A poly(A)-specific ribonuclease directly regulates the poly(A) status of mitochondrial mRNA in Arabidopsis

Nature Communications

Volumn 4, Issue , 2013, Pages

  Hirayama, Takashi ^a   Matsuura, Takakazu ^a   Ushiyama, Sho ^b   Narusaka, Mari ^c   Kurihara, Yukio ^d   Yasuda, Michiko ^e   Ohtani, Misato ^e   Seki, Motoaki ^d   Demura, Taku ^e   Nakashita, Hideo ^e   Narusaka, Yoshihiro ^c   Hayashi, Shimpei ^b  

^a OKAYAMA UNIVERSITY   (Japan)

^b YOKOHAMA CITY UNIVERSITY   (Japan)

^c Research Institute for Biological Sciences   (Japan)

^d Elements Chemistry Laboratory   (Japan)

^e RIKEN   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AGS1 PROTEIN; COMPLEMENTARY DNA; MITOCHONDRIAL RNA; POLYNUCLEOTIDE ADENYLYLTRANSFERASE; UNCLASSIFIED DRUG;

ENZYME ACTIVITY; EUKARYOTE; GENE EXPRESSION; MICROBIAL COMMUNITY; MITOCHONDRION; PROTEIN;

ARABIDOPSIS; ARTICLE; DNA SYNTHESIS; GENE MUTATION; IN VITRO STUDY; MITOCHONDRIAL GENE; MUTANT; NONHUMAN; PHENOTYPE; PROTEIN ANALYSIS; PROTEIN PURIFICATION; REGULATORY MECHANISM; TRANSCRIPTION REGULATION; TRANSGENIC PLANT;

EID: 84881354573     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms3247     Document Type: Article

References (47)

1. Butow, R. A. & Avadhani, N. G. Mitochondrial signaling: the retrograde response. Mol. Cell. 14, 1-15 (2004). (Pubitemid 38469905)
2. Woodson, J. D. & Chory, J. Coordination of gene expression between organellar and nuclear genomes. Nat. Rev. Genet. 9, 383-395 (2008). (Pubitemid 351559601)
3. Burger, G., Gray, M. W. & Franz Lang, B. Mitochondrial genomes: anything goes. Trends Genet. 19, 709-716 (2003). (Pubitemid 37464849)
4. Marienfeld, J., Unseld, M. & Brennicke, A. The mitochondrial genome of Arabidopsis is composed of both native and immigrant information. Trends Plant Sci. 4, 495-502 (1999).
5. Covello, P. S. & Gray, M. W. RNA editing in plant mitochondria. Nature 341, 662-666 (1989). (Pubitemid 19257319)
6. Hiesel, R., Wissinger, B., Schuster, W. & Brennicke, A. RNA editing in plant mitochondria. Science 246, 1632-1634 (1989). (Pubitemid 20036704)
7. Saha, D., Prasad, A. M. & Srinivasan, R. Pentatricopeptide repeat proteins and their emerging roles in plants. Plant Physiol. Biochem. 45, 521-534 (2007). (Pubitemid 47102628)
8. Schmitz-Linneweber, C. & Small, I. Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci. 13, 663-670 (2008).
9. Lange, H., Sement, F. M., Canaday, J. & Gagliardi, D. Polyadenylation-assisted RNA degradation processes in plants. Trends Plant Sci. 14, 497-504 (2009).
10. Binder, S. & Brennicke, A. Gene expression in plant mitochondria: transcriptional and post-transcriptional control. Phil. Trans. R. Soc. Lond. B 358, 181-189 (2003). (Pubitemid 36178227)
11. Houseley, J., LaCava, J. & Tollervey, D. RNA-quality control by the exosome. Nat. Rev. Mol. Cell Biol. 7, 529-539 (2006). (Pubitemid 44036458)
12. Doma, M. K. & Parker, R. RNA quality control in eukaryotes. Cell 131, 660-668 (2007). (Pubitemid 350087205)
13. Isken, O. & Maquat, L. E. Quality control of eukaryotic mRNA: safeguarding cells from abnormal mRNA function. Genes Dev. 21, 1833-1856 (2007). (Pubitemid 47204924)
14. Goldstrohm, A. C. & Wickens, M. Multifunctional deadenylase complexes diversify mRNA control. Nat. Rev. Mol. Cell Biol. 9, 337-344 (2008). (Pubitemid 351430850)
15. Eckmann, C. R., Rammelt, C. & Wahle, E. Control of poly(A) tail length. Wiley Interdiscip. Rev. RNA 2, 348-361 (2011).
16. Gagliardi, D., Stepien, P. P., Temperley, R. J., Lightowlers, R. N. & Chrzanowska-Lightowlers, Z. M. Messenger RNA stability in mitochondria: different means to an end. Trends Genet. 20, 260-267 (2004). (Pubitemid 38625684)
17. Chang, J. H. & Tong, L. Mitochondrial poly(A) polymerase and polyadenylation. BBA Gene Regul. Mech. 1819, 992-997 (2012).
18. Schuster, G. & Stern, D. in Molecular Biology of RNA Processing and Decay in Prokaryotes (Academic Press 85, 393-422, 2009).
19. Reverdatto, S. V., Dutko, J. A., Chekanova, J. A., Hamilton, D. A. & Belostotsky, D. A. Mrna deadenylation by PARN is essential for embryogenesis in higher plants. RNA 10, 1200-1214 (2004). (Pubitemid 38989006)
20. Chiba, Y. et al. AtPARN is an essential poly(A) ribonuclease in Arabidopsis. Gene 328, 95-102 (2004). (Pubitemid 38352885)
21. Nishimura, N. et al. Analysis of ABA hypersensitive germination2 revealed the pivotal functions of PARN in stress response in Arabidopsis. Plant J. 44, 972-984 (2005). (Pubitemid 43906726)
22. Nishimura, N. et al. ABA hypersensitive germination2-1 causes the activation of both abscisic acid and salicylic acid responses in Arabidopsis. Plant Cell Physiol. 50, 2112-2122 (2009).
23. Zimmer, S. L., Schein, A., Zipor, G., Stern, D. B. & Schuster, G. Polyadenylation in Arabidopsis and Chlamydomonas organelles: the input of nucleotidyltransferases, poly(A) polymerases and polynucleotide phosphorylase. Plant J. 59, 88-99 (2009).
24. Sallés, F. J., Richards, W. G. & Strickland, S. Assaying the polyadenylation state of mRNAs. Methods 17, 38-45 (1999). (Pubitemid 29440545)
25. Forner, J., Weber, B., Thuss, S., Wildum, S. & Binder, S. Mapping of mitochondrial mRNA termini in Arabidopsis thaliana: t-elements contribute to 50 and 30 end formation. Nucleic Acids Res. 35, 3676-3692 (2007). (Pubitemid 47244662)
26. Giegé, P. & Brennicke, A. RNA editing in Arabidopsis mitochondria effects 441 C to U changes in ORFs. Proc. Natl Acad. Sci. USA 96, 15324-15329 (1999). (Pubitemid 30019810)
27. Arimura, S. & Tsutsumi, N. A dynamin-like protein (ADL2b), rather than FtsZ, is involved in Arabidopsis mitochondrial division. Proc. Natl Acad. Sci. USA 99, 5727-5731 (2002). (Pubitemid 34411618)
28. Takanashi, H., Arimura, S., Sakamoto, W. & Tsutsumi, N. Different amounts of DNA in each mitochondrion in rice root. Genes Genet. Syst. 81, 215-218 (2006). (Pubitemid 44231995)
29. Oldenburg, D. J., Kumar, R. A. & Bendich, A. J. The amount and integrity of mtDNA in maize decline with development. Planta 237, 603-617 (2013).
30. Chandel, N. S. Mitochondrial complex III: An essential component of universal oxygen sensing machinery? Respir. Physiol. Neurobiol. 174, 175-181 (2010).
31. De Souza, W. et al. Characterization of Rubus fruticosus mitochondria and salicylic acid inhibition of reactive oxygen species generation at Complex III/Q cycle: potential implications for hypersensitive response in plants. J. Bioenerg. Biomemb. 43, 237-246 (2011).
32. Baker, B. M. & Haynes, C. M. Mitochondrial protein quality control during biogenesis and aging. Trends Biochem. Sci. 36, 254-261 (2011).
33. Moreno, A. B. et al. Cytoplasmic and nuclear quality control and turnover of single-stranded RNA modulate post-transcriptional gene silencing in plants. Nucleic Acids Res. 41, 4699-4708 (2013).
34. Holec, S. et al. Relaxed transcription in Arabidopsis Mitochondria is counterbalanced by RNA stability control mediated by polyadenylation and polynucleotide phosphorylase. Mol. Cell Biol. 26, 2869-2876 (2006).
35. Korner, C. G. et al. The deadenylating nuclease (DAN) is involved in poly(A) tail removal during the meiotic maturation of Xenopus oocytes. EMBO J. 17, 5427-5437 (1998). (Pubitemid 28427056)
36. Lejeune, F., Li, X. & Maquat, L. E. Nonsense-mediated mRNA decay in mammalian cells involves decapping, deadenylating, and exonucleolytic activities. Mol. Cell 12, 675-687 (2003). (Pubitemid 37222488)
37. Lee, J. E. et al. The PARN deadenylase targets a discrete set of mRNAs for decay and regulates cell motility in mouse myoblasts. PLoS Genet. 8, e1002901 (2012).
38. Yasuda, M. et al. Antagonistic interaction between systemic acquired resistance and the abscisic acid-mediated abiotic stress response in Arabidopsis. Plant Cell 20, 1678-1692 (2008). (Pubitemid 352844171)
39. Ton, J., Flors, V. & Mauch-Mani, B. The multifaceted role of ABA in disease resistance. Trends Plant Sci. 14, 310-317 (2009).
40. Atkin, O. K. & Macherel, D. The crucial role of plant mitochondria in orchestrating drought tolerance. Ann. Bot. 103, 581-597 (2009).
41. Millar, A. H., Whelan, J., Soole, K. L. & Day, D. A. Organization and regulation of mitochondrial respiration in plants. Annu. Rev. Plant Biol. 62, 79-104 (2011).
42. Alonso, J. M. et al. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301, 653-657 (2003). (Pubitemid 36927950)
43. Yoo, S.-D., Cho, Y.-H. & Sheen, J. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat. Protoc. 2, 1565-1572 (2007). (Pubitemid 47028844)
44. Couttet, P., Fromont-Racine, M., Steel, D., Pictet, R. & Grange, T. Messenger RNA deadenylylation precedes decapping in mammalian cells. Proc. Natl Acad. Sci. USA 94, 5628-5633 (1997). (Pubitemid 27241820)
45. Nagai, T. et al. A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat. Biotechnol. 20, 87-90 (2002). (Pubitemid 34044921)
46. Clough, S. J. & Bent, A. F. Floral dip: a simplified method for Agrobacteriummediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743 (1998).
47. Murota, K. et al. Arabidopsis cell-free extract, ACE, a new in vitro translation system derived from Arabidopsis callus cultures. Plant Cell Physiol. 52, 1443-1453 (2011).