The rice nuclear gene, VIRESCENT 2, is essential for chloroplast development and encodes a novel type of guanylate kinase targeted to plastids and mitochondria

Plant Journal

Volumn 52, Issue 3, 2007, Pages 512-527

  Sugimoto, Hiroki ^a   Kusumi, Kensuke ^a   Noguchi, Ko ^b   Yano, Masahiro ^c   Yoshimura, Atsushi ^a   Iba, Koh ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

Author keywords

Arabidopsis; Chloroplast development; Cytosolic guanylate kinase; Plastid and mitochondrial guanylate kinase; Rice; VIRESCENT 2

Indexed keywords

CHLOROPHYLL; GENETIC ENGINEERING; METABOLISM; NUCLEOTIDES; RNA;

ARABIDOPSIS; CHLOROPLAST DEVELOPMENT; CYTOSOLIC GUANYLATE KINASE; MITOCHONDRIAL GUANYLATE KINASE; PLASTID; RICE;

PLANTS (BOTANY);

GUANYLATE KINASE; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; CHEMISTRY; CHLOROPLAST; CYTOPLASM; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MITOCHONDRION; MOLECULAR GENETICS; MUTATION; PLANT LEAF; RICE; SEEDLING; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ARABIDOPSIS; CHLOROPLASTS; CYTOPLASM; GENE EXPRESSION REGULATION, PLANT; GUANYLATE KINASE; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; MUTATION; ORYZA SATIVA; PLANT LEAVES; PLANT PROTEINS; SEEDLING; SEQUENCE ALIGNMENT;

ANIMALIA; ARABIDOPSIS; BACTERIA (MICROORGANISMS); EMBRYOPHYTA;

EID: 35448963492     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2007.03251.x     Document Type: Article

References (57)

1. Abel, S. Theologis, A. (1994) Transient transformation of Arabidopsis leaf protoplasts: a versatile experimental system to study gene expression. Plant J. 5, 421 427.
2. Agarwal, K.C., Miech, R.P. Parks, R.E., Jr. (1978) Guanylate kinases from human erythrocytes, hog brain, and rat liver. Methods Enzymol. 51, 483 490.
3. Albrecht, V., Ingenfeld, A. Apel, K. (2006) Characterization of the snowy cotyledon 1 mutant of Arabidopsis thaliana: the impact of chloroplast elongation factor G on chloroplast development and plant vitality. Plant Mol. Biol. 60, 507 518.
4. Alonso, J.M., Stepanova, A.N., Leisse, T.J. et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science, 301, 653 657.
5. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. Lipman, D.J. (1990) Basic local alignment search tool. J. Mol. Biol. 215, 403 410.
6. Barkan, A. (1993) Nuclear mutants of maize with defects in chloroplast polysome assembly have altered chloroplast RNA metabolism. Plant Cell, 5, 389 402.
7. Beck, B.J., Huelsmeyer, M., Paul, S. Downs, D.M. (2003) A mutation in the essential gene gmk (encoding guanylate kinase) generates a requirement for adenine at low temperature in Salmonella enterica. J. Bacteriol. 185, 6732 6735.
8. Brady, W.A., Kokoris, M.S., Fitzgibbon, M. Black, M.E. (1996) Cloning, characterization, and modeling of mouse and human guanylate kinases. J. Biol. Chem. 271, 16734 16740.
9. Chiu, W., Niwa, Y., Zeng, W., Hirano, T., Kobayashi, H. Sheen, J. (1996) Engineered GFP as a vital reporter in plants. Curr. Biol. 6, 325 330.
10. Clough, S.J. Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735 743.
11. Duchêne, A.-M., Giritch, A., Hoffmann, B., Cognat, V., Lancelin, D., Peeters, N.M., Zaepfel, M., Maréchal-Drouard, L. Small, I.D. (2005) Dual targeting is the rule for organellar aminoacyl-tRNA synthetases in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA, 102, 16484 16489.
12. Elpeleg, O., Mandel, H. Saada, A. (2002) Depletion of the other genome-mitochondrial DNA depletion syndromes in humans. J. Mol. Med. 80, 389 396.
13. Emanuelsson, O., Nielsen, H., Brunak, S. von Heijne, G. (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 300, 1005 1016.
14. Funke, L., Dakoji, S. Bredt, D.S. (2005) Membrane-associated guanylate kinases regulate adhesion and plasticity at cell junctions. Annu. Rev. Biochem. 74, 219 245.
15. Fuse, T., Sasaki, T. Yano, M. (2001) Ti-plasmid vectors useful for functional analysis of rice genes. Plant Biotechnol. 18, 219 222.
16. Gaidarov, I.O., Suslov, O.N. Abdulaev, N.G. (1993) Enzymes of the cyclic GMP metabolism in bovine retina. I. Cloning and expression of the gene for guanylate kinase. FEBS Lett. 335, 81 84.
17. Gentry, D., Bengra, C., Ikehara, K. Cashel, M. (1993) Guanylate kinase of Escherichia coli K-12. J. Biol. Chem. 268, 14316 14321.
18. Harrak, H., Lagrange, T., Bisanz-Seyer, C., Lerbs-Mache, S. Mache, R. (1995) The expression of nuclear genes encoding plastid ribosomal proteins precedes the expression of chloroplast genes during early phases of chloroplast development. Plant Physiol. 108, 685 692.
19. Hedtke, B., Wagner, I., Börner, T. Hess, W.R. (1999) Inter-organellar crosstalk in higher plants: impaired chloroplast development affects mitochondrial gene and transcript levels. Plant J. 19, 635 643.
20. Iba, K., Takamiya, K., Toh, Y., Satoh, H. Nishimura, M. (1991) Formation of functionally active chloroplasts is determined at a limited stage of leaf development in virescent mutants of rice. Dev. Genet. 12, 342 348.
21. International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature, 436, 793 800.
22. Kato, Y., Miura, E., Matsushima, R. Sakamoto, W. (2007) White leaf sectors in yellow variegated2 are formed by viable cells with undifferentiated plastids. Plant Physiol. 144, 952 960.
23. Konrad, M. (1992) Cloning and expression of the essential gene for guanylate kinase from yeast. J. Biol. Chem. 267, 25652 25655.
24. Kuhlendahl, S., Spangenberg, O., Konrad, M., Kim, E. Garner, C.C. (1998) Functional analysis of the guanylate kinase-like domain in the synapse-associated protein SAP97. Eur. J. Biochem. 252, 305 313.
25. Kumar, V. (2000) Cloning and sequence analysis of lily and tobacco guanylate kinases. Mol. Biol. Rep. 27, 45 49.
26. Kumar, V., Spangenberg, O. Konrad, M. (2000) Cloning of the guanylate kinase homologues AGK-1 and AGK-2 from Arabidopsis thaliana and characterization of AGK-1. Eur. J. Biochem. 267, 606 615.
27. 1 determines the expression timing of plastid genes for transcription/translation apparatus during early leaf development in rice. Plant J. 12, 1241 1250.
28. Kusumi, K., Yara, A., Mitsui, N., Tozawa, Y. Iba, K. (2004) Characterization of a rice nuclear-encoded plastid RNA polymerase gene OsRpoTp. Plant Cell Physiol. 45, 1194 1201.
29. Leipe, D.D., Wolf, Y.I., Koonin, E.V. Aravind, L. (2002) Classification and evolution of P-loop GTPases and related ATPases. J. Mol. Biol. 317, 41 72.
30. Michaels, S.D. Amasino, R.M. (1998) A robust method for detecting single-nucleotide changes as polymorphic markers by PCR. Plant J. 14, 381 385.
31. Miki, D. Shimamoto, K. (2004) Simple RNAi vectors for stable and transient suppression of gene function in rice. Plant Cell Physiol. 45, 490 495.
32. Moffatt, B.A., Stevens, Y.Y., Allen, M.S., Snider, J.D., Pereira, L.A., Todorova, M.I., Summers, P.S., Weretilnyk, E.A., Martin-McCaffrey, L. Wagner, C. (2002) Adenosine kinase deficiency is associated with developmental abnormalities and reduced transmethylation. Plant Physiol. 128, 812 821.
33. Nemoto, K. Yamazaki, K 1993) Correlative development of vegetative organs. In Science of the Rice Plant (Matsuo, T. Hoshikawa, K., eds Vol. 1. Tokyo : Food and Agriculture Policy Research Center, pp. 625 627.
34. Notsu, Y., Masood, S., Nishikawa, T., Kubo, N., Akiduki, G., Nakazono, M., Hirai, A. Kadowaki, K. (2002) The complete sequence of the rice (Oryza sativa L.) mitochondrial genome: frequent DNA sequence acquisition and loss during the evolution of flowering plants. Mol. Genet. Genomics, 268, 434 445.
35. Olsen, O. Bredt, D.S. (2003) Functional analysis of the nucleotide binding domain of membrane-associated guanylate kinases. J. Biol. Chem. 278, 6873 6878.
36. Pesaresi, P., Masiero, S., Eubel, H., Braun, H.-P., Bhushan, S., Glaser, E., Salamini, F. Leister, D. (2006) Nuclear photosynthetic gene expression is synergistically modulated by rates of protein synthesis in chloroplasts and mitochondria. Plant Cell, 18, 970 991.
37. Ray, B.D., Jarori, G.K., Raghunathan, V., Yan, H. Nageswara Rao, B.D. (2005) Conformations of nucleotides bound to wild type and Y78 F mutant yeast guanylate kinase: proton two-dimensional transferred NOESY measurements. Biochemistry, 44, 13762 13770.
38. Rice Full-Length cDNA Consortium (2003) Collection, mapping, and annotation of over 28 000 cDNA clones from japonica rice. Science, 301, 376 379.
39. Saitoh, Y., Ogawa, K. Nishimoto, T. (2005) Brl1p - a novel nuclear envelope protein required for nuclear transport. Traffic, 6, 502 517.
40. Schmid, M., Davison, T.S., Henz, S.R., Pape, U.J., Demar, M., Vingron, M., Schölkopf, B., Weigel, D. Lohmann, J.U. (2005) A gene expression map of Arabidopsis thaliana development. Nat. Genet. 37, 501 506.
41. Schröder, M., Giermann, N. Zrenner, R. (2005) Functional analysis of the pyrimidine de novo synthesis pathway in solanaceous species. Plant Physiol. 138, 1926 1938.
42. Schultes, N.P., Sawers, R.J.H., Brutnell, T.P. Krueger, R.W. (2000) Maize high chlorophyll fluorescent 60 mutation is caused by an Ac disruption of the gene encoding the chloroplast ribosomal small subunit protein 17. Plant J. 21, 317 327.
43. Sessions, A., Burke, E., Presting, G. et al. (2002) A high-throughput Arabidopsis reverse genetics system. Plant Cell, 14, 2985 2994.
44. Shimada, H. Sugiura, M. (1991) Fine structural features of the chloroplast genome: comparison of the sequenced chloroplast genomes. Nucleic Acids Res. 19, 983 995.
45. Silva-Filho, M.C. (2003) One ticket for multiple destinations: dual targeting of proteins to distinct subcellular locations. Curr. Opin. Plant Biol. 6, 589 595.
46. Stasolla, C., Katahira, R., Thorpe, T.A. Ashihara, H. (2003) Purine and pyrimidine nucleotide metabolism in higher plants. J. Plant Physiol. 160, 1271 1295.
47. Stolworthy, T.S., Krabbenhoft, E. Black, M.E. (2003) A novel Escherichia coli strain allows functional analysis of guanylate kinase drug resistance and sensitivity. Anal. Biochem. 322, 40 47.
48. Sugimoto, H., Kusumi, K., Tozawa, Y., Yazaki, J., Kishimoto, N., Kikuchi, S. Iba, K. (2004) The virescent-2 mutation inhibits translation of plastid transcripts for the plastid genetic system at an early stage of chloroplast differentiation. Plant Cell Physiol. 45, 985 996.
49. Taira, M., Valtersson, U., Burkhardt, B. Ludwig, R.A. (2004) Arabidopsis thaliana GLN2-encoded glutamine synthetase is dual targeted to leaf mitochondria and chloroplasts. Plant Cell, 16, 2048 2058.
50. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. Higgins, D.G. (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876 4882.
51. Tokuhisa, J.G., Vijayan, P., Feldmann, K.A. Browse, J.A. (1998) Chloroplast development at low temperatures requires a homolog of DIM1, a yeast gene encoding the 18S rRNA dimethylase. Plant Cell, 10, 699 711.
52. Xu, J., Zhang, H.-Y., Xie, C.-H., Xue, H.-W., Dijkhuis, P. Liu, C.-M. (2005) EMBRYONIC FACTOR 1 encodes an AMP deaminase and is essential for the zygote to embryo transition in Arabidopsis. Plant J. 42, 743 756.
53. Yara, A., Otani, M., Kusumi, K., Matsuda, O., Shimada, T. Iba, K. (2001) Production of transgenic japonica rice (Oryza sativa) cultivar, Taichung 65, by the Agrobacterium-mediated method. Plant Biotechnol. 18, 305 310.
54. Yoshida, S., Forno, D.A., Cock, J.H. Gomes, K.A. (1976) Routine procedure for growing rice plants in culture solution. In Laboratory Manual for Physiological Studies of Rice (Yoshida, S., ed. 3rd edn. Philippines : The International Rice Research Institute, pp. 61 66.
55. Yoshimura, A., Ideta, O. Iwata, N. (1997) Linkage map of phenotype and RFLP markers in rice. Plant Mol. Biol. 35, 49 60.
56. Zhang, C., Guinel, F.C. Moffatt, B.A. (2002) A comparative ultrastructural study of pollen development in Arabidopsis thaliana ecotype Columbia and male-sterile mutant apt1-3. Protoplasma, 219, 59 71.
57. Zrenner, R., Stitt, M., Sonnewald, U. Boldt, R. (2006) Pyrimidine and purine biosynthesis and degradation in plants. Annu. Rev. Plant Biol. 57, 805 836.