Mutations defective in ribonucleotide reductase activity interfere with pollen plastid DNA degradation mediated by DPD1 exonuclease

Plant Journal

Volumn 70, Issue 4, 2012, Pages 637-649

  Tang, Lay Yin ^a   Matsushima, Ryo ^a   Sakamoto, Wataru ^a  

^a OKAYAMA UNIVERSITY   (Japan)

Author keywords

Arabidopsis; exonuclease; nucleotide biosynthesis; organellar DNA; plastid; pollen

Indexed keywords

ARABIDOPSIS; DNA DEGRADATION; EXONUCLEASE; MITOCHONDRIAL DNA; PLASTID; POLLEN; POLLEN DEVELOPMENT; POLLEN MATURATION; RATE-LIMITING STEPS; REPRODUCTIVE TISSUES; RIBONUCLEOTIDE REDUCTASE;

BIOCHEMISTRY; BIOSYNTHESIS; DEGRADATION; MITOCHONDRIA; NUCLEOTIDES;

DNA;

ARABIDOPSIS PROTEIN; DPD1 PROTEIN, ARABIDOPSIS; EXORIBONUCLEASE; MITOCHONDRIAL DNA; PHOTOPROTEIN; PLANT DNA; RIBONUCLEOTIDE REDUCTASE;

ARABIDOPSIS; ARTICLE; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENETICS; METABOLISM; MUTATION; PHENOTYPE; PLASTID; POLLEN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCANNING ELECTRON MICROSCOPY; TRANSGENIC PLANT; ULTRASTRUCTURE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; DNA, MITOCHONDRIAL; DNA, PLANT; EXORIBONUCLEASES; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; GENETIC COMPLEMENTATION TEST; LUMINESCENT PROTEINS; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, FLUORESCENCE; MUTATION; PHENOTYPE; PLANTS, GENETICALLY MODIFIED; PLASTIDS; POLLEN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RIBONUCLEOTIDE REDUCTASES;

ARABIDOPSIS;

EID: 84861336892     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2012.04904.x     Document Type: Article

References (69)

1. Abdelnoor, R.V., Yule, R., Elo, A., Christensen, A.C., Meyer-Gauen, G., and, Mackenzie, S.A., (2003) Substoichiometric shifting in the plant mitochondrial genome is influenced by a gene homologous to MutS. Proc. Natl Acad. Sci. USA, 100, 5968-5973.
2. Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature, 408, 796-815.
3. Bennett, M.D., and, Smith, J.B., (1976) Nuclear DNA amounts in angiosperms. Philos. Trans. R. Soc. Lond. B Biol. Sci. 274, 227-274.
4. Berthomé, R., Thomasset, M., Maene, M., Bourgeois, N., Froger, N., and, Budar, F., (2008) pur4 mutations are lethal to the male, but not the female, gametophyte and affect sporophyte development in Arabidopsis. Plant Physiol. 147, 650-660.
5. Bourdon, A., Minai, L., Serre, V., et al. (2007) Mutation of RRM2B, encoding p53-controlled ribonucleotide reductase (p53R2), causes severe mitochondrial DNA depletion. Nat. Genet. 39, 776-780.
6. Cahours, X., Morin, P., and, Dreux, M., (1998) Capillary electrophoretic study of the complexation of nucleotides with magnesium and calcium ions. Chromatographia, 48, 739-744.
7. Chen, X.J., and, Butow, R.A., (2005) The organization and inheritance of the mitochondrial genome. Nat. Rev. Genet. 6, 815-825.
8. Clough, S.J., and, Bent, A.F., (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
9. Coschigano, K.T., Melo-Oliveira, R., Lim, J., and, Coruzzi, G.M., (1998) Arabidopsis gls mutants and distinct Fd-GOGAT genes: implications for photorespiration and primary nitrogen assimilation. Plant Cell 10, 741-752.
10. Douce, R., and, Neuburger, M., (1999) Biochemical dissection of photorespiration. Curr. Opin. Plant Biol. 2, 214-222.
11. Elledge, S.J., Zhou, Z., and, Allen, J.B., (1992) Ribonucleotide reductase: regulation, regulation, regulation. Trends Biochem. Sci. 17, 119-123.
12. Farre, E.M., Tiessen, A., Roessner, U., Geigenberger, P., Trethewey, R.N., and, Willmitzer, L., (2001) Analysis of the compartmentation of glycolytic intermediates, nucleotides, sugars, organic acids, amino acids, and sugar alcohols in potato tubers using a nonaqueous fractionation method. Plant Physiol. 127, 685-700.
13. Frey, C.M., and, Stuehr, J.E., (1972) Interactions of divalent metal ions with inorganic and nucleotide phosphates. I. Thermodynamics. J. Am. Chem. Soc. 94, 8898-8904.
14. Garton, S., Knight, H., Warren, G.J., Knight, M.R., and, Thorlby, G.J., (2007) crinkled leaves 8- a mutation in the large subunit of ribonucleotide reductase-leads to defects in leaf development and chloroplast division in Arabidopsis thaliana. Plant J. 50, 118-127.
15. Geigenberger, P., Regierer, B., Nunes-Nesi, A., Leisse, A., Urbanczyk-Wochniak, E., Springer, F., van Dongen, J.T., Kossmann, J., and, Fernie, A.R., (2005) Inhibition of de novo pyrimidine synthesis in growing potato tubers leads to a compensatory stimulation of the pyrimidine salvage pathway and a subsequent increase in biosynthetic performance. Plant Cell, 17, 2077-2088.
16. Gray, M.W., (1993) Origin and evolution of organelle genomes. Curr. Opin. Genet. Dev. 3, 884-890.
17. Honys, D., and, Twell, D., (2004) Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol. 5, R85.
18. Hung, W.-F., Chen, L.-J., Boldt, R., Sun, C.-W., and, Li, H.-M., (2004) Characterization of Arabidopsis glutamine phosphoribosyl pyrophosphate amidotransferase-deficient mutants. Plant Physiol. 135, 1314-1323.
19. Inada, N., Sakai, A., Kuroiwa, H., and, Kuroiwa, T., (1999) Senescence program in rice (Oryza sautiva L.) leaves: analysis of the blade of the second leaf at the tissue and cellular levels. Protoplasma, 207, 222-232.
20. Jamai, A., Salome, P.A., Schilling, S.H., Weber, A.P.M., and, McClung, C.R., (2009) Arabidopsis photorespiratory serine hydroxymethyltransferase activity requires the mitochondrial accumulation of ferredoxin-dependent glutamate synthase. Plant Cell, 21, 595-606.
21. Jung, B., Florchinger, M., Kunz, H.-H., Traub, M., Wartenberg, R., Jeblick, W., Neuhaus, H.E., and, Mohlmann, T., (2009) Uridine-ribohydrolase is a key regulator in the uridine degradation pathway of Arabidopsis. Plant Cell, 21, 876-891.
22. Kampfenkel, K., Möhlmann, T., Batz, O., Montagu, M.V., Inzé, D., and, Neuhaus, H.E., (1995) Molecular characterization of an Arabidopsis thaliana cDNA encoding a novel putative adenylate translocator of higher plants. FEBS Lett. 374, 351-355.
23. Kuang, A., and, Musgrave, M.E., (1996) Dynamics of vegetative cytoplasm during generative cell formation and pollen maturation Arabidopsis thaliana. Protoplasma 194, 81-90.
24. Kucera, R., and, Paulus, H., (1986) Localization of the deoxyribonucleotide biosynthetic enzymes ribonucleotide reductase and thymidylate synthase in mouse L cells. Exp. Cell Res. 167, 417-428.
25. Kuroiwa, T., (2010) Review of cytological studies on cellular and molecular mechanisms of uniparental (maternal or paternal) inheritance of plastid and mitochondrial genomes induced by active digestion of organelle nuclei (nucleoids). J. Plant. Res. 123, 207-230.
26. Kuroiwa, T., Suzuki, T., Ogawa, K., and, Kawano, S., (1981) The chloroplast nucleus: distribution, number, size, and shape, and a model for the multiplication of the chloroplast genome during chloroplast development. Plant Cell Physiol. 22, 381-396.
27. Lamppa, G.K., and, Bendich, A.J., (1979) Changes in chloroplast DNA levels during development of pea (Pisum sativum). Plant Physiol. 64, 126-130.
28. Li, W., Ruf, S., and, Bock, R., (2006) Constancy of organellar genome copy numbers during leaf development and senescence in higher plants. Mol. Genet. Genomics, 275, 185-192.
29. Lincker, F., Philipps, G., and, Chabouté, M.-E., (2004) UV-C response of the ribonucleotide reductase large subunit involves both E2F-mediated gene transcriptional regulation and protein subcellular relocalization in tobacco cells. Nucleic Acids Res. 32, 1430-1438.
30. Mainguet, S.E., Gakière, B., Majira, A., Pelletier, S., Bringel, F., Guérard, F., Caboche, M., Berthomé, R., and, Renou, J.P., (2009) Uracil salvage is necessary for early Arabidopsis development. Plant J. 60, 280-291.
31. Marchler-Bauer, A., Anderson, J.B., Derbyshire, M.K., et al. (2006) CDD: a conserved domain database for interactive domain family analysis. Nucleic Acids Res. 35, D237-D240.
32. Martinez-Zapater, J.M., Gil, P., Capel, J., and, Somerville, C.R., (1992) Mutations at the Arabidopsis CHM locus promote rearrangements of the mitochondrial genome. Plant Cell, 4, 889-899.
33. Matsushima, R., Hamamura, Y., Higashiyama, T., Arimura, S.-I., Sodmergen, Tsutsumi, N., and, Sakamoto, W., (2008a) Mitochondrial dynamics in plant male gametophyte visualized by fluorescent live imaging. Plant Cell Physiol. 49, 1074-1083.
34. Matsushima, R., Hu, Y., Toyoda, K., Sodmergen, and, Sakamoto, W., (2008b) The model plant Medicago truncatula exhibits biparental plastid inheritance. Plant Cell Physiol. 49, 81-91.
35. 2+-dependent exonuclease degrades organelle DNA during Arabidopsis pollen development. Plant Cell, 23, 1608-1624.
36. McCormick, S., (1993) Male gametophyte development. Plant Cell, 5, 1265-1275.
37. Miura, E., Kato, Y., Matsushima, R., Albrecht, V., Laalami, S., and, Sakamoto, W., (2007) The balance between protein synthesis and degradation in chloroplasts determines leaf variegation in Arabidopsis yellow variegated mutants. Plant Cell, 19, 1313-1328.
38. Nagata, N., (2010) Mechanisms for independent cytoplasmic inheritance of mitochondria and plastids in angiosperms. J. Plant. Res. 123, 193-199.
39. Nagata, N., Saito, C., Sakai, A., Kuroiwa, H., and, Kuroiwa, T., (1999) The selective increase or decrease of organellar DNA in generative cells just after pollen mitosis one controls cytoplasmic inheritance. Planta, 209, 53-65.
40. Neuhaus, H.E., Thom, E., Möhlmann, T., Steup, M., and, Kampfenkel, K., (1997) Characterization of a novel eukaryotic ATP/ADP translocator located in the plastid envelope of Arabidopsis thaliana L. Plant J. 11, 73-82.
41. Nishimura, Y., Higashiyama, T., Suzuki, L., Misumi, O., and, Kuroiwa, T., (1998) The biparental transmission of the mitochondrial genome in Chlamydomonas reinhardtii visualized in living cell. Eur. J. Cell Biol. 77, 124-133.
42. - chloroplasts during sexual reproduction in C. reinhardtii. Genes Dev. 16, 1116-1128.
43. Paungfoo-Lonhienne, C., Lonhienne, T.G.A., Mudge, S.R., Schenk, P.M., Christie, M., Carroll, B.J., and, Schmidt, S., (2010) DNA is taken up by root hairs and pollen, and stimulates root and pollen tube growth. Plant Physiol. 153, 799-805.
44. Pontarin, G., Fijolek, A., Pizzo, P., Ferraro, P., Rampazzo, C., Pozzan, T., Thelander, L., Reichard, P.A., and, Bianchi, V., (2008) Ribonucleotide reduction is a cytosolic process in mammalian cells independently of DNA damage. Proc. Natl Acad. Sci. USA, 105, 17801-17806.
45. Preuten, T., Cincu, E., Fuchs, J., Zoschke, R., Liere, K., and, Börner, T., (2010) Fewer genes than organelles: extremely low and variable gene copy numbers in mitochondria of somatic plant cells. Plant J. 64, 948-959.
46. Rauwolf, U., Golczyk, H., Greiner, S., and, Herrmann, R., (2010) Variable amounts of DNA related to the size of chloroplasts III. Biochemical determinations of DNA amounts per organelle. Mol. Genet. Genomics, 283, 35-47.
47. Rowan, B.A., Oldenburg, D.J., and, Bendich, A.J., (2004) The demise of chloroplast DNA in Arabidopsis. Curr. Genet. 46, 176-181.
48. Rowan, B., Oldenburg, D., and, Bendich, A., (2009) A multiple-method approach reveals a declining amount of chloroplast DNA during development in Arabidopsis. BMC Plant Biol. 9, 3.
49. Sakamoto, W., Kondo, H., Murata, M., and, Motoyoshi, F., (1996) Altered mitochondrial gene expression in a maternal distorted leaf mutant of Arabidopsis induced by chloroplast mutator. Plant Cell, 8, 1377-1390.
50. Sakamoto, W., Miyagishima, S.Y., and, Jarvis, P., (2008) Chloroplast biogenesis: control of plastid development, protein import, division and inheritance. in The Arabidopsis Book, 6 (, Sommerville, C.R., and, Meyerowitz, E.M,., eds). Rockville, MD: The American Society of Plant Biologists, p. e0110; doi:.
51. Sears, B.B., and, VanWinkle-Swift, K., (1994) The salvage/turnover/repair (STOR) model for uniparental inheritance in Chlamydomonas: DNA as a source of sustenance. J. Hered. 85, 366-376.
52. Sodmergen, Kawano, S., Tano, S., and, Kuroiwa, T., (1991) Degradation of chloroplast DNA in second leaves of rice Oryza sativa before leaf yellowing. Protoplasma 160, 89-98.
53. Stitt, M., Lilley, R.M., and, Heldt, H.W., (1982) Adenine nucleotide levels in the cytosol, chloroplasts, and mitochondria of wheat leaf protoplasts. Plant Physiol. 70, 971-977.
54. Stitt, M., Lilley, R.M., Gerhardt, R., and, Heldt, H.W., (1989) Metabolite levels in specific cells and subcellular compartments of plant leaves. Methods Enzymol. 174, 518-552.
55. Takanashi, H., Ohnishi, T., Mogi, M., Okamoto, T., Arimura, S., and, Tsutsumi, N., (2010) Studies of mitochondrial morphology and DNA amount in the rice egg cell. Curr. Genet. 56, 33-41.
56. Takechi, K., Sodmergen, Murata, M., Motoyoshi, F., and, Sakamoto, W., (2000) The YELLOW VARIEGATED (VAR2) locus encodes a homologue of FtsH, an ATP-dependent protease in Arabidopsis. Plant Cell Physiol. 41, 1334-1346.
57. Tang, L.Y., and, Sakamoto, W., (2011) Tissue-specific organelle DNA degradation mediated by DPD1 exonuclease. Plant Signal. Behav. 6, 1391-1393.
58. Tang, L.Y., Nagata, N., Matsushima, R., Chen, Y., Yoshioka, Y., and, Sakamoto, W., (2009) Visualization of plastids in pollen grains: involvement of FtsZ1 in pollen plastid division. Plant Cell Physiol. 50, 904-908.
59. Tyynismaa, H., Ylikallio, E., Patel, M., Molnar, M.J., Haller, R.G., and, Suomalainen, A., (2009) A heterozygous truncating mutation in RRM2B causes autosomal-dominant progressive external ophthalmoplegia with multiple mtDNA deletions. Am. J. Hum. Genet. 85, 290-295.
60. Van Aelst, A.C., and, Van Went, J.L., (1992) Ultrastructural immuno-localization of pectins and glycoproteins Arabidopsis thaliana pollen grains. Protoplasma, 168, 14-19.
61. Wang, C., and, Liu, Z., (2006) Arabidopsis ribonucleotide reductases are critical for cell cycle progression, DNA damage repair, and plant development. Plant Cell, 18, 350-365.
62. Wang, D.-Y., Zhang, Q., Liu, Y., Lin, Z.-F., Zhang, S.-X., Sun, M.-X., and, Sodmergen, (2010) The levels of male gametic mitochondrial DNA are highly regulated in angiosperms with regard to mitochondrial inheritance. Plant Cell, 22, 2402-2416.
63. Winkler, H.H., and, Neuhaus, H.E., (1999) Non-mitochondrial ATP transport. Trends Biochem. Sci. 24, 64-68.
64. Yang, H.Y., (1986) Fluorescein diacetate used as a vital stain for labeling living pollen tubes. Plant Sci. 44, 59-63.
65. Yehudai-Resheff, S., Zimmer, S.L., Komine, Y., and, Stern, D.B., (2007) Integration of chloroplast nucleic acid metabolism into the phosphate deprivation response in Chlamydomonas reinhardtii. Plant Cell, 19, 1023-1038.
66. Ylikallio, E., Page, J.L., Xu, X., Lampinen, M., Bepler, G., Ide, T., Tyynismaa, H., Weiss, R.S., and, Suomalainen, A., (2010) Ribonucleotide reductase is not limiting for mitochondrial DNA copy number in mice. Nucleic Acids Res. 38, 8208-8218.
67. Yoo, S.-C., Cho, S.-H., Sugimoto, H., Li, J., Kusumi, K., Koh, H.-J., Iba, K., and, Paek, N.-C., (2009) Rice Virescent3 and Stripe1 encoding the large and small subunits of ribonucleotide reductase are required for chloroplast biogenesis during early leaf development. Plant Physiol. 150, 388-401.
68. Zrenner, R., Stitt, M., Sonnewald, U., and, Boldt, R., (2006) Pyrimidine and purine biosynthesis and degradation in plants. Annu. Rev. Plant Biol. 57, 805-836.
69. Zrenner, R., Riegler, H., Marquard, C.R., Lange, P.R., Geserick, C., Bartosz, C.E., Chen, C.T., and, Slocum, R.D., (2009) A functional analysis of the pyrimidine catabolic pathway in Arabidopsis. New Phytol. 183, 117-132.