaf senescence. Ann Rev Plant Biol 2007, 58:115-136.
93. Livingston A.K., Cruz J.A., Kohzuma K., Dhingra A., Kramer D.M. An Arabidopsis mutant with high cyclic electron flow around photosystem I (hcef) involving the NADPH dehydrogenase complex. Plant Cell 2010, 22:221-233.
94. Marty L., Siala W., Schwarzlander M., Fricker M.D., Wirtz M., Sweetlove L.J., et al. The NADPH-dependent thioredoxin system constitutes a functional backup for cytosolic glutathione reductase in Arabidopsis. Proc Natl Acad Sci USA 2009, 106(22):9109-9114.
95. 2-triggered retrograde signaling from chloroplasts to nucleus plays a specific role in the response to stress. J Biol Chem 2012, 287:11717-11729.
96. Maruta T., Tanouchi A., Tamoi M., Yabuta Y., Yoshimura K., Ishikawa T., et al. Arabidopsis chloroplastic ascorbate peroxidase isoenzymes play a dual role in photoprotection and gene regulation under photooxidative stress. Plant Cell Physiol 2010, 51:190-200.
97. Mateo A., Mühlenbock P., Rustérucci C., Chi-Chen C., Miszalski Z., Karpinska B., et al. The LESION SIMULATING DISEASE (LSD1) gene is required for acclimation to conditions that promote excess excitation energy. Plant Physiol 2004, 136:2818-2830.
98. Matile P. Chloroplast senescence. Crop Photosynthesis: Spatial and Temporal Determinants 1992, 423-440. Elsevier, Amsterdam, The Netherlands. N.R. Baker, H. Thomas (Eds.).
99. Melotto M., Underwood W., Koczan J., Nomura K., He S.Y. Plant stomata function in innate immunity against bacterial invasion. Cell 2006, 126:969-980.
100. Mhamdi A., Hager J., Chaouch S., Queval G., Han Y., Taconnat L., et al. Glutathione peroxidase genes in Arabidopsis are ubiquitous and regulated by abiotic stresses through diverse signaling pathways. Plant J 2003, 36:602-615.
101. Mhamdi A., Hager J., Chaouch S., Queval G., Han Y., Taconnat L., et al. Arabidopsis GLUTATHIONE REDUCTASE 1 plays a crucial role in leaf responses to intracellular hydrogen peroxide and in ensuring appropriate gene expression through both salicylic acid and jasmonic acid signaling pathways. Plant Physiol 2010, 153:1144-1160.
102. Miller G., Schlauch K., Tam R., Cortes D., Torres M.A., Shulaev V., et al. The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci Signal 2009, 84:45.
103. Mochizuki N., Brusslan J.A., Larkin R., Nagatani A., Chory J. Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid- to-nucleus signal transduction. Proc Natl Acad Sci USA 2001, 98:2053-2058.
104. Mochizuki N., Tanaka R., Grimm B., Masuda T., Moulin M., Smith A.G., et al. The cell biology of tetrapyrroles: a life and death struggle. Trends Plant Sci 2010, 15:488-498.
105. Mochizuki N., Tanaka R., Tanaka T., Masuda T., Nagatani A The steady-state level of Mg-protoporphyrin IX is not a determinant of plastid-to-nucleus signalling in Arabidopsis. Proc Natl Acad Sci USA 2008, 105:15184-15189.
106. Monteiro G., Horta B.B., Pimenta D.C., Augusto O., Netto L.E.S. Reduction of 1-Cys peroxiredoxins by ascorbate changes the thiol-specific antioxidant paradigm, revealing another function of vitamin C. Proc Natl Acad Aci U S A 2007, 104:4886-4891.
107. Mühlenbock P., Plaszczyca M., Mellerowicz E., Karpiński S. Lysigenous aerenchyma formation in Arabidopsis is controlled by LESION SIMULATING DISEASE1. Plant Cell 2007, 19:3819-3830.
108. Mühlenbock P., Szechyńska-Hebda M., Płaszczyca M., Baudo M., Mullineaux P.M., Parker J.E., et al. Chloroplast signaling and LESION SIMULATING DISEASE1 regulate crosstalk between light acclimation and immunity in Arabidopsis. Plant Cell 2008, 20:2339-2356.
109. Mullineaux P.M., Karpiński S., Baker N.R. Spatial dependence for hydrogen peroxide-directed signaling in light-stressed plants. Plant Physiol 2006, 141:346-350.
110. Muthuramalingam M., Seidel T., Laxa M., Nunes de Miranda S.M., Gärtner F., Ströher E., et al. Multiple redox and non-redox interactions define 2-cys peroxiredoxin as a regulatory hub in the chloroplast. Mol Plant 2009, 2:1273-1288.
111. Myouga F., Hosoda C., Umezawa T., Iizumi H., Kuromori T., Motohashi R., et al. A heterocomplex of iron superoxide dismutases defends chloroplast nucleoids against oxidative stress and is essential for chloroplast development in Arabidopsis. Plant Cell 2008, 20:3148-3162.
112. Nicolai M., Nicolaï M., Roncato M.A., Canoy A.S., Rouquié D., Sarda X., et al. Large-scale analysis of mRNA translation states during sucrose starvation in Arabidopsis cells identifies cell proliferation and chromatin structure as targets of translational control. Plant Physiol 2006, 141:663-673.
113. Niyogi K.K. Safety valves for photosynthesis. Curr Opin Plant Biol 2000, 3:455-460.
114. Noctor G., Veljovic-Jovanovic S.D., Driscoll S., Novitskaya L., Foyer C.H. Drought and oxidative load in the leaves of C3 plants: a predominant role for photorespiration?. Ann Bot (Lond) 2002, 89:841-850.
115. Nott A., Jung H.S., Koussevitzky S., Chory J. Plastid-to-nucleus retrograde signaling. Ann Rev Plant Biol 2006, 57:739-759.
116. Oelze M.L., Vogel M.O., Alsharafa K., Kahmann U., Viehhauser A., Maurino V.G., et al. Efficient acclimation of the chloroplast antioxidant defence of Arabidopsis thaliana leaves in response to a 10- or 100-fold light increment and the possible involvement of retrograde signals. J Exp Bot 2012, 63:1297-1313.
117. op den Camp R.G., Przybyla D., Ochsenbein C., Laloi C., Kim C., Danon A., et al. Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell 2003, 15:2320-2332.
118. Peng L., Yamamoto H., Shikanai T. Structure and biogenesis of the chloroplast NAD(P)H dehydrogenase complex. Biochim Biophys Acta 2011, 1807:945-953.
119. Pesaresi P., Hertle A., Pribil M., Kleine T., Wagner R., Strissel H., et al. Arabidopsis STN7 kinase provides a link between short- and long-term photosynthetic acclimation. Plant Cell 2009, 21:2402-2423.
120. Petersson U.A., Kieselbach T., García-Cerdán J.G., Schröder W.P. The Prx Q protein of Arabidopsis thaliana is a member of the luminal chloroplast proteome. FEBS Lett 2006, 580:6055-6061.
121. Petrov V.D., Van Breusegem F. Hydrogen peroxide - a central hub for information flow in plant cells. AoB Plants 2012, 10.1093/aobpla/pls014.
122. Pfannschmidt T. Chloroplast redox signals: how photosynthesis controls its own genes. Trends Plant Sci 2003, 8:33-41.
123. Pfannschmidt T. Plastidial retrograde signalling - a true "plastid factor" or just metabolite signatures?. Trends Plant Sci 2010, 15:427-435.
124. Piippo M., Allahverdiyeva Y., Paakkarinen V., Suoranta U.M., Battchikova N., Aro E.M. Chloroplast-mediated regulation of nuclear genes in Arabidopsis thaliana in the absence of light stress. Physiol Genomics 2006, 25:142-152.
125. Pogson B.J., Woo N.S., Forster B., Small I.D. Plastid signalling to the nucleus and beyond. Trends Plant Sci 2008, 13:602-609.
126. Puthiyaveetil S., Ibrahim I.M., Allen J.F. Oxidation-reduction signalling components in regulatory pathways of state transitions and photosystem stoichiometry adjustment in chloroplasts. Plant Cell Environ 2012, 35:347-359.
127. Reiland S., Finazzi G., Endler A., Willig A., Baerenfaller K., Grossmann J., et al. Comparative phosphoproteome profiling reveals a function of the STN8 kinase in fine-tuning of cyclic electron flow (CEF). Proc Natl Acad Sci USA 2011, 108(31):12955-12960.
128. Richter R., Behringer C., Muller I.K., Schwechheimer C. The GATA-type transcription factors GNC and GNL/CGA1 repress gibberellin signaling downstream from DELLA proteins and PHYTOCHROME-INTERACTING FACTORS. Genes Dev 2010, 24:2093-2104.
129. Rintamäki E., Martinsuo P., Pursiheimo S., Aro E.M. Cooperative regulation of light-harvesting complex II phosphorylation via the plastoquinol and ferredoxin-thioredoxin system in chloroplasts. Proc Natl Acad Sci USA 2000, 97:11644-11649.
130. Rizhsky L., Liang H., Mittler L. The water-water-cycle is essential for chloroplast protection in the absence of stress. J Biol Chem 2003, 278:38921-38925.
131. Rodríguez-Concepción M. Early steps in isoprenoid biosynthesis: multilevel regulation of the supply of common precursors in plant cells. Phytochem Rev 2006, 5:1-15.
132. Rogalski M., Karcher D., Bock R. Superwobbling facilitates translation with reduced tRNA sets. Nat Struct Mol Biol 2008, 15:192-198.
133. Rogalski M., Schöttler M.A., Thiele W., Schulze W.X., Bock R. Rpl33, a nonessential plastid-encoded ribosomal protein in tobacco, is required under cold stress conditions. Plant Cell 2008, 20:2221-2237.
134. Rossel J.B., Wilson P.B., Hussain D., Woo N.S., Gordon M.J., Mewett O.P., et al. Systemic and intracellular response to photooxidative stress in Arabidopsis. Plant Cell 2007, 19:4091-4110.
135. Ruckle M.E., Burgoon L.D., Lawrence L.A., Sinkler C.A., Larkin R.M. Plastids are major regulators of light signaling in Arabidopsis. Plant Physiol 2012, 159:366-390.
136. Ruckle M.E., DeMarco S.M., Larkin R.M. Plastid signals remodel light signaling networks and are essential for efficient chloroplast biogenesis in Arabidopsis. Plant Cell 2007, 19:3944-3960.
137. Ruckle M.E., Larkin R.M. Plastid signals that affect photomorphogenesis in Arabidopsis thaliana are dependent on GENOMES UNCOUPLED 1 and cryptochrome 1. New Phytol 2009, 182:367-379.
138. Rumeau D., Peltier G., Cournac L. Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response. Plant Cell Environ 2007, 30:1041-1051.
139. Sakuraba Y., Balazadeh S., Tanaka R., Mueller-Roeber B., Tanaka A. Overproduction of Chl b retards senescence through transcriptional reprogramming in Arabidopsis. Plant Cell Physiol 2012, 53:505-517.
140. Sasaki-Sekimoto Y., Taki N., Obayashi T., Aono M., Matsumoto F., Sakurai N., et al. Coordinated activation of metabolic pathways for antioxidants and defence compounds by jasmonates and their roles in stress tolerance in Arabidopsis. Plant J 2005, 44:653-668.
141. Sirikhachornkit A., Niyogi K.K. Antioxidants and photo-oxidative stress responses in plants and algae. The Chloroplast Basics and Applications Series: Advances in Photosynthesis and Respiration 2010, vol. 31:389-390. p. XLII, 426.
142. Skovsen E., Snyder J.W., Lambert J.D.C., Ogilby P.R. Lifetime and diffusion of singlet oxygen in a cell. J Phys Chem B 2005, 109:8570-8573.
143. Stettler M., Eicke S., Mettler T., Messerli G., Hörtensteiner S., Zeeman S.C. Blocking the metabolism of starch breakdown products in Arabidopsis leaves triggers chloroplast degradation. Mol Plant 2009, 2:1233-1246.
144. Sun X., Feng P., Xu X., Guo H., Ma J., Chi W., et al. A chloroplast envelope-bound PHD transcription factor mediates chloroplast signals to the nucleus. Nat Commun 2011, 2:477. 10.1038/ncomms1486.
145. Suorsa M., Järvi S., Grieco M., Nurmi M., Pietrzykowska M., Rantala M., et al. PROTON GRADIENT REGULATION5 is essential for proper acclimation of Arabidopsis Photosystem I to naturally and artificially fluctuating light conditions. Plant Cell 2012, 24:2934-2948.
146. Suwa K., Kimura T., Schaap A.P. Reactivity of singlet molecular oxygen with cholesterol in a phospholipid membrane matrix. A model for oxidative damage of membranes. Biochem Biophys Res Commun 1979, 75:785-792.
147. Suzuki N., Koussevitzky S., Mittler R., Miller G. ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ 2012, 35:259-270.
148. Szechyńska-Hebda M., Kruk J., Gorecka M., Karpinska B., Karpiński S. Evidence for light wavelength-specific systemic photoelectrophysiological signalling and cellular light memory of excess light episode in Arabidopsis. Plant Cell 2010, 22:1-18.
149. Taniguchi M., Miyake H. Redox-shuttling between chloroplast and cytosol: integration of intra-chloroplast and extra-chloroplast metabolism. Curr Opin Plant Biol 2012, 15:252-260.
150. Thomas J., Weinstein J.D. Measurement of heme efflux and heme content in isolated developing chloroplasts. Plant Physiol 1990, 94:1414-1423.
151. Timmis J.N., Ayliffe M.A., Huang C.Y., Martin W. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 2004, 5:123-135.
152. Tirlapur U.K., Dahse I., Reiss B., Meurer J., Oelmuller R. Characterization of the activity of a plastid-targeted green fluorescent protein in Arabidopsis. Eur J Cell Biol 1999, 78:233-240.
153. Usadel B., Bläsing O.E., Gibon Y., Retzlaff K., Höhne M., Günther M., et al. Global transcript levels respond to small changes of the carbon status during a progressive exhaustion of carbohydrates in Arabidopsis rosettes. Plant Physiol 2008, 46:1834-1861.
154. Van Breusegem F., Bailey-Serres J., Mittler R. Unravelling the tapestry of networks involving reactive oxygen species in plants. Plant Physiol 2008, 147:978-984.
155. van Doorn W.G. Is the onset of senescence in leaf cells of intact plants due to low or high sugar levels?. J Exp Bot 2008, 59:1963-1972.
156. Vanderauwera S., Zimmermann P., Rombauts S., Vandenabeele S., Langebartels C., Gruissem W., et al. Genome-wide analysis of hydrogen peroxide-regulated gene expression in Arabidopsis reveals a high light-induced transcriptional cluster involved in anthocyanin biosynthesis. Plant Physiol 2005, 139:806-821.
157. Wada M., Kagawa T., Sato Y. Chloroplast movement. Ann Rev Plant Biol 2003, 54:455-468.
158. Wagstaff C., Yang T.J.W., Stead A.D., Buchanan-Wollaston V., Roberts J.A. A molecular and structural characterization of senescing Arabidopsis siliques and comparison of transcriptional profiles with senescing petals and leaves. Plant J 2009, 57:690-705.
159. Waters M.T., Wang P., Korkaric M., Capper R.G., Saunders N.J., Langdale J.A. GLK transcription factors coordinate expression of the photosynthetic apparatus in Arabidopsis. Plant Cell 2009, 21:1109-1128.
160. Wheeler G.L., Brownlee C. Evolution of calcium channels in plants and green algae. Trends Plant Sci 2008, 13:506-514.
161. Wilhelm C., Selmar D. Energy dissipation is an essential mechanism to sustain the viability of plants: the physiological limits of improved photosynthesis. J Plant Physiol 2011, 168:79-87.
162. Wituszyńska W., Slesak I., Vanderauwera S., Szechyńska-Hebda M., Kornas A., Van Der Kelen K., et al. Lesion simulating disease1, enhanced disease susceptibility1, and phytoalexin deficient4 conditionally regulate cellular signaling homeostasis, photosynthesis, water use efficiency, and seed yield in Arabidopsis. Plant Physiol 2013, 161:1795-1805.
163. Woodson J.-D., Perez-Ruiz J.M., Chory J. Heme synthesis by plastid ferrochelatase 1 regulates nuclear gene expression in plants. Curr Biol 2011, 21:897-903.
164. Woodson J.D., Perez-Ruiz J.M., Chory J. Heme synthesis by plastid ferrochelatase I regulates nuclear gene expression in plants. Curr Biol 2011, 21:897-903.
165. Xiao Y., Savchenko T., Baidoo E.E.K., Chehab W.E., Hayden D.M., Tolstikov V., et al. Retrograde signaling by the plastidial metabolite mecpp regulates expression of nuclear stress-response genes. Cell 2012, 149:1525-1535.
166. Yano S., Terashima I. Separate localization of light signal perception for sun or shade type chloroplast and palisade tissue differentiation in Chenopodium album. Plant Cell Physiol 2001, 42:1303-1310.
167. Yoshida S., Tamaoki M., Shikano T., Nakajima N., Ogawa D., Ioki M., et al. Cytosolic dehydroascorbate reductase is important for ozone tolerance in Arabidopsis thaliana. Plant Cell Physiol 2006, 47:304-308.
168. Yu F., Fu A., Aluru M., Park S., Xu Y., Liu H., et al. Variegation mutants and mechanisms of chloroplast biogenesis. Plant Cell Environ 2007, 30:350-365.
169. Yu H.D., Yang X.F., Chen S.T., Wang Y.T., Li J.K., Li J.K., et al. Downregulation of chloroplast RPS1 negatively modulates nuclear heat-responsive expression of HsfA2 and its target genes in Arabidopsis. PLoS Genet 2012, 8. 10.1371/journal.pgen.1002669.