A deficiency in chloroplastic ferredoxin 2 facilitates effective photosynthetic capacity during long-term high light acclimation in Arabidopsis thaliana

Plant Journal

Volumn 76, Issue 5, 2013, Pages 861-874

  Liu, Jun ^a   Wang, Peng ^a   Liu, Bing ^a   Feng, Dongru ^a   Zhang, Jie ^a   Su, Jianbin ^a   Zhang, Yang ^a   Wang, Jin Fa ^a   Wang, Hong Bin ^a  

^a SUN YAT SEN UNIVERSITY   (China)

Author keywords

Arabidopsis thaliana; ferredoxin 2 knockout; high light acclimation; PGR5 dependent cyclic electron flow; photosynthetic capacity; redox signaling

Indexed keywords

ARABIDOPSIS THALIANA; CYCLIC ELECTRON FLOW; FERREDOXIN 2 KNOCKOUT; HIGH LIGHTS; PHOTOSYNTHETIC CAPACITY; REDOX SIGNALING;

TRANSCRIPTION;

PLANTS (BOTANY);

ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN; FERREDOXIN; PGR5 PROTEIN, ARABIDOPSIS;

ACCLIMATIZATION; ARABIDOPSIS; ARABIDOPSIS THALIANA; ARTICLE; CHLOROPLAST; FERREDOXIN 2 KNOCKOUT; GENE INACTIVATION; GENETICS; HIGH LIGHT ACCLIMATION; LIGHT; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PGR5-DEPENDENT CYCLIC ELECTRON FLOW; PHOTOSYNTHESIS; PHOTOSYNTHETIC CAPACITY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; RADIATION EXPOSURE; REDOX SIGNALING;

ARABIDOPSIS THALIANA; FERREDOXIN 2 KNOCKOUT; HIGH LIGHT ACCLIMATION; PGR5-DEPENDENT CYCLIC ELECTRON FLOW; PHOTOSYNTHETIC CAPACITY; REDOX SIGNALING;

ACCLIMATIZATION; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHLOROPLASTS; FERREDOXINS; GENE KNOCKOUT TECHNIQUES; LIGHT; MOLECULAR SEQUENCE DATA; PHOTOSYNTHESIS; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; STRESS, PHYSIOLOGICAL;

EID: 84889101422     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12341     Document Type: Article

References (54)

1. Arnon, D.I., (1988) The discovery of ferredoxin: the photosynthetic path. Trends Biochem. Sci. 13, 30-33.
2. Baena-Gonzalez, E., and, Aro, E.M., (2002) Biogenesis, assembly and turnover of photosystem II units. Philos. Trans. R. Soc. Lond. B Biol. Sci. 357, 1451-1459; discussion 1459-1460.
3. Baier, M., and, Dietz, K.J., (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.
4. Baker, N. R., (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu. Rev. Plant Biol. 59, 89-113.
5. 2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 170, 489-504.
6. Blanco, N.E., Ceccoli, R.D., Segretin, M.E., Poli, H.O., Voss, I., Melzer, M., Bravo-Almonacid, F.F., Scheibe, R., Hajirezaei, M.R., and, Carrillo, N., (2011) Cyanobacterial flavodoxin complements ferredoxin deficiency in knocked-down transgenic tobacco plants. Plant J. 65, 922-935.
7. Blanco, N.E., Ceccoli, R.D., Via, M.V., Voss, I., Segretin, M.E., Bravo-Almonacid, F.F., Melzer, M., Hajirezaei, M.R., Scheibe, R., and, Hanke, G.T., (2013) Expression of the minor isoform pea ferredoxin in tobacco alters photosynthetic electron partitioning and enhances cyclic electron flow. Plant Physiol. 161, 866-879.
8. DalCorso, G., Pesaresi, P., Masiero, S., Aseeva, E., Schunemann, D., Finazzi, G., Joliot, P., Barbato, R., and, 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.
9. Dietz, K.J., (2003) Redox control, redox signaling, and redox homeostasis in plant cells. Int. Rev. Cytol. 228, 141-193.
10. Dietz, K.J., and, Pfannschmidt, T., (2011) Novel regulators in photosynthetic redox control of plant metabolism and gene expression. Plant Physiol. 155, 1477-1485.
11. Falk, S., Samson, G., Bruce, D., Huner, N.P.A., and, Laudenbach, D.E., (1995) Functional analysis of the iron-stress induced CP 439 polypeptide of PS II in the cyanobacterium Synechococcus sp PCC 7942. Photosynth. Res. 45, 51-60.
12. Fernandez, A.P., and, Strand, A., (2008) Retrograde signaling and plant stress: plastid signals initiate cellular stress responses. Curr. Opin. Plant Biol. 11, 509-513.
13. Foyer, C.H., Neukermans, J., Queval, G., Noctor, G., and, Harbinson, J., (2012) Photosynthetic control of electron transport and the regulation of gene expression. J. Exp. Bot. 63, 1637-1661.
14. Grieco, M., Tikkanen, M., Paakkarinen, V., Kangasjarvi, S., and, Aro, E.M., (2012) Steady-state phosphorylation of light-harvesting complex II proteins preserves photosystem I under fluctuating white light. Plant Physiol. 160, 1896-1910.
15. Hanke, G.T., and, Hase, T., (2008) Variable photosynthetic roles of two leaf-type ferredoxins in Arabidopsis, as revealed by RNA interference. Photochem. Photobiol. 84, 1302-1309.
16. Hanke, G.T., Kimata-Ariga, Y., Taniguchi, I., and, Hase, T., (2004) A post genomic characterization of Arabidopsis ferredoxins. Plant Physiol. 134, 255-264.
17. 2-free air. Plant Physiol. 97, 141-149.
18. Holtgrefe, S., Bader, K.P., Horton, P., Scheibe, R., von Schaewen, A., and, Backhausen, J.E., (2003) Decreased content of leaf ferredoxin changes electron distribution and limits photosynthesis in transgenic potato plants. Plant Physiol. 133, 1768-1778.
19. Huang, W., Zhang, S.B., and, Cao, K.F., (2010) Stimulation of cyclic electron flow during recovery after chilling-induced photoinhibition of PSII. Plant Cell Physiol. 51, 1922-1928.
20. Hutin, C., Nussaume, L., Moise, N., Moya, I., Kloppstech, K., and, Havaux, M., (2003) Early light-induced proteins protect Arabidopsis from photooxidative stress. Proc. Natl Acad. Sci. USA, 100, 4921-4926.
21. Iida, A., Kazuoka, T., Torikai, S., Kikuchi, H., and, Oeda, K., (2000) A zinc finger protein RHL41 mediates the light acclimatization response in Arabidopsis. Plant J. 24, 191-203.
22. Joliot, P., and, Johnson, G.N., (2011) Regulation of cyclic and linear electron flow in higher plants. Proc. Natl Acad. Sci. USA, 108, 13317-13322.
23. Keren, N., Ohkawa, H., Welsh, E.A., Liberton, M., and, Pakrasi, H.B., (2005) Psb29, a conserved 22-kD protein, functions in the biogenesis of photosystem II complexes in Synechocystis and Arabidopsis. Plant Cell, 17, 2768-2781.
24. Kim, J., and, Mayfield, S.P., (1997) Protein disulphide isomerase as a regulator of chloroplast translational activation. Science, 278, 1954-1957.
25. Koussevitzky, S., Nott, A., Mockler, T.C., Hong, F., Sachetto-Martins, G., Surpin, M., Lim, J., Mittler, R., and, Chory, J., (2007) Signals from chloroplasts converge to regulate nuclear gene expression. Science, 316, 715-719.
26. A redox state and excitation energy fluxes. Photosynth. Res. 79, 209-218.
27. Li, Z., Wakao, S., Fischer, B.B., and, Niyogi, K.K., (2009) Sensing and responding to excess light. Annu. Rev. Plant Biol. 60, 239-260.
28. Long, T.A., Okegawa, Y., Shikanai, T., Schmidt, G.W., and, Covert, S.F., (2008) Conserved role of PROTON GRADIENT REGULATION 5 in the regulation of PSI cyclic electron transport. Planta, 228, 907-918.
29. Lu, Y., Hall, D.A., and, Last, R.L., (2011) A small zinc finger thylakoid protein plays a role in maintenance of photosystem II in Arabidopsis thaliana. Plant Cell, 23, 1861-1875.
30. Mazouni, K., Domain, F., Chauvat, F., and, Cassier-Chauvat, C., (2003) Expression and regulation of the crucial plant-like ferredoxin of cyanobacteria. Mol. Microbiol. 49, 1019-1029.
31. Muller, P., Li, X.P., and, Niyogi, K.K., (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol. 125, 1558-1566.
32. Munekage, Y., Hojo, M., Meurer, J., Endo, T., Tasaka, M., and, 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. Munekage, Y., Hashimoto, M., Miyake, C., Tomizawa, K., Endo, T., Tasaka, M., and, Shikanai, T., (2004) Cyclic electron flow around photosystem I is essential for photosynthesis. Nature, 429, 579-582.
34. Nelson, N., and, Yocum, C.F., (2006) Structure and function of photosystems I and II. Annu. Rev. Plant Biol. 57, 521-565.
35. Niyogi, K.K., Grossman, A.R., and, 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. Nott, A., Jung, H.S., Koussevitzky, S., and, Chory, J., (2006) Plastid-to-nucleus retrograde signaling. Annu. Rev. Plant Biol. 57, 739-759.
37. Oelze, M.L., Vogel, M.O., Alsharafa, K., Kahmann, U., Viehhauser, A., Maurino, V.G., and, Dietz, K.J., (2012) 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. 63, 1297-1313.
38. Okegawa, Y., Kagawa, Y., Kobayashi, Y., and, Shikanai, T., (2008) Characterization of factors affecting the activity of photosystemI cyclic electron transport in chloroplasts. Plant Cell Physiol. 49, 825-834.
39. Peng, L., Shimizu, H., and, Shikanai, T., (2008) The chloroplast NAD(P)H dehydrogenase complex interacts with photosystem I in Arabidopsis. J. Biol. Chem. 283, 34873-34879.
40. Pfannschmidt, T., Schutze, K., Brost, M., and, Oelmuller, R., (2001) A novel mechanism of nuclear photosynthesis gene regulation by redox signals from the chloroplast during photosystem stoichiometry adjustment. J. Biol. Chem. 276, 36125-36130.
41. Pogson, B.J., Woo, N.S., Forster, B., and, Small, I.D., (2008) Plastid signalling to the nucleus and beyond. Trends Plant Sci. 13, 602-609.
42. Pribil, M., Pesaresi, P., Hertle, A., Barbato, R., and, Leister, D., (2010) Role of plastid protein phosphatase TAP38 in LHCII dephosphorylation and thylakoid electron flow. PLoS Biol. 8, e1000288.
43. Rochaix, J.D., (2011) Assembly of the photosynthetic apparatus. Plant Physiol. 155, 1493-1500.
44. Rossel, J.B., Wilson, P.B., Hussain, D., Woo, N.S., Gordon, M.J., Mewett, O.P., Howell, K.A., Whelan, J., Kazan, K., and, Pogson, B.J., (2007) Systemic and intracellular responses to photooxidative stress in Arabidopsis. Plant Cell, 19, 4091-4110.
45. Scheibe, R., and, Dietz, K.J., (2012) Reduction-oxidation network for flexible adjustment of cellular metabolism in photoautotrophic cells. Plant, Cell Environ. 35, 202-216.
46. Shikanai, T., (2007) Cyclic electron transport around photosystem I: genetic approaches. Annu. Rev. Plant Biol. 58, 199-217.
47. Suorsa, M., Jarvi, S., Grieco, M., et al. (2012) PROTON GRADIENT REGULATION5 is essential for proper acclimation of Arabidopsis photosystem I to naturally and artificially fluctuating light conditions. Plant Cell, 24, 2934-2948.
48. Tognetti, V.B., Palatnik, J.F., Fillat, M.F., Melzer, M., Hajirezaei, M.R., Valle, E.M., and, Carrillo, N., (2006) Functional replacement of ferredoxin by a cyanobacterial flavodoxin in tobacco confers broad-range stress tolerance. Plant Cell, 18, 2035-2050.
49. Voss, I., Koelmann, M., Wojtera, J., Holtgrefe, S., Kitzmann, C., Backhausen, J.E., and, Scheibe, R., (2008) Knockout of major leaf ferredoxin reveals new redox-regulatory adaptations in Arabidopsis thaliana. Physiol. Plant. 133, 584-598.
50. Voss, I., Goss, T., Murozuka, E., Altmann, B., McLean, K.J., Rigby, S.E., Munro, A.W., Scheibe, R., Hase, T., and, Hanke, G.T., (2011) FdC1, a novel ferredoxin protein capable of alternative electron partitioning, increases in conditions of acceptor limitation at photosystem I. J. Biol. Chem. 286, 50-59.
51. Yao, C.W., Hsu, B.D., and, Chen, B.S., (2011) Constructing gene regulatory networks for long term photosynthetic light acclimation in Arabidopsis thaliana. BMC Bioinformatics, 12, 335.
52. Zeng, X. Q., Chow, W. S., Su, L. J., Peng, X. X., and, Peng, C. L., (2010) Protective effect of supplemental anthocyanins on Arabidopsis leaves under high light. Physiol. Plant. 138, 215-225.
53. Zimmermann, P., Hirsch-Hoffmann, M., Hennig, L., and, Gruissem, W., (2004) Genevestigator. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136, 2621-2632.
54. Zurbriggen, M.D., Tognetti, V.B., and, Carrillo, N., (2007) Stress-inducible flavodoxin from photosynthetic microorganisms. The mystery of flavodoxin loss from the plant genome. IUBMB Life, 59, 355-360.