An Arabidopsis soluble chloroplast proteomic analysis reveals the participation of the Executer pathway in response to increased light conditions

Journal of Experimental Botany

Volumn 66, Issue 7, 2015, Pages 2067-2077

  Uberegui, Estefanía ^a,b   Hall, Michael ^b   Lorenzo, Óscar ^c   Schröder, Wolfgang P ^b   Balsera, Mónica ^a  

^a INSTITUTO DE RECURSOS NATURALES Y AGROBIOLOGÍA DE SALAMANCA   (Spain)

^b UMEÅ UNIVERSITY   (Sweden)

^c UNIVERSITY OF SALAMANCA   (Spain)

Author keywords

Abiotic stress; acclimation response; chloroplast metabolism; DIGE; light; retrograde signalling; ROS

Indexed keywords

ARABIDOPSIS;

ARABIDOPSIS PROTEIN; PROTEOME; SINGLET OXYGEN;

ACCLIMATIZATION; ARABIDOPSIS; CHLOROPLAST; GENE EXPRESSION REGULATION; GENETICS; LIGHT; METABOLISM; PHOTOSYNTHESIS; PHYSIOLOGICAL STRESS; PROTEOMICS; RADIATION RESPONSE; SIGNAL TRANSDUCTION;

ACCLIMATIZATION; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHLOROPLASTS; GENE EXPRESSION REGULATION, PLANT; LIGHT; PHOTOSYNTHESIS; PROTEOME; PROTEOMICS; SIGNAL TRANSDUCTION; SINGLET OXYGEN; STRESS, PHYSIOLOGICAL;

EID: 84928902114     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erv018     Document Type: Article

References (76)

1. Alonso JM, Stepanova AN, Leisse TJ et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301, 653-657
2. Apel K. (2004). Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55, 373-399
3. Asada K. (2006). Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiology 141, 391-396
4. Barajas-López JdD, Blanco NE, Strand Å. (2013). Plastid-To-nucleus communication, signals controlling the running of the plant cell. Biochimica et Biophysica Acta (BBA)-Molecular Cell Research 1833, 425-437
5. Baruah A, Šimková K, Apel K, Laloi C. (2009). Arabidopsis mutants reveal multiple singlet oxygen signaling pathways involved in stress response and development. Plant Molecular Biology 70, 547-563
6. Bilger W, Björkman O. (1990). Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynthesis Research 25, 173-185
7. Bradford MM. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248-254
8. Bricker TM, Roose JL, Fagerlund RD, Frankel LK, Eaton-Rye JJ. (2012). The extrinsic proteins of Photosystem II. Biochimica et Biophysica Acta (BBA)-Bioenergetics 1817, 121-142
9. Buchert F, Forreiter C. (2010). Singlet oxygen inhibits ATPase and proton translocation activity of the thylakoid ATP synthase CF1CFo. FEBS Letters 584, 147-152
10. Buchert F, Schober Y, Römpp A, Richter ML, Forreiter C. (2012). Reactive oxygen species affect ATP hydrolysis by targeting a highly conserved amino acid cluster in the thylakoid ATP synthase ? subunit. Biochimica et Biophysica Acta (BBA)-Bioenergetics 1817, 2038-2048
11. Chi W, Sun X, Zhang L (2013). Intracellular signaling from plastid to nucleus. Annual Review of Plant Biology 64, 559-582
12. Estavillo GM, Crisp PA, Pornsiriwong W, Wirtz M, Collinge D, Carrie C, Giraud E, Whelan J, David P, Javot H, Brearley C, Hell R, Marin E, Pogson BJ. (2011). Evidence for a SAL1-PAP chloroplast retrograde pathway that functions in drought and high light signaling in Arabidopsis. The Plant Cell Online 23, 3992-4012
13. Ettinger WF, Theg SM. (1991). Physiologically active chloroplasts contain pools of unassembled extrinsic proteins of the photosynthetic oxygenevolving enzyme complex in the thylakoid lumen. The Journal of Cell Biology 115, 321-328
14. Fett JP, Coleman JR. (1994). Characterization and expression of two cDNAs encoding carbonic anhydrase in Arabidopsis thaliana. Plant Physiology 105, 707-713
15. Foyer CH, Noctor G. (2009). Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxidants& Redox Signaling 11, 861-905
16. Fryer MJ, Oxborough K, Mullineaux PM, Baker NR. (2002). Imaging of photo-oxidative stress responses in leaves. Journal of Experimental Botany 53, 1249-1254
17. Gadjev I, Vanderauwera S, Gechev TS, Laloi C, Minkov IN, Shulaev V, Apel K, Inzé D, Mittler R, Van Breusegem F. (2006). Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiology 141, 436-445
18. Galvez-Valdivieso G, Fryer MJ, Lawson T, Slattery K, Truman W, Smirnoff N, Asami T, Davies WJ, Jones AM, Baker NR, Mullineaux PM. (2009). The high light response in Arabidopsis involves ABA signaling between vascular and bundle sheath cells. The Plant Cell Online 21, 2143-2162
19. Galvez-Valdivieso G, Mullineaux PM. (2010). The role of reactive oxygen species in signalling from chloroplasts to the nucleus. Physiologia Plantarum 138, 430-439
20. Genty B, Briantais J-M, Baker NR. (1989). The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta (BBA)-General Subjects 990, 87-92
21. Gollnick K. (2007). Type II photooxygenation reactions in solution. Advances in Photochemistry. John Wiley & Sons, Inc., pp 1-122
22. Haake V, Geiger M, Walch-Liu P, Of Engels C, Zrenner R, Stitt M. (1999). Changes in aldolase activity in wild-Type potato plants are important for acclimation to growth irradiance and carbon dioxide concentration, because plastid aldolase exerts control over the ambient rate of photosynthesis across a range of growth conditions. The Plant Journal 17, 479-489
23. Haake V, Haake V, Zrenner R, Sonnewald U, Stitt M. (1998). A moderate decrease of plastid aldolase activity inhibits photosynthesis, alters the levels of sugars and starch, and inhibits growth of potato plants. The Plant Journal 14, 147-157
24. Hall M, Mishra Y, Schröder W. (2011). Preparation of stroma, thylakoid membrane, and lumen fractions from Arabidopsis thaliana chloroplasts for proteomic analysis. In: Jarvis RP, ed. Chloroplast Research in Arabidopsis, 775. Humana Press, pp 207-222
25. Henkes S, Sonnewald U, Badur R, Flachmann R, Stitt M. (2001). A small cecrease of plastid transketolase activity in antisense tobacco transformants has dramatic effects on photosynthesis and phenylpropanoid metabolism. The Plant Cell Online 13, 535-551
26. Ishikawa A, Tanaka H, Kato C, Iwasaki Y, Asahi T. (2005). Molecular characterization of the ZKT gene encoding a protein with PDZ, K-Box, and TPR motifs in Arabidopsis. Bioscience, Biotechnology, and Biochemistry 69, 972-978
27. Kangasjärvi S, Nurmi M, Tikkanen M, Aro E-M. (2009). Cell-specific mechanisms and systemic signalling as emerging themes in light acclimation of C3 plants. Plant, Cell and Environment 32, 1230-1240
28. Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen G, Mullineaux P. (1999). Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284, 654-657
29. Karpinski S, Szechynska-Hebda M, Wituszynska W, Burdiak P. (2013). Light acclimation, retrograde signalling, cell death and immune defences in plants. Plant Cell and Environment 36, 736-744
30. Kim C, Apel K. (2013). 1O2-mediated and EXECUTER-dependent retrograde plastid-To-nucleus signaling in norflurazon-Treated seedlings of Arabidopsis thaliana. Molecular Plant 6, 1580-1591
31. Kim C, Apel K. (2013). Singlet oxygen-mediated signaling in plants: moving from flu to wild type reveals an increasing complexity. Photosynthesis Research 116, 455-464
32. Kim C, Lee KP, Baruah A, Nater M, Göbel C, Feussner I, Apel K. (2009). 1O2-mediated retrograde signaling during late embryogenesis predetermines plastid differentiation in seedlings by recruiting abscisic acid. Proceedings of the National Academy of Sciences 106, 9920-9924
33. Kim C, Meskauskiene R, Zhang S, Lee KP, Lakshmanan Ashok M, Blajecka K, Herrfurth C, Feussner I, Apel K. (2012). Chloroplasts of Arabidopsis are the source and a primary target of a plant-specific programmed cell death signaling pathway. The Plant Cell Online 24, 3026-3039
34. Kohzuma K, Dal Bosco C, Meurer J, Kramer DM. (2013). Light-And metabolism-related regulation of the chloroplast ATP synthase has distinct mechanisms and functions. Journal of Biological Chemistry 288, 13156-13163
35. Kosová K, Vítámvás P, PráŠil IT, Renaut J. (2011). Plant proteome changes under abiotic stress-Contribution of proteomics studies to understanding plant stress response. Journal of Proteomics 74, 1301-1322
36. 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
37. Krieger-Liszkay A, Fufezan C, Trebst A. (2008). Singlet oxygen production in photosystem II and related protection mechanism. Photosynthesis Research 98, 551-564
38. Laloi C, Przybyla D, Apel K. (2006). A genetic approach towards elucidating the biological activity of different reactive oxygen species in Arabidopsis thaliana. Journal of Experimental Botany 57, 1719-1724
39. 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. Proceedings of the National Academy of Sciences 104, 672-677
40. Ledford HK, Chin BL, Niyogi KK. (2007). Acclimation to singlet oxygen stress in Chlamydomonas reinhardtii. Eukaryotic Cell 6, 919-930
41. 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. Proceedings of the National Academy of Sciences 104, 10270-10275
42. Lintala M, Allahverdiyeva Y, Kangasjärvi S, Lehtimäki N, Keränen M, Rintamäki E, Aro EM, Mulo P. (2009). Comparative analysis of leaf-Type ferredoxin-NADP+ oxidoreductase isoforms in Arabidopsis thaliana. Plant Journal 57, 1103-1115
43. Marín-Navarro J, Manuell A, Wu J, P. Mayfield S. (2007). Chloroplast translation regulation. Photosynthesis Research 94, 359-374
44. 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. Proceedings of the National Academy of Sciences 98, 12826-12831
45. Michelet L, Zaffagnini M, Morisse S, Sparla F, Pérez-Pérez ME, Francia F, Danon A, Marchand C, Fermani S, Trost P, Lemaire SD. (2013). Redox regulation of the Calvin-Benson cycle: something old, something new. Frontiers in Plant Science 4, 470
46. Miflin BJ, Habash DZ. (2002). The role of glutamine synthetase and glutamate dehydrogenase in nitrogen assimilation and possibilities for improvement in the nitrogen utilization of crops. Journal of Experimental Botany 53, 979-987
47. Mur LAJ, Aubry S, Mondhe M, Kingston Smith A, Gallagher J, Timms-Taravella E, Timms Taravella E, James C, Papp I, Hörtensteiner S, Thomas H, Ougham H. (2010). Accumulation of chlorophyll catabolites photosensitizes the hypersensitive response elicited by Pseudomonas syringae in Arabidopsis. New Phytologist 188, 161-174
48. Ng S, De Clercq I, Van Aken O, Law SR, Ivanova A, Willems P, Giraud E, Van Breusegem F, Whelan J. (2014). Anterograde and retrograde regulation of nuclear genes encoding mitochondrial proteins during growth, development, and stress. Molecular Plant 7, 1075-1093
49. Nott A, Jung H-S, Koussevitzky S, Chory J. (2006). Plastid-To-nucleus retrograde signaling. Annual Review of Plant Biology 57, 739-759
50. op den Camp RGL, Przybyla D, Ochsenbein C, Laloi C, Kim C, Danon A, Wagner D, Hideg É, Göbel C, Feussner I, Nater M, Apel K. (2003). Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. The Plant Cell Online 15, 2320-2332
51. Paul M, Driscoll S, Andralojc PJ et al. (2000). Decrease of phosphoribulokinase activity by antisense RNA in transgenic tobacco: definition of the light environment under which phosphoribulokinase is not in large excess. Planta 211, 112-119
52. Pesaresi P, Hertle A, Pribil M, Kleine T, Wagner R, Strissel H, Ihnatowicz A, Bonardi V, Scharfenberg M, Schneider A, Pfannschmidt T, Leister D. (2009). Arabidopsis STN7 kinase provides a link between short-And long-Term photosynthetic acclimation. The Plant Cell Online 21, 2402-2423
53. Petrillo E, Godoy Herz MA, Fuchs A, Reifer D, Fuller J, Yanovsky MJ, Simpson C, Brown JWS, Barta A, Kalyna M, Kornblihtt AR. (2014). A chloroplast retrograde signal regulates nuclear alternative splicing. Science 344, 427-430
54. Pfalz J, Liebers M, Hirth M, Gruebler B, Holtzegel U, Schroeter Y, Dietzel L, Pfannschmidt T. (2012). Environmental control of plant nuclear gene expression by chloroplast redox signals. Frontiers in Plant Science 3
55. Pfannschmidt T. (2010). Plastidial retrograde signalling-A true 'plastid factor' or just metabolite signatures? Trends in Plant Science 15, 427-435
56. Pogson BJ, Albrecht V. (2011). Genetic dissection of chloroplast biogenesis and development: An overview. Plant Physiology 155, 1545-1551
57. Portis A, Jr. (2003). Rubisco activase-Rubisco's catalytic chaperone. Photosynthesis Research 75, 11-27
58. Przybyla D, Göbel 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. The Plant Journal 54, 236-248
59. Qi Y, Armbruster U, Schmitz-Linneweber C, Delannoy E, de Longevialle AF, Rühle T, Small I, Jahns P, Leister D. (2012). Arabidopsis CSP41 proteins form multimeric complexes that bind and stabilize distinct plastid transcripts. Journal of Experimental Botany 63, 1251-1270
60. Raines C. (2003). The Calvin cycle revisited. Photosynthesis Research 75, 1-10
61. Ramel F, Birtic S, Ginies C, Soubigou-Taconnat L, Triantaphylidès C, Havaux M. (2012). Carotenoid oxidation products are stress signals that mediate gene responses to singlet oxygen in plants. Proceedings of the National Academy of Sciences 109, 5535-5540
62. Rolland F, Baena-Gonzalez E, Sheen J. (2006). Sugar sensing and signaling in plants: Conserved and novel mechanisms. Annual Review of Plant Biology 57, 675-709
63. Schubert M, Petersson UA, Haas BJ, Funk C, Schröder WP, Kieselbach T. (2002). Proteome map of the chloroplast lumen of Arabidopsis thaliana. Journal of Biological Chemistry 277, 8354-8365
64. Strand A, Asami T, Alonso J, Ecker JR, Chory J. (2003). Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrinIX. Nature 421, 79-83
65. Sun X, Feng P, Xu X, Guo H, Ma J, Chi W, Lin R, Lu C, Zhang L (2011). A chloroplast envelope-bound PHD transcription factor mediates chloroplast signals to the nucleus. Nature Communications 2, 477
66. Tanaka R, Kobayashi K, Masuda T. (2011). Tetrapyrrole metabolism in Arabidopsis thaliana. The Arabidopsis Book 9, e0145
67. Tetlow IJ, Rawsthorne S, Raines C, Emes MJ. (2005). Plastid metabolic pathways. Annual Plant Reviews 13, 60-125
68. Uematsu K, Suzuki N, Iwamae T, Inui M, Yukawa H. (2012). Increased fructose 1, 6-bisphosphate aldolase in plastids enhances growth and photosynthesis of tobacco plants. Journal of Experimental Botany 63, 3001-3009
69. Wagner D, Przybyla D, op den Camp R, Kim C, Landgraf F, Lee KP, Würsch M, Laloi C, Nater M, Hideg E, Apel K. (2004). The genetic basis of singlet oxygen induced stress responses of Arabidopsis thaliana. Science 306, 1183-1185
70. Weigel D. (2002). CTAB DNA miniprep. In: Curtis S, ed. Arabidopsis: a Laboratory Manual, 165. New York: Cold Spring Harbor Laboratory Press
71. Woodson JD, Chory J. (2008). Coordination of gene expression between organellar and nuclear genomes. Nature Reviews Genetics 9, 383-395
72. Woodson Jesse D, Perez-Ruiz Juan M, Chory J. (2011). Heme synthesis by plastid ferrochelatase i regulates nuclear gene expression in plants. Current Biology 21, 897-903
73. Xiao Y, Savchenko T, Baidoo Edward EK, Chehab Wassim E, Hayden Daniel M, Tolstikov V, Corwin Jason A, Kliebenstein Daniel J, Keasling Jay D, Dehesh K. (2012). Retrograde signaling by the plastidial metabolite MEcPP regulates expression of nuclear stressresponse genes. Cell 149, 1525-1535
74. Yamaguchi K, Subramanian AR. (2003). Proteomic identification of all plastid-specific ribosomal proteins in higher plant chloroplast 30S ribosomal subunit. European Journal of Biochemistry 270, 190-205
75. Zhang Z-W, Yuan S, Feng H, Xu F, Cheng J, Shang J, Zhang D-W, Lin H-H. (2011). Transient accumulation of Mg-protoporphyrin IX regulates expression of PhANGs-New evidence for the signaling role of tetrapyrroles in mature Arabidopsis plants. Journal of Plant Physiology 168, 714-721
76. Zhang Z-W, Yuan S, Xu F, Yang H, Zhang N-H, Cheng J, Lin H-H. (2010). The plastid hexokinase pHXK: A node of convergence for sugar and plastid signals in Arabidopsis. FEBS Letters 584, 3573-3579