Characterization of mutations in barley fch2 encoding chlorophyllide a oxygenase

Plant and Cell Physiology

Volumn 53, Issue 7, 2012, Pages 1232-1246

  Mueller, Andre Hubertus ^a,d   Dockter, Christoph ^a   Gough, Simon Peter ^a   Lundqvist, Udda ^b   Von Wettstein, Diter ^c   Hansson, Mats ^a  

^a CARLSBERG LABORATORY   (Denmark)

^b Nordic Genetic Resources Center (NordGen)   (Sweden)

^c WASHINGTON STATE UNIVERSITY   (United States)

^d STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Barley (Hordeum vulgare L.); chlorina f2; Chloropyllide a oxygenase; fch2

Indexed keywords

CHLOROPHYLL; CHLOROPHYLL A OXYGENASE; CHLOROPHYLL B; OXYGENASE; VEGETABLE PROTEIN;

ALLELE; AMINO ACID SEQUENCE; ARTICLE; CHROMOSOME MAP; ELECTRON TRANSPORT; ENZYME ACTIVE SITE; ENZYMOLOGY; FRAMESHIFT MUTATION; GENE EXPRESSION REGULATION; GENETICS; HORDEUM; METABOLISM; MISSENSE MUTATION; MOLECULAR CLONING; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHENOTYPE; PLANT CHROMOSOME; PLANT GENE; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT; STOP CODON; SYNTENY;

ALLELES; AMINO ACID SEQUENCE; CATALYTIC DOMAIN; CHLOROPHYLL; CHROMOSOME MAPPING; CHROMOSOMES, PLANT; CLONING, MOLECULAR; CODON, NONSENSE; ELECTRON TRANSPORT; FRAMESHIFT MUTATION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; HORDEUM; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; OXYGENASES; PHENOTYPE; PLANT PROTEINS; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; SYNTENY;

CHLORINA; HORDEUM; HORDEUM VULGARE SUBSP. VULGARE;

EID: 84863938407     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcs062     Document Type: Article

References (66)

1. Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W. et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402.
2. Apel, P. (1967) Photosynthesemessungen an Chlorophyllmutanten von Gerste (Lichtkurven, 'Lichtatmung', Starklichempfindlichkeit). Stud. Biophys. 5: 105-110.
3. Axelsson, E., Lundqvist, J., Sawicki, A., Nilsson, S., Schröder, I., Al-Karadaghi, S. et al. (2006) Recessiveness and dominance in barley mutants deficient in Mg-chelatase subunit D, an AAA protein involved in chlorophyll biosynthesis. Plant Cell 18: 3606-3616.
4. Bartsch, S., Monnet, J., Selbach, K., Quigley, F., Gray, J., von Wettstein, D. et al. (2008) Three thioredoxin targets in the inner envelope membrane of chloroplasts function in protein import and chlorophyll metabolism. Proc. Natl Acad. Sci. USA 105: 4933-4938.
5. Bhalla, P. and Bennett, J. (1987) Chloroplast phosphoproteins: phosphorylation of a 12-kDa stromal protein by the redox-controlled kinase of thylakoid membranes. Arch. Biochem. Biophys. 252: 97-104.
6. Bossmann, B., Knoetzel, J. and Jansson, S. (1997) Screening of chlorina mutants of barley (Hordeum vulgare L.) with antibodies against light-harvesting proteins of PS I and PS II: absence of specific antenna proteins. Photosynth. Res. 52: 127-136.
7. Burger-Wiersma, T. and Post, A.F. (1989) Functional analysis of the photosynthetic apparatus of Prochlorothrix hollandica (Prochlorales), a chlorophyll b containing procaryote. Plant Physiol. 91: 770-774.
8. D'Ordine, R.L., Rydel, T.J., Storek, M.J., Sturman, E.J., Moshiri, F., Bartlett, R.K. et al. (2009) Dicamba monooxygenase: structural insights into a dynamic Rieske oxygenase that catalyzes an exocyclic monooxygenation. J. Mol. Biol. 392: 481-497.
9. Druka, A., Franckowiak, J., Lundqvist, U., Bonar, N., Alexander, J., Houston, K. et al. (2010) Genetic dissection of barley morphology and development. Plant Physiol. 155: 617-627.
10. Dumitru, R., Jiang, W.Z., Weeks, D.P. and Wilsom, M.A. (2009) Crystal structure of dicamba monooxygenase: a Rieske nonheme oxygenase that catalyzes oxidative demethylation. J. Mol. Biol. 392: 498-510.
11. Eggink, L.L., LoBrutto, R., Brune, D.C., Brusslan, J., Yamasato, A., Tanaka, A. et al. (2004) Synthesis of chlorophyll b: localization of chlorophyllide a oxygenase and discovery of a stable radical in the catalytic subunit. BMC Plant Biol. 4: 5.
12. Emanuelsson, O., Nielsen, H. and von Heijne, G. (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci. 8: 978-984.
13. 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.
14. Franckowiak, J.D. (1997) Stock number: BGS 117. Barley Genet. Newslett. 26: 151-152.
15. Gadjieva, R., Axelsson, E., Olsson, U., Vallon-Christersson, J. and Hansson, M. (2004) Nonsense-mediated mRNA decay in barley mutants allows the cloning of mutated genes by a microarray approach. Plant Physiol. Biochem. 42: 681-685.
16. Goodchild, D.J., Highkin, H.R. and Boardman, N.K. (1966) The fine structure of chloroplasts in a barley mutant lacking chlorophyll b. Exp. Cell Res. 43: 684-688.
17. Hager, A. and Bertenrath, T. (1962) Verteilungschromatographische Trennung von Chlorophyllen und Carotinoiden grüner Pflanzen an Dünnschichten. Planta 58: 564-568.
18. Hager, A. and Meyer-Bertenrath, T. (1966) Die Isolierung und quantitative Bestimmung der Carotinoide und Chlorophylle von Blättern, Algen und isolierten Chloroplasten mit Hilfe dünnschichtchromatographischer Methoden. Planta 69: 198-217.
19. Hansson, A., Kannangara, C.G., von Wettstein, D. and Hansson, M. (1999) Molecular basis for semidominance of missense mutations in the XANTHA-H (42-kDa) subunit of magnesium chelatase. Proc. Natl Acad. Sci. USA 96: 1744-1749.
20. Harrison, M.A., Nemson, J.A. and Melis, A. (1993) Assembly and composition of the chlorophyll a-b light harvesting complex of barley (Hordeum vulgare L.): immunochemical analysis of chlorophyll b-less and chlorophyll b-deficient mutants. Photosynth. Res. 38: 141-151.
21. Harwood, W.A. (2012) Advances and remaining challenges in the transformation of barley and wheat. J. Exp. Bot. 63: 1791-1798.
22. Havaux, M. and Tardy, F. (1997) Thermostability and photostability of photosystem II in leaves of the chlorina-f2 barley mutant deficient in light-harvesting chlorophyll a/b protein complexes. Plant Physiol. 113: 913-923.
23. Henriques, F. and Park, R.B. (1975) Further chemical and morphological characterization of chloroplast membranes from a chlorophyll b-less mutant of Hordeum vulgare. Plant Physiol. 55: 763-767.
24. Herman, P.L., Behrens, M., Chakraborty, S., Chrastil, B.M., Barycki, J. and Weeks, D.P. (2005) A three-component dicamba O-demethylase from Pseudomonas maltophila, strain DI-6. J. Biol. Chem. 280: 24759-24767.
25. Hirashima, M., Satoh, S., Tanaka, R. and Tanaka, A. (2006) Pigment shuffling in antenna systems achieved by expressing prokaryotic chlorophyllide a oxygenase in Arabidopsis. J. Biol. Chem. 281: 15385-15393.
26. Hobe, S., Niemeier, H., Bender, A. and Paulsen, H. (2000) Carotenoid binding sites in LHCIIb. Eur. J. Biochem. 267: 616-624.
27. Highkin, H.R. (1950) Chlorophyll studies on barley mutants. Plant Physiol. 25: 294-306.
28. Highkin, H.R. and Frenkel, A.W. (1952) Studies of growth and metabolism of a barley mutant lacking chlorophyll b. Plant Physiol. 37: 814-820.
29. Hiller, R.G. and Raison, J.K. (1980) The fluidity of chloroplast thylakoid membranes and their constituent lipids-a comparative study by ESR. Biochim. Biophys. Acta 599: 63-72.
30. Lee, K.P., Kim, C., Lee, D.W. and Apel, K. (2003) TIGRINA d, required for regulating the biosynthesis of tetrapyrroles in barley, is an ortholog of the FLU gene of Arabidopsis thaliana. FEBS Lett. 553: 119-124.
31. Lee, S., Kim, J.-H., Yoo, E.S., Lee, C.-H., Hirochika, H. and An, G. (2005) Differential regulation of chlorophyll a oxygenase in rice. Plant Mol. Biol. 57: 805-818.
32. Lundqvist, U. (1992) Mutation research in barley. PhD thesis. The Swedish University of Agricultural Sciences, Svalöv.
33. Machold, O., Meister, A., Sagromsky, H., Høyer-Hansen, G. and von Wettstein, D. (1977) Composition of photosynthetic membranes of wild-type barley and chlorophyll b-less mutants. Photosynthetica 11: 200-206.
34. Mansiaux, Y., Joseph, A.P., Gelly, J.C. and de Brevern, A.G. (2011) Assignment of polyproline II conformation and analysis of sequence-structure relationship. PLoS ONE 6: e18401.
35. Martinson, T.A. and Plumley, F.G. (1995) One-step extraction and concentration of pigments and acyl lipids by sec-butanol from in vitro and in vivo samples. Anal. Biochem. 228: 123-130.
36. Matsumoto, T., Tanaka, T., Sakai, H., Amano, N., Kanamori, H., Kurita, K. et al. (2011) Comprehensive sequence analysis of 24,783 barley full-length cDNAs from 12 clone libraries. Plant Physiol. 156: 20-28.
37. Montrichard, F., Alkhalfioui, F., Yano, H., Vensel, W.H., Hurkman, W.J. and Buchanan, B.B. (2009) Thioredoxin targets in plants: the first 30 years. J. Proteomics 72: 452-474.
38. Müller, A.H., Gough, S.P., Bollivar, D.W., Meldahl, M., Willows, R.D. and Hansson, M. (2011) Methods for the preparation of chlorophyllide a: an intermediate of the chlorophyll biosynthetic pathway. Anal. Biochem. 419: 271-276.
39. Mullet, J.E., Burke, J.J. and Arntzen, C.J. (1980) A developmental study of photosystem I peripheral chlorophyll proteins. Plant Physiol. 65: 823-827.
40. Nagata, N., Satoh, S., Tanaka, R. and Tanaka, A. (2004) Domain structures of chlorophyllide a oxygenase of green plants and Prochlorothrix hollandica in relation to catalytic functions. Planta 218: 1019-1025.
41. Olsson, U., Sirijovski, N. and Hansson, M. (2004) Characterization of eight barley xantha-f mutants deficient in magnesium chelatase. Plant Physiol. Biochem. 42: 557-564.
42. Oster, U., Tanaka, R., Tanaka, A. and Rüdiger, W. (2000) Cloning and functional expression of the gene encoding the key enzyme for chlorophyll b biosynthesis (CAO) from Arabidopsis thaliana. Plant J. 21: 305-310.
43. Pettersen, E.F., Goddard, T.D., Huang, C.C., Couch, G.S., Greenblatt, D.M., Meng, E.C. et al. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25: 1605-1612.
44. Preiss, S. and Thornber, J.P. (1995) Stability of the apoproteins of light harvesting complex I and II during biogenesis of thylakoids in the chlorophyll b-less barley mutant chlorina f2. Plant Physiol. 107: 709-717.
45. Rai, R., Aravinda, S., Kanagarajadurai, K., Raghothama, S., Shamala, N. and Balaram, P. (2006) Diproline templates as folding nuclei in designed peptides. Conformational analysis of synthetic peptide helices containing amino terminal Pro-Pro segments. J. Amer, Chem. Soc. 28: 7916-7928.
46. Rudoi, A.B. and Shcherbakov, R.A. (1998) Analysis of the chlorophyll biosynthetic system in a chlorophyll b-less barley mutant. Photosynth. Res. 58: 71-80.
47. Rzeznicka, K., Walker, C.J., Westergren, T., Kannangara, C.G., von Wettstein, D., Merchant, S. et al. (2005) Xantha-l encodes a membrane subunit of the aerobic Mg-protoporphyrin IX monomethylester cyclase involved in chlorophyll biosynthesis. Proc. Natl Acad. Sci. USA 102: 5886-5891.
48. Sagromsky, H. (1974) Zur physiologischen Bedeutung von Chlorophyll b. Biochem. Physiol. Pflanz. 166: 95-104.
49. Saito, A., Iino, T., Sonoike, K., Miwa, E. and Higuchi, K. (2010) Remodeling of the major light-harvesting antennae protein of PSII protects the young leaves of barley (Hordeum vulgare L.) from photoinhibition under prolonged iron deficiency. Plant Cell Physiol. 51: 2013-2030.
50. Sakuraba, Y., Tanaka, R., Yamasato, A. and Tanaka, A. (2009) Determination of a chloroplast degron in the regulatory domain of chlorophyllide a oxygenase. J. Biol. Chem. 284: 36689-36699.
51. Sakuraba, Y., Yamasato, A., Tanaka, R. and Tanaka, A. (2007) Functional analysis of N-terminal domains of Arabidopsis chlorophyllide a oxygenase. Plant Physiol. Biochem. 45: 740-749.
52. Schneegurt, M.A. and Beale, S.I. (1992) Origin of the chlorophyll b formyl oxygen in Chlorella vulgaris. Biochemistry 31: 11677-11683.
53. Simpson, D.J., Machold, O., Høyer-Hansen, G. and von Wettstein, D. (1985) Chlorina mutants of barley (Hordeum vulgare L.). Carlsberg Res. Commun. 50: 223-238.
54. Simpson, D.J. and von Wettstein, D. (1992) Coordinator's report: nuclear genes affecting the chloroplast. Stock list of mutants kept at the Carlsberg Laboratory. Barley Genet. Newslett. 21: 102-108.
55. Takahashi, R., Hayashi, J., Konishi, T. and Moriya, I. (1975) Linkage analysis of barley mutants. Barley Genet Newslett. 5: 56-60.
56. Tanaka, A., Ito, H., Tanaka, R., Tanaka, N.K., Yoshida, K. and Okada, K. (1998) Chlorophyll a oxygenase (CAO) is involved in chlorophyll b formation from chlorophyll a. Proc. Natl Acad. Sci. USA 95: 12719-12723.
57. Tanaka, R. and Tanaka, A. (2005) Effects of chlorophyllide a oxygenase overexpression on light acclimation in Arabidopsis thaliana. Photosynth. Res. 85: 327-340.
58. Thornber, J.P. and Highkin, H.R. (1974) Composition of the photosynthetic apparatus of normal barley leaves and a mutant lacking chlorophyll b. Eur. J. Biochem. 41: 109-116.
59. Tsuchiya, T. (1972) BGS 0117 Chlorina f2. Barley Genet. Newslett. 2: 183.
60. Tsuchiya, T. and Robertson, D.W. (1971) Association of a chlorina mutant with chromosome 3. Barley Genet. Newslett. 1: 64-65.
61. Tyutereva, E.V. and Voitsekhovskaja, O.V. (2011a) Responses of chlorophyll b-free chlorina 3613 barley mutant to a prolonged decrease in illuminance: 1. Dynamics of chlorophyll content, growth, and productivity. Russ. J. Plant Physiol. 58: 1-8.
62. Tyutereva, E.V. and Voitsekhovskaja, O.V. (2011b) Responses of chlorophyll b-less chlorina 3613 mutant of barley to a prolonged decrease in illuminance: 2. Dynamics of carotenoids in leaf chloroplasts. Russ. J. Plant Physiol. 58: 218-225.
63. Wang, G. and Dunbrack, R.L. (2003) PISCES: a protein culling server. Bioinformatics 19: 1589-1591.
64. Wang, J., Yan, Z., Zhuo, K. and Lu, J. (1999) Partial molar volumes of some alpha-amino acids in aqueous sodium acetate solutions at 308.15 K. Biophys. Chem. 80: 179-188.
65. Waterhouse, A.M., Procter, J.B., Martin, D.M.A., Clamp, M. and Barton, G.J. (2009) Jalview version 2: a multiple sequence alignment and analysis workbench. Bioinformatics 25: 1189-1191.
66. Yamasato, A., Tanaka, R. and Tanaka, A. (2008) Loss of the N-terminal domain of chlorophyllide a oxygenase induces photodamage during greening of Arabidopsis seedlings. BMC Plant Biol. 8: 64.