The Arabidopsis nox mutant lacking carotene hydroxylase activity reveals a critical role for xanthophylls in photosystem I biogenesis

Plant Cell

Volumn 25, Issue 2, 2013, Pages 591-608

  Dall'Osto, Luca ^a   Piques, Maria ^b   Ronzani, Michela ^a   Molesini, Barbara ^a   Alboresi, Alessandro ^a   Cazzaniga, Stefano ^a   Bassia, Roberto ^a,c  

^a UNIVERSITY OF VERONA   (Italy)

^b MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^c FORSCHUNGSZENTRUM JÜLICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84875511436     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.112.108621     Document Type: Article

References (99)

1. Ahn, T.K., Avenson, T.J., Ballottari, M., Cheng, Y.C., Niyogi, K.K., Bassi, R., and Fleming, G.R. (2008). Architecture of a chargetransfer state regulating light harvesting in a plant antenna protein. Science 320: 794-797.
2. Alboresi, A., Ballottari, M., Hienerwadel, R., Giacometti, G.M., and Morosinotto, T. (2009). Antenna complexes protect photosystem I from photoinhibition. BMC Plant Biol. 9: 71.
3. Albus, C.A., Ruf, S., Schöttler, M.A., Lein, W., Kehr, J., and Bock, R. (2010). Y3IP1, a nucleus-encoded thylakoid protein, cooperates with the plastid-encoded Ycf3 protein in photosystem I assembly of tobacco and Arabidopsis. Plant Cell 22: 2838-2855.
4. Amann, K., Lezhneva, L., Wanner, G., Herrmann, R.G., and Meurer, J. (2004). ACCUMULATION OF PHOTOSYSTEM ONE1, a member of a novel gene family, is required for accumulation of [4Fe-4S] cluster-containing chloroplast complexes and antenna proteins. Plant Cell 16: 3084-3097.
5. Amunts, A., Toporik, H., Borovikova, A., and Nelson, N. (2010). Structure determination and improved model of plant photosystem I. J. Biol. Chem. 285: 3478-3486.
6. Antonkine, M.L., Jordan, P., Fromme, P., Krauss, N., Golbeck, J.H., and Stehlik, D. (2003). Assembly of protein subunits within the stromal ridge of photosystem I. Structural changes between unbound and sequentially PS I-bound polypeptides and correlated changes of the magnetic properties of the terminal iron sulfur clusters. J. Mol. Biol. 327: 671-697.
7. Avenson, T.J., Ahn, T.K., Zigmantas, D., Niyogi, K.K., Li, Z., Ballottari, M., Bassi, R., and Fleming, G.R. (2008). Zeaxanthin radical cation formation in minor light-harvesting complexes of higher plant antenna. J. Biol. Chem. 283: 3550-3558.
8. Barkan, A. (1993). Nuclear mutants of maize with defects in chloroplast polysome assembly have altered chloroplast RNA metabolism. Plant Cell 5: 389-402.
9. Barkan, A., Voelker, R., Mendel-Hartvig, J., Johnson, D., and Walker, M. (1995). Genetic analysis of chloroplast biogenesis in higher plants. Physiol. Plant. 93: 163-170.
10. Barneche, F., Winter, V., Crèvecoeur, M., and Rochaix, J.D. (2006). ATAB2 is a novel factor in the signalling pathway of light-controlled synthesis of photosystem proteins. EMBO J. 25: 5907-5918.
11. Baroli, I., Do, A.D., Yamane, T., and Niyogi, K.K. (2003). Zeaxanthin accumulation in the absence of a functional xanthophyll cycle protects Chlamydomonas reinhardtii from photooxidative stress. Plant Cell 15: 992-1008.
12. Bassi, R., Pineau, B., Dainese, P., and Marquardt, J. (1993). Carotenoid-binding proteins of photosystem II. Eur. J. Biochem. 212: 297-303.
13. Bassi, R., Rigoni, F., Barbato, R., and Giacometti, G.M. (1988). Light-harvesting chlorophyll a/b proteins (LHCII) populations in phosphorylated membranes. Biochim. Biophys. Acta 936: 29-38.
14. Betterle, N., Ballottari, M., Zorzan, S., de Bianchi, S., Cazzaniga, S., Dall'osto, L., Morosinotto, T., and Bassi, R. (2009). Light-induced dissociation of an antenna hetero-oligomer is needed for non-photochemical quenching induction. J. Biol. Chem. 284: 15255-15266.
15. Boudreau, E., Takahashi, Y., Lemieux, C., Turmel, M., and Rochaix, J.D. (1997). The chloroplast ycf3 and ycf4 open reading frames of Chlamydomonas reinhardtii are required for the accumulation of the photosystem I complex. EMBO J. 16: 6095-6104.
16. Britton, G., Liaaen-Jensen, S., and Pfander, H. (2004). Carotenoids Hand Book. (Basel, Switzerland: Birkhauser Publishing).
17. Caffarri, S., Kouril, R., Kereïche, S., Boekema, E.J., and Croce, R. (2009). Functional architecture of higher plant photosystem II supercomplexes. EMBO J. 28: 3052-3063.
18. Caffarri, S., Passarini, F., Bassi, R., and Croce, R. (2007). A specific binding site for neoxanthin in the monomeric antenna proteins CP26 and CP29 of photosystem II. FEBS Lett. 581: 4704-4710.
19. Croce, R., Weiss, S., and Bassi, R. (1999). Carotenoid-binding sites of the major light-harvesting complex II of higher plants. J. Biol. Chem. 274: 29613-29623.
20. Cuttriss, A.J., and Pogson, B.J. (2006). Carotenoids. In The Structure and Function of Plastids, R.R. Wise and J.K. Hoober, eds (Dordrecht, The Netherlands: Springer), pp. 315-334.
21. Dainese, P., Santini, C., Ghiretti-Magaldi, A., Marquardt, J., Tidu, V., Mauro, S., Bergantino, E., and Bassi, R. (1992). The organization of pigment-proteins within photosystem II. In Research in Photosynthesis, Vol. II, N. Murata, ed (Dordrecht, The Netherlands: Kluwer Academic Publishers), pp. 13-20.
22. Dall'Osto, L., Caffarri, S., and Bassi, R. (2005). A mechanism of nonphotochemical energy dissipation, independent from PsbS, revealed by a conformational change in the antenna protein CP26. Plant Cell 17: 1217-1232.
23. Dall'Osto, L., Cazzaniga, S., Havaux, M., and Bassi, R. (2010). Enhanced photoprotection by protein-bound vs. free xanthophyll pools: A comparative analysis of chlorophyll b and xanthophyll biosynthesis mutants. Mol. Plant 3: 576-593.
24. Dall'Osto, L., Cazzaniga, S., North, H., Marion-Poll, A., and Bassi, R. (2007a). The Arabidopsis aba4-1 mutant reveals a specific function for neoxanthin in protection against photooxidative stress. Plant Cell 19: 1048-1064.
25. Dall'Osto, L., Fiore, A., Cazzaniga, S., Giuliano, G., and Bassi, R. (2007b). Different roles of α-and β-branch xanthophylls in photosystem assembly and photoprotection. J. Biol. Chem. 282: 35056-35068.
26. Davison, P.A., Hunter, C.N., and Horton, P. (2002). Overexpression of beta-carotene hydroxylase enhances stress tolerance in Arabidopsis. Nature 418: 203-206.
27. DellaPenna, D., and Pogson, B.J. (2006). Vitamin synthesis in plants: Tocopherols and carotenoids. Annu. Rev. Plant Biol. 57: 711-738.
28. Demmig-Adams, B., and Adams, W.W. (1992a). Carotenoid composition in sun and shade leaves of plants with different life forms. Plant Cell Environ. 15: 411-419.
29. Demmig-Adams, B., and Adams, W.W. (1992b). Photoprotection and other responses of plants to high light stress. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43: 599-626.
30. Espineda, C.E., Linford, A.S., Devine, D., and Brusslan, J.A. (1999). The AtCAO gene, encoding chlorophyll a oxygenase, is required for chlorophyll b synthesis in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 96: 10507-10511.
31. Fiore, A., Dallosto, L., Cazzaniga, S., Diretto, G., Giuliano, G., and Bassi, R. (2012). A quadruple mutant of Arabidopsis reveals a β-carotene hydroxylation activity for LUT1/CYP97C1 and a regulatory role of xanthophylls on determination of the PSI/PSII ratio. BMC Plant Biol. 12: 50.
32. Fiore, A., Dall'osto, L., Fraser, P.D., Bassi, R., and Giuliano, G. (2006). Elucidation of the beta-carotene hydroxylation pathway in Arabidopsis thaliana. FEBS Lett. 580: 4718-4722.
33. Flors, C., Fryer, M.J., Waring, J., Reeder, B., Bechtold, U., Mullineaux, P.M., Nonell, S., Wilson, M.T., and Baker, N.R. (2006). Imaging the production of singlet oxygen in vivo using a new fluorescent sensor, Singlet Oxygen Sensor Green. J. Exp. Bot. 57: 1725-1734.
34. Formaggio, E., Cinque, G., and Bassi, R. (2001). Functional architecture of the major light-harvesting complex from higher plants. J. Mol. Biol. 314: 1157-1166.
35. Ganeteg, U., Külheim, C., Andersson, J., and Jansson, S. (2004). Is each light-harvesting complex protein important for plant fitness? Plant Physiol. 134: 502-509.
36. Gilmore, A.M., and Yamamoto, H.Y. (1991). Zeaxanthin formation and energy-dependent fluorescence quenching in pea chloroplasts under artificially mediated linear and cyclic electron transport. Plant Physiol. 96: 635-643.
37. Gomez-Roldan, V., et al. (2008). Strigolactone inhibition of shoot branching. Nature 455: 189-194.
38. Haldrup, A., Simpson, D.J., and Scheller, H.V. (2000). Downregulation of the PSI-F subunit of photosystem I (PSI) in Arabidopsis thaliana. The PSI-F subunit is essential for photoautotrophic growth and contributes to antenna function. J. Biol. Chem. 275: 31211-31218.
39. Härtel, H., Lokstein, H., Dörmann, P., Grimm, B., and Benning, C. (1997). Changes in the composition of the photosynthetic apparatus in the galactolipid-deficient dgd1 mutant of Arabidopsis thaliana. Plant Physiol. 115: 1175-1184.
40. Havaux, M., Dall'osto, L., and Bassi, R. (2007). Zeaxanthin has enhanced antioxidant capacity with respect to all other xanthophylls in Arabidopsis leaves and functions independent of binding to PSII antennae. Plant Physiol. 145: 1506-1520.
41. Havaux, M., Dall'Osto, L., Cuiné, S., Giuliano, G., and Bassi, R. (2004). The effect of zeaxanthin as the only xanthophyll on the structure and function of the photosynthetic apparatus in Arabidopsis thaliana. J. Biol. Chem. 279: 13878-13888.
42. Havaux, M., and Niyogi, K.K. (1999). The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. Proc. Natl. Acad. Sci. USA 96: 8762-8767.
43. Hein, P., Stöckel, J., Bennewitz, S., and Oelmüller, R. (2009). A protein related to prokaryotic UMP kinases is involved in psaA/B transcript accumulation in Arabidopsis. Plant Mol. Biol. 69: 517-528.
44. Holt, N.E., Zigmantas, D., Valkunas, L., Li, X.P., Niyogi, K.K., and Fleming, G.R. (2005). Carotenoid cation formation and the regulation of photosynthetic light harvesting. Science 307: 433-436.
45. Ihnatowicz, A., Pesaresi, P., Varotto, C., Richly, E., Schneider, A., Jahns, P., Salamini, F., and Leister, D. (2004). Mutants for photosystem I subunit D of Arabidopsis thaliana: Effects on photosynthesis, photosystem I stability and expression of nuclear genes for chloroplast functions. Plant J. 37: 839-852.
46. Kim, J., and DellaPenna, D. (2006). Defining the primary route for lutein synthesis in plants: The role of Arabidopsis carotenoid beta-ring hydroxylase CYP97A3. Proc. Natl. Acad. Sci. USA 103: 3474-3479.
47. Kim, J., Smith, J.J., Tian, L., and Dellapenna, D. (2009). The evolution and function of carotenoid hydroxylases in Arabidopsis. Plant Cell Physiol. 50: 463-479.
48. Klimmek, F., Ganeteg, U., Ihalainen, J.A., van Roon, H., Jensen, P.E., Scheller, H.V., Dekker, J.P., and Jansson, S. (2005). The structure of higher plant LHCI: In vivo characterisation and structural interdependence of the Lhca proteins. Biochemisty 44: 3065-3073.
49. Koniger, M., Harris, G.C., Virgo, A., and Winter, K. (1995). Xanthophyllcycle pigments and photosynthetic capacity in tropical forest species-A comparative field study on canopy, gap and understory plants. Oecologia 104: 280-290.
50. Krech, K., Ruf, S., Masduki, F.F., Thiele, W., Bednarczyk, D., Albus, C.A., Tiller, N., Hasse, C., Schöttler, M.A., and Bock, R. (2012). The plastid genome-encoded Ycf4 protein functions as a nonessential assembly factor for photosystem I in higher plants. Plant Physiol. 159: 579-591.
51. Krieger-Liszkay, A. (2005). Singlet oxygen production in photosynthesis. J. Exp. Bot. 56: 337-346.
52. Kull, O., and Pfander, H. (1995). List of new carotenoids. In Carotenoids: Isolation and Analysis, S.L.-J.a.H.P.e.G. Britton, ed (Basel, Switzerland: Birkhauser Publishing), pp. 295-317.
53. Landau, A.M., Lokstein, H., Scheller, H.V., Lainez, V., Maldonado, S., and Prina, A.R. (2009). A cytoplasmically inherited barley mutant is defective in photosystem I assembly due to a temperaturesensitive defect in ycf3 splicing. Plant Physiol. 151: 1802-1811.
54. Lezhneva, L., Amann, K., and Meurer, J. (2004). The universally conserved HCF101 protein is involved in assembly of [4Fe-4S]-cluster-containing complexes in Arabidopsis thaliana chloroplasts. Plant J. 37: 174-185.
55. Lezhneva, L., and Meurer, J. (2004). The nuclear factor HCF145 affects chloroplast psaA-psaB-rps14 transcript abundance in Arabidopsis thaliana. Plant J. 38: 740-753.
56. Li, X.P., Björkman, O., Shih, C., Grossman, A.R., Rosenquist, M., Jansson, S., and Niyogi, K.K. (2000). A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403: 391-395.
57. Li, X.P., Muller-Moule, P., Gilmore, A.M., and Niyogi, K.K. (2002). PsbSdependent enhancement of feedback de-excitation protects photosystem II from photoinhibition. Proc. Natl. Acad. Sci. USA 99: 15222-15227.
58. Liu, Z., Yan, H., Wang, K., Kuang, T., Zhang, J., Gui, L., An, X., and Chang, W. (2004). Crystal structure of spinach major light-harvesting complex at 2.72 A resolution. Nature 428: 287-292.
59. Malkin, S., Armond, P.A., Mooney, H.A., and Fork, D.C. (1981). Photosystem II photosynthetic unit sizes from fluorescence induction in leaves. Correlation to photosynthetic capacity. Plant Physiol. 67: 570-579.
60. Mathews, M.B., Sonenberg, N., and Hershey, J.W.B. (2007). Origins and principles of translational control. In Translational Control in Biology and Medicine, M.B. Mathews, N. Sonenberg, and J.W.B. Hershey, eds (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press), pp. 1-40.
61. Meurer, J., Grevelding, C., Westhoff, P., and Reiss, B. (1998). The PAC protein affects the maturation of specific chloroplast mRNAs in Arabidopsis thaliana. Mol. Gen. Genet. 258: 342-351.
62. Morosinotto, T., Castelletti, S., Breton, J., Bassi, R., and Croce, R. (2002). Mutation analysis of Lhca1 antenna complex. Low energy absorption forms originate from pigment-pigment interactions. J. Biol. Chem. 277: 36253-36261.
63. Mozzo, M., Morosinotto, T., Bassi, R., and Croce, R. (2006). Probing the structure of Lhca3 by mutation analysis. Biochim. Biophys. Acta 1757: 1607-1613.
64. 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.
65. Nelson, N., and Ben Shem, A. (2004). The complex architecture of oxygenic photosynthesis. Nature 5: 1-12.
66. Niyogi, K.K. (2000). Safety valves for photosynthesis. Curr. Opin. Plant Biol. 3: 455-460.
67. Niyogi, K.K., Shih, C., Soon Chow, W., Pogson, B.J., Dellapenna, D., and Björkman, O. (2001). Photoprotection in a zeaxanthin-and lutein-deficient double mutant of Arabidopsis. Photosynth. Res. 67: 139-145.
68. North, H.M., De Almeida, A., Boutin, J.P., Frey, A., To, A., Botran, L., Sotta, B., and Marion-Poll, A. (2007). The Arabidopsis ABAdeficient mutant aba4 demonstrates that the major route for stressinduced ABA accumulation is via neoxanthin isomers. Plant J. 50: 810-824.
69. Pan, X., Li, M., Wan, T., Wang, L., Jia, C., Hou, Z., Zhao, X., Zhang, J., and Chang, W. (2011). Structural insights into energy regulation of light-harvesting complex CP29 from spinach. Nat. Struct. Mol. Biol. 18: 309-315.
70. Paulsen, H. (1997). Pigment ligation to proteins of the photosynthetic apparatus in higher plants. Physiol. Plant. 100: 760-768.
71. Peter, G.F., Takeuchi, T., and Thornber, J.P. (1991). Solubilization and two-dimensional electrophoretic procedures for studying the organization and composition of photosynthetic membrane polypeptides. Methods: A Companion to Methods in Enzymology 3: 115-124.
72. Piques, M., Schulze, W.X., Höhne, M., Usadel, B., Gibon, Y., Rohwer, J., and Stitt, M. (2009). Ribosome and transcript copy numbers, polysome occupancy and enzyme dynamics in Arabidopsis. Mol. Syst. Biol. 5: 314.
73. Plumley, F.G., and Schmidt, G.W. (1987). Reconstitution of chlorophyll a/b light-harvesting complexes: Xanthophyll-dependent assembly and energy transfer. Proc. Natl. Acad. Sci. USA 84: 146-150.
74. Pogson, B.J., Niyogi, K.K., Björkman, O., and DellaPenna, D. (1998). Altered xanthophyll compositions adversely affect chlorophyll accumulation and nonphotochemical quenching in Arabidopsis mutants. Proc. Natl. Acad. Sci. USA 95: 13324-13329.
75. Pogson, B.J., and Rissler, H.M. (2000). Genetic manipulation of carotenoid biosynthesis and photoprotection. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355: 1395-1403.
76. Ramel, F., Birtic, S., Ginies, C., Soubigou-Taconnat, L., Triantaphylidès, C., and Havaux, M. (2012). Carotenoid oxidation products are stress signals that mediate gene responses to singlet oxygen in plants. Proc. Natl. Acad. Sci. USA 109: 5535-5540.
77. Rappaport, F., Béal, D., Joliot, A., and Joliot, P. (2007). On the advantages of using green light to study fluorescence yield changes in leaves. Biochim. Biophys. Acta 1767: 56-65.
78. Redding, K., Cournac, L., Vassiliev, I.R., Golbeck, J.H., Peltier, G., and Rochaix, J.-D. (1999). Photosystem I is indispensable for photoautotrophic growth, CO2 fixation, and H2 photoproduction in Chlamydomonas reinhardtii. J. Biol. Chem. 274: 10466-10473.
79. Sane, P.V., Ivanov, A.G., Hurry, V., Huner, N.P., and Oquist, G. (2003). Changes in the redox potential of primary and secondary electron-accepting quinones in photosystem II confer increased resistance to photoinhibition in low-temperature-acclimated Arabidopsis. Plant Physiol. 132: 2144-2151.
80. Sbarbati, A., Merigo, F., Benati, D., Tizzano, M., Bernardi, P., and Osculati, F. (2004). Laryngeal chemosensory clusters. Chem. Senses 29: 683-692.
81. Schägger, H., and von Jagow, G. (1987). Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166: 368-379.
82. Schöttler, M.A., Albus, C.A., and Bock, R. (2011). Photosystem I: Its biogenesis and function in higher plants. J. Plant Physiol. 168: 1452-1461.
83. Schwenkert, S., Netz, D.J.A., Frazzon, J., Pierik, A.J., Bill, E., Gross, J., Lill, R., and Meurer, J. (2010). Chloroplast HCF101 is a scaffold protein for [4Fe-4S] cluster assembly. Biochem. J. 425: 207-214.
84. Sonoike, K. (2011). Photoinhibition of photosystem I. Physiol. Plant. 142: 56-64.
85. Stern, D.B., Goldschmidt-Clermont, M., and Hanson, M.R. (2010). Chloroplast RNA metabolism. Annu. Rev. Plant Biol. 61: 125-155.
86. Stöckel, J., Bennewitz, S., Hein, P., and Oelmüller, R. (2006). The evolutionarily conserved tetratrico peptide repeat protein pale yellow green7 is required for photosystem I accumulation in Arabidopsis and copurifies with the complex. Plant Physiol. 141: 870-878.
87. Sun, X.W., Ouyang, M., Guo, J.K., Ma, J.F., Lu, C.M., Adam, Z., and Zhang, L.X. (2010). The thylakoid protease Deg1 is involved in photosystem-II assembly in Arabidopsis thaliana. Plant J. 62: 240-249.
88. Telfer, A. (2005). Too much light? How beta-carotene protects the photosystem II reaction centre. Photochem. Photobiol. Sci. 4: 950-956.
89. Tian, L., Magallanes-Lundback, M., Musetti, V., and DellaPenna, D. (2003). Functional analysis of beta-and epsilon-ring carotenoid hydroxylases in Arabidopsis. Plant Cell 15: 1320-1332.
90. Tian, L., Musetti, V., Kim, J., Magallanes-Lundback, M., and DellaPenna, D. (2004). The Arabidopsis LUT1 locus encodes a member of the cytochrome p450 family that is required for carotenoid epsilon-ring hydroxylation activity. Proc. Natl. Acad. Sci. USA 101: 402-407.
91. Tottey, S., Block, M.A., Allen, M., Westergren, T., Albrieux, C., Scheller, H.V., Merchant, S., and Jensen, P.E. (2003). Arabidopsis CHL27, located in both envelope and thylakoid membranes, is required for the synthesis of protochlorophyllide. Proc. Natl. Acad. Sci. USA 100: 16119-16124.
92. Van Kooten, O., and Snel, J.F.H. (1990). The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth. Res. 25: 147-150.
93. Varotto, C., Pesaresi, P., Meurer, J., Oelmüller, R., Steiner-Lange, S., Salamini, F., and Leister, D. (2000). Disruption of the Arabidopsis photosystem I gene psaE1 affects photosynthesis and impairs growth. Plant J. 22: 115-124.
94. Walters, R.G., and Horton, P. (1995). Acclimation of Arabidopsis thaliana to the light environment: Changes in photosynthetic function. Planta 197: 306-312.
95. Wang, Y.L., Mao, L.S., and Hu, X.C. (2004). Insight into the structural role of carotenoids in the photosystem I: A quantum chemical analysis. Biophys. J. 86: 3097-3111.
96. Watkins, K.P., Rojas, M., Friso, G., van Wijk, K.J., Meurer, J., and Barkan, A. (2011). APO1 promotes the splicing of chloroplast group II introns and harbors a plant-specific zinc-dependent RNA binding domain. Plant Cell 23: 1082-1092.
97. Yabe, O.T., Morimoto, K., Kikuchi, S., Nishio, K., Terashima, I., and Nakai, M. (2004). The Arabidopsis chloroplastic NifU-like protein CnfU, which can act as an iron-sulfur cluster scaffold protein, is required for biogenesis of ferredoxin and photosystem I. Plant Cell 16: 993-1007.
98. Yamamoto, H.Y., Nakayama, T.O., and Chichester, C.O. (1962). Studies on the light and dark interconversions of leaf xanthophylls. Arch. Biochem. Biophys. 97: 168-173.
99. Ye, J.-W., Gong, Z.-Y., Chen, C.-G., Mi, H.-L., and Chen, G.-Y. (2012). A mutation of OSOTP 51 leads to impairment of photosystem I complex assembly and serious photo-damage in rice. J. Integr. Plant Biol. 54: 87-98.