Functional analysis of two isoforms of leaf-type ferredoxin-NADP+-oxidoreductase in rice using the heterologous expression system of arabidopsis

Plant Physiology

Volumn 157, Issue 1, 2011, Pages 96-108

  Higuchi Takeuchi, Mieko ^a   Ichikawa, Takanari ^b   Kondou, Youichi ^c   Matsui, Keiko ^a   Hasegawa, Yukako ^a   Kawashima, Mika ^a   Sonoike, Kintake ^d   Mori, Masaki ^e   Hirochika, Hirohiko ^e   Matsui, Minami ^a  

^a RIKEN   (Japan)

^b OKINAWA INSTITUTE OF SCIENCE AND TECHNOLOGY GRADUATE UNIVERSITY   (Japan)

^c KANTO GAKUIN UNIVERSITY   (Japan)

^d WASEDA UNIVERSITY   (Japan)

^e NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; ORYZA SATIVA;

EID: 80052402386     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.111.181248     Document Type: Article

References (54)

1. Albinsky D, Kusano M, Higuchi M, Hayashi N, Kobayashi M, Fukushima A, Mori M, Ichikawa T, Matsui K, Kuroda H, et al (2010) Metabolomic screening applied to rice FOX Arabidopsis lines leads to the identification of a gene-changing nitrogen metabolism. Mol Plant 3: 125-142
2. Allahverdiyeva Y, Mamedov F, Suorsa M, Styring S, Vass I, Aro EM (2007) Insights into the function of PsbR protein in Arabidopsis thaliana. Biochim Biophys Acta 1767: 677-685
3. Alte F, Stengel A, Benz JP, Petersen E, Soll J, Groll M, Bölter B (2010) Ferredoxin:NADPH oxidoreductase is recruited to thylakoids by binding to a polyproline type II helix in a pH-dependent manner. Proc Natl Acad Sci USA 107: 19260-19265
4. + reductases: a basal structural framework and a multiplicity of functions. FASEB J 11: 133-140
5. Asada K (2000) The water-water cycle as alternative photon and electron sinks. Philos Trans R Soc Lond B Biol Sci 355: 1419-1431
6. Benz JP, Lintala M, Soll J, Mulo P, Bölter B (2010) A new concept for ferredoxin-NADP(H) oxidoreductase binding to plant thylakoids. Trends Plant Sci 15: 608-613
7. Benz JP, Stengel A, Lintala M, Lee YH, Weber A, Philippar K, Gügel IL, Kaieda S, Ikegami T, Mulo P, et al (2009) Arabidopsis Tic62 and ferredoxin-NADP(H) oxidoreductase form light-regulated complexes that are integrated into the chloroplast redox poise. Plant Cell 21: 3965-3983
8. Breyton C, Nandha B, Johnson GN, Joliot P, Finazzi G (2006) Redox modulation of cyclic electron flow around photosystem I in C3 plants. Biochemistry 45: 13465-13475
9. + reductase catalytic mechanism. Eur J Biochem 270: 1900-1915
10. Clarke L, Carbon J (1976) A colony bank containing synthetic Col E1 hybrid plasmids representative of the entire E. coli genome. Cell 9: 91-99
11. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
12. DalCorso G, Pesaresi P, Masiero S, Aseeva E, Schunemann D, Finazzi G, Joliot P, Barbato R, Leister D (2008) A complex containing PGRL1 and PGR5 is involved in the switch between linear and cyclic electron flow in Arabidopsis. Cell 132: 273-285
13. Dobakova M, Sobotka R, Tichy M, Komenda J (2009) Psb28 protein is involved in the biogenesis of the photosystem II inner antenna CP47 (PsbB) in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 149: 1076-1086
14. Dubouzet JG, Maeda S, Sugano S, Ohtake M, Hayashi N, Ichikawa T, Kondou Y, Kuroda H, Horii Y, Matsui M, et al (2011) Screening for resistance against Pseudomonas syringae in rice-FOX Arabidopsis lines identified a putative receptor-like cytoplasmic kinase gene that confers resistance to major bacterial and fungal pathogens in Arabidopsis and rice. Plant Biotechnol J 9: 466-485
15. Guedeney G, Corneille S, Cuine S, Peltier G (1996) Evidence for an association of ndh B, ndh J gene products and ferredoxin-NAD Preductase as components of a chloroplastic NAD(P)H dehydrogenase complex. FEBS Lett 378: 277-280
16. + oxidoreductase in wheat leaves. J Exp Bot 58: 3971-3985
17. +-dependent ferredoxin oxidoreductase lead to impaired plant growth and restrict photosynthetic activity of transgenic tobacco plants. Plant J 29: 281-293
18. Hanke GT, Endo T, Satoh F, Hase T (2008a) Altered photosynthetic electron channelling into cyclic electron flow and nitrite assimilation in a mutant of ferredoxin:NADP(H) reductase. Plant Cell Environ 31: 1017-1028
19. Hanke GT, Hase T (2008b) Variable photosynthetic roles of two leaf-type ferredoxins in Arabidopsis, as revealed by RNA interference. Photochem Photobiol 84: 1302-1309
20. Hanke GT, Kurisu G, Kusunoki M, Hase T (2004) Fd:FNR electron transfer complexes: evolutionary refinement of structural interactions. Photosynth Res 81: 317-327
21. Hanke GT, Okutani S, Satomi Y, Takao T, Suzuki A, Hase T (2005) Multiple iso-proteins of FNR in Arabidopsis: evidence for different contributions to chloroplast function and nitrogen assimilation. Plant Cell Environ 28: 1146-1157
22. Higuchi M, Ozaki H, Matsui M, Sonoike K (2009) A T-DNA insertion mutant of AtHMA1 gene encoding a Cu transporting ATPase in Arabidopsis thaliana has a defect in the water-water cycle of photosynthesis. J Photochem Photobiol B 94: 205-213
23. Ichikawa T, Nakazawa M, Kawashima M, Iizumi H, Kuroda H, Kondou Y, Tsuhara Y, Suzuki K, Ishikawa A, Seki M, et al (2006) The FOX hunting system: an alternative gain-of-function gene hunting technique. Plant J 48: 974-985
24. Joet T, Cournac L, Peltier G, Havaux M (2002) Cyclic electron flow around photosystem I in C3 plants: in vivo control by the redox state of chloroplasts and involvement of the NADH-dehydrogenase complex. Plant Physiol 128: 760-769
25. Juric S, Hazler-Pilepi K, Tomasic A, Lepedus H, Jelicic B, Puthiyaveetil S, Bionda T, Vojta L, Allen JF, Schleiff E, et al (2009) Tethering of ferredoxin: NADP(+) oxidoreductase to thylakoid membranes is mediated by novel chloroplast protein TROL. Plant J 60: 783-794
26. Kondou Y, Higuchi M, Takahashi S, Sakurai T, Ichikawa T, Kuroda H, Yoshizumi T, Tsumoto Y, Horii Y, Kawashima M, et al (2009) Systematic approaches to using the FOX hunting system to identify useful rice genes. Plant J 57: 883-894
27. Kondou Y, Nakazawa M, Kawashima M, Ichikawa T, Yoshizumi T, Suzuki K, Ishikawa A, Koshi T, Matsui R, Muto S, et al (2008) RETARDED GROWTH OF EMBRYO1, a new basic helix-loop-helix protein, expresses in endosperm to control embryo growth. Plant Physiol 147: 1924-1935
28. Li XP, Bjorkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, Niyogi KK (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403: 391-395
29. Lintala M, Allahverdiyeva Y, Kangasjarvi S, Lehtimaki N, Keranen M, Rintamaki E, Aro EM, Mulo P (2009) Comparative analysis of leaf-type ferredoxin-NADP oxidoreductase isoforms in Arabidopsis thaliana. Plant J 57: 1103-1115
30. +-oxidoreductase using knock-out mutants of Arabidopsis. Plant J 49: 1041-1052
31. Meurer J, Meierhoff K, Westhoff P (1996) Isolation of high-chlorophyllfluorescence mutants of Arabidopsis thaliana and their characterization by spectroscopy, immunoblotting and northern hybridisation. Planta 198: 385-396
32. Munekage Y, Hojo M, Meurer J, Endo T, Tasaka M, Shikanai T (2002) PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110: 361-371
33. Nakamura H, Hakata M, Amano K, Miyao A, Toki N, Kajikawa M, Pang J, Higashi N, Ando S, Toki S, et al (2007) A genome-wide gain-of-function analysis of rice genes using the FOX-hunting system. Plant Mol Biol 65: 357-371
34. Niyogi KK, Bjorkman O, Grossman AR (1997) Chlamydomonas xanthophylls cycle mutants identified by video imaging of chlorophyll fluorescence quenching. Plant Cell 9: 1369-1380
35. Niyogi KK, Grossman AR, Bjorkman O (1998) Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 10: 1121-1134
36. Okegawa Y, Kagawa Y, Kobayashi Y, Shikanai T (2008) Characterization of factors affecting the activity of photosystem I cyclic electron transport in chloroplasts. Plant Cell Physiol 49: 825-834
37. Ozaki H, Ikeuchi M, Ogawa T, Fukuzawa H, Sonoike K (2007) Large-scale analysis of chlorophyll fluorescence kinetics in Synechocystis sp. PCC 6803: identification of the factors involved in the modulation of photosystem stoichiometry. Plant Cell Physiol 48: 451-458
38. Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975: 384-394
39. Rodriguez RE, Lodeyro A, Poli HO, Zurbriggen M, Peisker M, Palatnik JF, Tognetti VB, Tschiersch H, Hajirezaei MR, Valle EM, et al (2007) Transgenic tobacco plants overexpressing chloroplastic ferredoxin- NADP(H) reductase display normal rates of photosynthesis and increased tolerance to oxidative stress. Plant Physiol 143: 639-649
40. Sakurai I, Mizusawa N, Ohashi S, Kobayashi M, Wada H (2007) Effects of the lack of phosphatidylglycerol on the donor side of photosystem II. Plant Physiol 144: 1336-1346
41. Schreiber U, Klughammer C, Neubauer C (1988) Measuring P-700 absor- bance changes around 830 nm with a new type of pulse modulation system. Z Naturforsch Teil C 43: 686-698
42. Schurmann P, Buchanan BB (2008) The ferredoxin/thioredoxin system of oxygenic photosynthesis. Antioxid Redox Signal 10: 1235-1274
43. Shikanai T (2007) Cyclic electron transport around photosystem I: genetic approaches. Annu Rev Plant Biol 58: 199-217
44. Shikanai T, Endo T, Hashimoto T, Yamada Y, Asada K, Yokota A (1998) Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I. Proc Natl Acad Sci USA 95: 9705-9709
45. Shikanai T, Munekage Y, Shimizu K, Endo T, Hashimoto T (1999) Identification and characterization of Arabidopsis mutants with reduced quenching of chlorophyll fluorescence. Plant Cell Physiol 40: 1134-1142
46. Toki S, Hara N, Ono K, Onodera H, Tagiri A, Oka S, Tanaka H (2006) Early infection of scutellum tissue with Agrobacterium allows high-speed transformation of rice. Plant J 47: 969-976
47. Varotto C, Pesaresi P, Meurer J, Oelmuller R, Steiner-Lange S, Salamini F, Leister D (2000) Disruption of the Arabidopsis photosystem I gene psaE1 affects photosynthesis and impairs growth. Plant J 22: 115-124
48. Wingler A, Lea PJ, Quick WP, Leegood RC (2000) Photorespiration: metabolic pathways and their role in stress protection. Philos Trans R Soc Lond B Biol Sci 355: 1517-1529
49. Yokotani N, Higuchi M, Kondou Y, Ichikawa T, Iwabuchi M, Hirochika H, Matsui M, Oda K (2011) A novel chloroplast protein, CEST induces tolerance to multiple environmental stresses and reduces photooxidative damage in transgenic Arabidopsis. J Exp Bot 62: 557-569
50. Yokotani N, Ichikawa T, Kondou Y, Maeda S, Iwabuchi M, Mori M, Hirochika H, Matsui M, Oda K (2009a) Overexpression of a rice gene encoding a small C2 domain protein OsSMCP1 increases tolerance to abiotic and biotic stresses in transgenic Arabidopsis. Plant Mol Biol 71: 391-402
51. Yokotani N, Ichikawa T, Kondou Y, Matsui M, Hirochika H, Iwabuchi M, Oda K (2008) Expression of rice heat stress transcription factor OsHsfA2e enhances tolerance to environmental stresses in transgenic Arabidopsis. Planta 227: 957-967
52. Yokotani N, Ichikawa T, Kondou Y, Matsui M, Hirochika H, Iwabuchi M, Oda K (2009b) Tolerance to various environmental stresses conferred by the salt-responsive rice gene ONAC063 in transgenic Arabidopsis. Planta 229: 1065-1075
53. Zhang H, Cramer WA (2004) Purification and crystallization of the cytochrome b6f complex in oxygenic photosynthesis. Methods Mol Biol 274: 67-78
54. Zulfugarov IS, Ham OK, Mishra SR, Kim JY, Nath K, Koo HY, Kim HS, Moon YH, An G, Lee CH (2007) Dependence of reaction center-type energy-dependent quenching on photosystem II antenna size. Biochim Biophys Acta 1767: 773-780