Integration of chloroplast nucleic acid metabolism into the phosphate deprivation response in Chlamydomonas reinhardtii

Plant Cell

Volumn 19, Issue 3, 2007, Pages 1023-1038

  Yehudai Resheff, Shlomit ^a,c   Zimmer, Sara L ^a,b   Komine, Yutaka ^a,d   Stern, David B ^a  

^a United States Department of Agriculture   (United States)

^b Department of Molecular Biology and Genetics   (United States)

^c TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^d TOKYO UNIVERSITY OF AGRICULTURE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; METABOLISM; RNA;

PHOSPHATE DEPRIVATION; POLYNUCLEOTIDE PHOSPHORYLASE;

GENETIC ENGINEERING;

CELLS; GENETIC ENGINEERING; METABOLISM; NUCLEIC ACIDS;

CHLAMYDOMONAS REINHARDTII;

EID: 34250749349     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.106.045427     Document Type: Article

References (85)

1. Abel, S., Ticconi, C.A., and Delatorre, C.A. (2002). Phosphate sensing in higher plants. Physiol. Plant. 115: 1-8.
2. Allen, J.F. (2003). The function of genomes in bioenergetic organelles. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358: 19-38.
3. Asamizu, E., Nakamura, Y., Sato, S., Fukuzawa, H., and Tabata, S. (1999). A large scale structural analysis of cDNAs in a unicellular green alga, Chlamydomonas reinhardtii. I. Generation of 3433 non-redundant expressed sequence tags. DNA Res. 6: 369-373.
4. Aung, K., Lin, S.I., Wu, C.C., Huang, Y.T., Su, C.L., and Chiou, T.J. (2006). pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiol. 141: 1000-1011.
5. Bari, R., Datt Pant, B., Stitt, M., and Scheible, W.R. (2006). PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol. 141: 988-999.
6. Bariola, P.A., Howard, C.J., Taylor, C.B., Verburg, M.T., Jaglan, V.D., and Green, P.J. (1994). The Arabidopsis ribonuclease gene RNS1 is tightly controlled in response to phosphate limitation. Plant J. 6: 673-685.
7. Bendich, A.J. (1987). Why do chloroplasts and mitochondria contain so many copies of their genome? Bioessays 6: 279-282.
8. Bisanz, C., Begot, L., Carol, P., Perez, P., Bligny, M., Pesey, H., Gallois, J.L., Lerbs-Mache, S., and Mache, R. (2003). The Arabidopsis nuclear DAL gene encodes a chloroplast protein which is required for the maturation of the plastid ribosomal RNAs and is essential for chloroplast differentiation. Plant Mol. Biol. 51: 651-663.
9. Bollenbach, T.J., Lange, H., Gutierrez, R., Erhardt, M., Stern, D.B., and Gagliardi, D. (2005). RNR1, a 3′-5′ exoribonuclease belonging to the RNR superfamily, catalyzes 3′ maturation of chloroplast ribosomal RNAs in Arabidopsis thaliana. Nucleic Acids Res. 33: 2751-2763.
10. Chen, D.L., Delatorre, C.A., Bakker, A., and Abel, S. (2000). Conditional identification of phosphate-starvation-response mutants in Arabidopsis thaliana. Planta 211: 13-22.
11. Chiou, T.J., Aung, K., Lin, S.I., Wu, C.C., Chiang, S.F., and Su, C.L. (2006). Regulation of phosphate homeostasis by microRNA in Arabidopsis. Plant Cell 18: 412-421.
12. Ciereszko, I., Johansson, H., Hurry, V., and Kleczkowski, L.A. (2001). Phosphate status affects the gene expression, protein content and enzymatic activity of UDP-glucose pyrophosphorylase in wild-type and pho mutants of Arabidopsis. Planta 212: 598-605.
13. Clarke, D.J., and Dowds, B.C. (1994). The gene coding for polynucleotide phosphorylase in Photorhabdus sp. strain K122 is induced at low temperatures. J. Bacteriol. 176: 3775-3784.
14. Clements, M.O., Eriksson, S., Thompson, A., Lucchini, S., Hinton, J.C., Normark, S., and Rhen, M. (2002). Polynucleotide phosphorylase is a global regulator of virulence and persistency in Salmonella enterica. Proc. Natl. Acad. Sci. USA 99: 8784-8789.
15. Crutchfield, A.L.M., Diller, K.R., and Brand, J.J. (1999). Cryopreservation of Chlamydomonas reinhardtii (Chlorophyta). Eur. J. Phycol. 34: 43-52.
16. Curtis, M.D., and Grossniklaus, U. (2003). A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133: 462-469.
17. Davies, J.P., Yildiz, F., and Grossman, A.R. (1994). Mutants of Chlamydomonas with aberrant responses to sulfur deprivation. Plant Cell 6: 53-63.
18. Davies, J.P., Yildiz, F.H., and Grossman, A.R. (1999). Sac3, an Snf1-like serine/threonine kinase that positively and negatively regulates the responses of Chlamydomonas to sulfur limitation. Plant Cell 11: 1179-1190.
19. Delhaize, E., and Randall, P.J. (1995). Characterization of a phosphate-accumulator mutant of Arabidopsis thaliana. Plant Physiol. 107: 207-213.
20. Donovan, W.P., and Kushner, S.R. (1986). Polynucleotide phosphorylase and ribonuclease II are required for cell viability and mRNA turnover in Escherichia coli K-12. Proc. Natl. Acad. Sci. USA 83: 120-124.
21. Drapier, D., Suzuki, H., Levy, H., Rimbault, B., Kindle, K.L., Stern, D.B., and Wollman, F.-A. (1998). The chloroplast atpA gene cluster in Chlamydomonas reinhardtii: Functional analysis of a polycistronic transcription unit. Plant Physiol. 117: 629-641.
22. Dreyfus, M., and Regnier, P. (2002). The poly(A) tail of mRNAs. Bodyguard in eukaryotes, scavenger in bacteria. Cell 111: 611-613.
23. Eberhard, S., Drapier, D., and Wollman, F.A. (2002). Searching limiting steps in the expression of chloroplast-encoded proteins: Relations between gene copy number, transcription, transcript abundance and translation rate in the chloroplast of Chlamydomonas reinhardtii. Plant J. 31: 149-160.
24. Emanuelsson, O., Nielsen, H., Brunak, S., and von Heijne, G. (2000). Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 300: 1005-1016.
25. Fujii, H., Chiou, T.J., Lin, S.I., Aung, K., and Zhu, J.K. (2005). A miRNA involved in phosphate-starvation response in Arabidopsis. Curr. Biol. 15: 2038-2043.
26. Goverde, R.L., Huis in't Veld, J.H., Kusters, J.G., and Mooi, F.R. (1998). The psychrotrophic bacterium Yersinia enterocolitica requires expression of pnp, the gene for polynucleotide phosphorylase, for growth at low temperature (5°C). Mol. Microbiol. 28: 555-569.
27. Green, P.J. (1994). The ribonucleases of higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45: 421-445.
28. Grossman, A. (2000). Acclimation of Chlamydomonas reinhardtii to its nutrient environment. Protist 151: 201-224.
29. Hahnen, E., Znamenskaya, L., Koczan, D., and Leshchinskaya, I. (2000). A novel secreted ribonuclease from Bacillus intermedius: Gene structure and regulatory control. Mol. Gen. Genet. 263: 571-580.
30. Harris, E.H. (1989). The Chlamydomonas Sourcebook: A Comprehensive Guide to Biology and Laboratory Use. (San Diego, CA: Academic Press).
31. Hausler, R.E., Schlieben, N.H., Schulz, B., and Flugge, U.I. (1998). Compensation of decreased triose phosphate/phosphate translocator activity by accelerated starch turnover and glucose transport in transgenic tobacco. Planta 204: 366-376.
32. Hayes, R., Kudla, J., Schuster, G., Gabay, L., Maliga, P., and Gruissem, W. (1996). Chloroplast mRNA 3′-end processing by a high molecular weight protein complex is regulated by nuclear encoded RNA binding proteins. EMBO J. 15: 1132-1141.
33. Helliwell, C., and Waterhouse, P. (2003). Constructs and methods for high-throughput gene silencing in plants. Methods 30: 289-295.
34. Hwang, S., Kawazoe, R., and Herrin, D.L. (1996). Transcription of tufA and other chloroplast-encoded genes is controlled by a circadian clock in Chlamydomonas. Proc. Natl. Acad. Sci. USA 93: 996-1000.
35. Irihimovitch, V., and Stern, D.B. (2006). The SAC3 kinase is required for chloroplast transcriptional repression under sulfur limitation in Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 103: 7911-7916.
36. Kishine, M., Takabayashi, A., Munekage, Y., Shikanai, T., Endo, T., and Sato, F. (2004). Ribosomal RNA processing and an RNase R family member in chloroplasts of Arabidopsis. Plant Mol. Biol. 55: 595-606.
37. Kobayashi, K., Masuda, T., Takamiya, K.-i., and Ohta, H. (2006). Membrane lipid alteration during phosphate starvation is regulated by phosphate signaling and auxin/cytokinin cross-talk. Plant J. 47: 238-248.
38. Koumandou, V.L., Nisbet, R.E.R., Barbrook, A.C., and Howe, C.J. (2004). Dinoflagellate chloroplasts - Where have all the genes gone? Trends Genet. 20: 261-267.
39. Kudla, J., Hayes, R., and Gruissem, W. (1996). Polyadenylation accelerates degradation of chloroplast mRNA. EMBO J. 15: 7137-7146.
40. Lee, T.-M., Tsai, P.-F., Shyu, Y.-T., and Sheu, F. (2005). The effects of phosphite on phosphate starvation responses of Ulva lactuca (Ulvales, Chlorophyta). J. Phycol. 41: 975-982.
41. 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.
42. Lisitsky, I., Kotler, A., and Schuster, G. (1997). The mechanism of preferential degradation of polyadenylated RNA in the chloroplast: The exoribonuclease 100RNP-polynucleotide phosphorylase displays high binding affinity for poly(A) sequences. J. Biol. Chem. 272: 17648-17653.
43. Luttinger, A., Hahn, J., and Dubnau, D. (1996). Polynucleotide phosphorylase is necessary for competence development in Bacillus subtilis. Mol. Microbiol. 19: 343-356.
44. Misson, J., et al. (2005). A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proc. Natl. Acad. Sci. USA 102: 11934-11939.
45. Misumi, O., Suzuki, L., Nishimura, Y., Sakai, A., Kawano, S., Kuroiwa, H., and Kuroiwa, T. (1999). Isolation and phenotypic characterization of Chlamydomonas reinhardtii mutants defective in chloroplast DNA segregation. Protoplasma 209: 273-282.
46. Miura, K., Rus, A., Sharkhuu, A., Yokoi, S., Karthikeyan, A.S., Raghothama, K.G., Baek, D., Koo, Y.D., Jin, J.B., Bressan, R.A., Yun, D.-J., and Hasegawa, P.M. (2005). The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proc. Natl. Acad. Sci. USA 102: 7760-7765.
47. Morita, T., Kawamoto, H., Mizota, T., Inada, T., and Aiba, H. (2004). Enolase in the RNA degradosome plays a crucial role in the rapid decay of glucose transporter mRNA in the response to phosphosugar stress in Escherichia coli. Mol. Microbiol. 54: 1063-1075.
48. Moseley, J.L., Chang, C.-W., and Grossman, A.R. (2006). Genome-based approaches to understanding phosphorus deprivation responses and PSR1 control in Chlamydomonas reinhardtii. Eukaryot. Cell 5: 26-44.
49. Nishimura, Y., Kikis, E.A., Zimmer, S.L., Komine, Y., and Stern, D.B. (2004). Antisense transcript and RNA processing alterations suppress instability of polyadenylated mRNA in Chlamydomonas chloroplasts. Plant Cell 16: 2849-2869.
50. Nishimura, Y., Misumi, O., Kato, K., Inada, N., Higashiyama, T., Momoyama, Y., and Kuroiwa, T. (2002). An mt(+) gamete-specific nuclease that targets mt(-) chloroplasts during sexual reproduction in C. reinhardtii. Genes Dev. 16: 1116-1128.
51. Nishimura, Y., Misumi, O., Matsunaga, S., Higashiyama, T., Yokota, A., and Kuroiwa, T. (1999). The active digestion of uniparental chloroplast DNA in a single zygote of Chlamydomonas reinhardtii is revealed by using the optical tweezer. Proc. Natl. Acad. Sci. USA 96: 12577-12582.
52. Nürnberger, T., Abel, S., Jost, W., and Glund, K. (1989). Induction of an extracellular ribonuclease in cultured tomato cells upon phosphate starvation. Plant Physiol. 92: 970-976.
53. Perrin, R., Lange, H., Grienenberger, J.M., and Gagliardi, D. (2004). AtmtPNPase is required for multiple aspects of the 18S rRNA metabolism in Arabidopsis thaliana mitochondria. Nucleic Acids Res. 32: 5174-5182.
54. Persson, B.L., Lagerstedt, J.O., Pratt, J.R., Pattison-Granberg, J., Lundh, K., Shokrollahzadeh, S., and Lundh, F. (2003). Regulation of phosphate acquisition in Saccharomyces cerevisiae. Curr. Genet. 43: 225-244.
55. Poirier, Y., and Bucher, M. (September 30, 2002). Phosphate transport and homeostasis in Arabidopsis. In The Arabidopsis Book, C.R. Somerville and E.M. Meyerowitz, eds (Rockville, MD: American Society of Plant Biologists), doi/10.1199/tab.0099, http://www.aspb.org/publications/arabidopsis/ .
56. Race, H.L., Herrmann, R.G., and Martin, W. (1999). Why have organelles retained genomes? Trends Genet. 15: 364-370.
57. Ris, H., and Plaut, W. (1962). Ultrastructure of DNA-containing areas in the chloroplast of Chlamydomonas. J. Cell Biol. 13: 383-391.
58. Rochaix, J.-D. (1980). Restriction fragments from Chlamydomonas chloroplast DNA. Methods Enzymol. 65: 785-795.
59. Rohr, J., Sarkar, N., Balenger, S., Jeong, B.R., and Cerutti, H. (2004). Tandem inverted repeat system for selection of effective transgenic RNAi strains in Chlamydomonas. Plant J. 40: 611-621.
60. Rosenzweig, J.A., Weltman, G., Plano, G.V., and Schesser, K. (2005). Modulation of Yersinia type three secretion system by the S1 domain of polynucleotide phosphorylase. J. Biol. Chem. 280: 156-163.
61. Rubio, V., Linhares, F., Solano, R., Martin, A.C., Iglesias, J., Leyva, A., and Paz-Ares, J. (2001). A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev. 15: 2122-2133.
62. Sarkar, D., and Fisher, P.B. (2006). Human polynucleotide phosphorylase (hPNPase old-35): An RNA degradation enzyme with pleiotrophic biological effects. Cell Cycle 5: 1080-1084.
63. Sauret-Gueto, S., Botella-Pavia, P., Flores-Perez, U., Martinez-Garcia, J.F., San Roman, C., Leon, P., Boronat, A., and Rodriguez-Concepcion, M. (2006). Plastid cues posttranscriptionally regulate the accumulation of key enzymes of the methylerythritol phosphate pathway in Arabidopsis. Plant Physiol. 141: 75-84.
64. Schroda, M., Beck, C.F., and Vallon, O. (2002). Sequence elements within an HSP70 promoter counteract transcriptional transgene silencing in Chlamydomonas. Plant J. 31: 445-455.
65. Schuster, G., Lisitsky, I., and Klaff, P. (1999). Polyadenylation and degradation of mRNA in the chloroplast. Plant Physiol. 120: 937-944.
66. 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.
67. Shaver, J.M., Oldenburg, D.J., and Bendich, A.J. (2006). Changes in chloroplast DNA during development in tobacco, Medicago truncatula, pea, and maize. Planta 224: 72-82.
68. Shimogawara, K., Fujiwara, S., Grossman, A., and Usuda, H. (1998). High-efficiency transformation of Chlamydomonas reinhardtii by electroporation. Genetics 148: 1821-1828.
69. Shimogawara, K., Wykoff, D.D., Usuda, H., and Grossman, A.R. (1999). Chlamydomonas reinhardtii mutants abnormal in their responses to phosphorus deprivation. Plant Physiol. Biochem. 120: 685-694.
70. Slomovic, S., Portnoy, V., Liveanu, V., and Schuster, G. (2006). RNA polyadenylation in prokaryotes and organelles: Different tails tell different tales. CRC Crit. Rev. Plant Sci. 25: 65-77.
71. Tasaki, Y., Azwan, A., Hara, T., and Joh, T. (2004). Structure and expression of a phosphate deficiency-inducible ribonuclease gene in Pholiota nameko. Curr. Genet. 45: 28-36.
72. Ticconi, C.A., Delatorre, C.A., and Abel, S. (2001). Attenuation of phosphate starvation responses by phosphite in Arabidopsis. Plant Physiol. 127: 963-972.
73. Varadarajan, D.K., Karthikeyan, A.S., Matilda, P.D., and Raghothama, K.G. (2002). Phosphite, an analog of phosphate, suppresses the coordinated expression of genes under phosphate starvation. Plant Physiol. 129: 1232-1240.
74. Versaw, W.K., and Harrison, M.J. (2002). A chloroplast phosphate transporter, PHT2;1, influences allocation of phosphate within the plant and phosphate-starvation responses. Plant Cell 14: 1751-1766.
75. Walter, M., Kilian, J., and Kudla, J. (2002). PNPase activity determines the efficiency of mRNA 3′-end processing, the degradation of tRNA and the extent of polyadenylation in chloroplasts. EMBO J. 21: 6905-6914.
76. Weber, A.P. (2004). Solute transporters as connecting elements between cytosol and plastid stroma. Curr. Opin. Plant Biol. 7: 247-253.
77. Wu, P., Ma, L., Hou, X., Wang, M., Wu, Y., Liu, F., and Deng, X.W. (2003). Phosphate starvation triggers distinct alterations of genome expression in Arabidopsis roots and leaves. Plant Physiol. 132: 1260-1271.
78. Wurtz, E.A., Boynton, J.E., and Gillham, N.W. (1977). Perturbation of chloroplast DNA amounts and chloroplast gene transmission in Chlamydomonas reinhardtii by 5-fluorodeoxyuridine. Proc. Natl. Acad. Sci. USA 74: 4552-4556.
79. Wykoff, D.D., Grossman, A.R., Weeks, D.P., Usuda, H., and Shimogawara, K. (1999). Psr1, a nuclear localized protein that regulates phosphorus metabolism in Chlamydomonas. Proc. Natl. Acad. Sci. USA 96: 15336-15341.
80. Xing, T., Malik, K., Martin, T., and Miki, B.L. (2001). Activation of tomato PR and wound-related genes by a mutagenized tomato MAP kinase kinase through divergent pathways. Plant Mol. Biol. 46: 109-120.
81. Yamanaka, K., and Inouye, M. (2001). Selective mRNA degradation by polynucleotide phosphorylase in cold shock adaptation in Escherichia coli. J. Bacteriol. 183: 2808-2816.
82. Yang, K., and Metcalf, W.W. (2004). A new activity for an old enzyme: Escherichia coli bacterial alkaline phosphatase is a phosphite-dependent hydrogenase. Proc. Natl. Acad. Sci. USA 101: 7919-7924.
83. Yehudai-Resheff, S., Hirsh, M., and Schuster, G. (2001). Polynucleotide phosphorylase functions as both an exonuclease and a poly(A) polymerase in spinach chloroplasts. Mol. Cell. Biol. 21: 5408-5416.
84. Yehudai-Resheff, S., Portnoy, V., Yogev, S., Adir, N., and Schuster, G. (2003). Domain analysis of the chloroplast polynucleotide phosphorylase reveals discrete functions in RNA degradation, polyadenylation, and sequence homology with exosome proteins. Plant Cell 15: 2003-2019.
85. Zilhao, R., Cairrao, F., Regnier, P., and Arraiano, C.M. (1996). PNPase modulates RNase II expression in Escherichia coli: Implications for mRNA decay and cell metabolism. Mol. Microbiol. 20: 1033-1042.