The cutting crew-ribonucleases are key players in the control of plastid gene expression

Journal of Experimental Botany

Volumn 63, Issue 4, 2012, Pages 1663-1673

  Stoppel, Rhea ^a   Meurer, Jörg ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

Chloroplast RNA metabolism; ribonucleases; rRNA processing

Indexed keywords

CHLOROPLAST RNA; RIBONUCLEASE; RIBOSOME RNA;

ARABIDOPSIS; CHLOROPLAST; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PLASTID; REVIEW; RNA STABILITY;

ARABIDOPSIS; CHLOROPLASTS; GENE EXPRESSION REGULATION, PLANT; PLASTIDS; RIBONUCLEASES; RNA STABILITY; RNA, CHLOROPLAST; RNA, RIBOSOMAL;

ARABIDOPSIS; BACTERIA (MICROORGANISMS); EMBRYOPHYTA; EUKARYOTA;

EID: 84857990796     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/err401     Document Type: Review

References (93)

1. Arraiano CM, Andrade JM, Domingues S, et al. 2010. The critical role of RNA processing and degradation in the control of gene expression. FEMS Microbiology Reviews 34, 883-923.
2. Altman S, Gopalan V, Vioque A. 2000. Varieties of RNase P: a nomenclature problem? RNA 6, 1689-1694. (Pubitemid 32001939)
3. Awano N, Inouye M, Phadtare S. 2008. RNase activity of polynucleotide phosphorylase is critical at low temperature in Escherichia coli and is complemented by RNase II. Journal of Bacteriology 190, 5924-5933.
4. Babitzke P, Granger L, Olszewski J, Kushner SR. 1993. Analysis of mRNA decay and rRNA processing in Escherichia coli multiple mutants carrying a deletion in RNase III. Journal of Bacteriology 175, 229-239. (Pubitemid 23016671)
5. Baginsky S, Shteiman-Kotler A, Liveanu V, Yehudai-Resheff S, Bellaoui M, Settlage RE, Shabanowitz J, Hunt DF, Schuster G, Gruissem W. 2001. Chloroplast PNPase exists as a homo-multimer enzyme complex that is distinct from the Escherichia coli degradosome. RNA 7, 1464-1475. (Pubitemid 32973232)
6. Baker ME, Grundy WN, Elkan CP. 1998. Spinach CSP41, an mRNA-binding protein and ribonuclease, is homologous to nucleotidesugar epimerases and hydroxysteroid dehydrogenases. Biochemical and Biophysical Research Communications 248, 250-254. (Pubitemid 28386408)
7. Barkan A. 2011. Expression of plastid genes: organelle-specific elaborations on a prokaryotic scaffold. Plant Physiology 155, 1520-1532.
8. Bellaoui M, Keddie JS, Gruissem W. 2003. DCL is a plant-specific protein required for plastid ribosomal RNA processing and embryo development. Plant Molecular Biology 53, 531-543. (Pubitemid 38345345)
9. Beligni MV, Mayfield SP. 2008. Arabidopsis thaliana mutants reveal a role for CSP41a and CSP41b, two ribosome-associated endonucleases, in chloroplast ribosomal RNA metabolism. Plant Molecular Biology 67, 389-401.
10. Bernstein JA, Khodursky AB, Lin PH, Lin-Chao S, Cohen SN. 2002. Global analysis of mRNA decay and abundance in Escherichia coli at single-gene resolution using two-color fluorescent DNA microarrays. Proceedings of the National Academy of Sciences USA 99, 9697-9702. (Pubitemid 34831110)
11. Betat H, Rammelt C, Mörl M. 2010. tRNA nucleotidyltransferases: ancient catalysts with an unusual mechanism of polymerization. Cellular and Molecular Life Sciences 67, 1447-1463.
12. Bisanz C, Bégot L, Carol P, Perez P, Bligny M, Pesey H, Gallois JL, Lerbs-Mache S, 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 Molecular Biology 51, 651-663. (Pubitemid 36386299)
13. Blum E, Carpousis AJ, Higgins CF. 1999. Polyadenylation promotes degradation of 3'-structured RNA by the Escherichia coli mRNA degradosome in vitro. Journal of Biological Chemistry 274, 4009-4016.
14. Bollenbach TJ, Lange H, Gutierrez R, Erhardt M, Stern DB, 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 Research 33, 2751-2763. (Pubitemid 41511293)
15. Bollenbach TJ, Schuster G, Portnoy V, Stern D. 2007. Polyadenylation, processing and degradation of chloroplast RNA. Topics in Current Genetics 19, 175-211.
16. Bollenbach TJ, Sharwood RE, Gutierrez R, Lerbs-Mache S, Stern DB. 2009. The RNA-binding proteins CSP41a and CSP41b may regulate transcription and translation of chloroplast-encoded RNAs in Arabidopsis. Plant Molecular Biology 69, 541-552.
17. Bollenbach TJ, Tatman DA, Stern DB. 2003. CSP41a, a multifunctional RNA-binding protein, initiates mRNA turnover in tobacco chloroplasts. The Plant Journal 36, 842-852. (Pubitemid 38069771)
18. Canino G, Bocian E, Barbezier N, Echeverría M, Forner J, Binder S, Marchfelder A. 2009. Arabidopsis encodes four tRNase Z enzymes. Plant Physiology 150, 1494-1502.
19. Carpousis AJ. 2007. The RNA degradosome of Escherichia coli: an mRNA-degrading machine assembled on RNase E. Annual Reviews of Microbiology 61, 71-87. (Pubitemid 350058200)
20. Cerritelli SM, Crouch RJ. 2009. Ribonuclease H: the enzymes in eukaryotes. FEBS Journal 276, 1494-1505.
21. Chekanova JA, Shaw RJ, Wills MA, Belostotsky DA. 2000. Poly(A) tail-dependent exonuclease AtRrp41p from Arabidopsis thaliana rescues 5.8 S rRNA processing and mRNA decay defects of the yeast ski6 mutant and is found in an exosome-sized complex in plant and yeast cells. Journal of Biological Chemistry 275, 33158-33166.
22. Cheng ZF, Deutscher MP. 2003. Quality control of ribosomal RNA mediated by polynucleotide phosphorylase and RNase R. Proceedings of the National Academy of Sciences USA 100, 6388-6393. (Pubitemid 36666591)
23. Cho WK, Geimer S, Meurer J. 2009. Cluster analysis and comparison of various chloroplast transcriptomes and genes in Arabidopsis thaliana. DNA Research 16, 31-44.
24. Coburn GA, Mackie GA. 1996. Overexpression, purification, and properties of Escherichia coli ribonuclease II. Journal of Biological Chemistry 271, 1048-1053. (Pubitemid 26034964)
25. Cohen SN, McDowall KJ. 1997. RNase E: still a wonderfully mysterious enzyme. Molecular Microbiology 23, 1099-1106. (Pubitemid 27122196)
26. Comella P, Pontvianne F, Lahmy S, Vignols F, Barbezier N, Debures A, Jobet E, Brugidou E, Echeverria M, Sáez-Vásquez J. 2008. Characterization of a ribonuclease III-like protein required for cleavage of the pre-rRNA in the 3'ETS in Arabidopsis. Nucleic Acids Research 36, 1163-1175. (Pubitemid 351330934)
27. Condon C, Putzer H. 2002. The phylogenetic distribution of bacterial ribonucleases. Nucleic Acids Research 30, 5339-5346. (Pubitemid 36113910)
28. Davies BW, Köhrer C, Jacob AI, Simmons LA, Zhu J, Aleman LM, Rajbhandary UL, Walker GC. 2010. Role of Escherichia coli YbeY, a highly conserved protein, in rRNA processing. Molecular Microbiology 78, 506-518.
29. De la Cruz J, Vioque A. 2003. A structural and functional study of plastid RNAs homologous to catalytic bacterial RNase P RNA. Gene 321, 47-56. (Pubitemid 37421394)
30. Deutscher MP. 1973. Synthesis and functions of the-C-C-A terminus of transfer RNA. Progress in Nucleic Acid Research and Molecular Biology 13, 51-92.
31. Even S, Pellegrini O, Zig L, Labas V, Vinh J, Bréchemmier-Baey D, Putzer H. 2005. Ribonucleases J1 and J2: two novel endoribonucleases in B. subtilis with functional homology to E. coli RNase E. Nucleic Acids Research 33, 2141-2152. (Pubitemid 41439882)
32. Evguenieva-Hackenberg E. 2005. Bacterial ribosomal RNA in pieces. Molecular Microbiology 57, 318-325. (Pubitemid 40979335)
33. Gegenheimer P, Apirion D. 1975. Escherichia coli ribosomal ribonucleic acids are not cut from an intact precursor molecule. Journal of Biological Chemistry 250, 2407-2409.
34. Gegenheimer P, Apirion D. 1981. Processing of procaryotic ribonucleic acid. Microbiology Reviews 45, 502-541. (Pubitemid 12185806)
35. Germain A, Herlich S, Larom S, Kim SH, Schuster G, Stern DB. 2011. Mutational analysis of Arabidopsis chloroplast polynucleotide phosphorylase reveals roles for both RNase PH core domains in polyadenylation, RNA 3'-end maturation and intron degradation. The Plant Journal 67, 381-394.
36. Gobert A, Gutmann B, Taschner A, Gössringer M, Holzmann J, Hartmann RK, Rossmanith W, GiegéP. 2010. A single Arabidopsis organellar protein has RNase P activity. Nature Structural and Molecular Biology 17, 740-744.
37. Haeusler RA, Engelke DR. 2006. Spatial organization of transcription by RNA polymerase III. Nucleic Acids Research 34, 4826-4836. (Pubitemid 44607803)
38. Harris EH, Boynton JE, Gillham NW. 1994. Chloroplast ribosomes and protein synthesis. Microbiology Reviews 58, 700-754.
39. Hashimoto M, Endo T, Peltier G, Tasaka M, Shikanai T. 2003. A nucleus-encoded factor, CRR2, is essential for the expression of chloroplast ndhB in Arabidopsis. The Plant Journal 36, 541-549. (Pubitemid 37457941)
40. Holzmann J, Frank P, Löffler E, Bennett KL, Gerner C, Rossmanith W. 2008. RNase P without RNA: identification and functional reconstitution of the human mitochondrial tRNA processing enzyme. Cell 135, 462-474.
41. Kaberdin VR, Miczak A, Jakobsen JS, Lin-Chao S, McDowall KJ, von Gabain A. 1998. The endoribonucleolytic Nterminal half of Escherichia coli RNase E is evolutionarily conserved in Synechocystis sp. and other bacteria but not the C-terminal half, which is sufficient for degradosome assembly. Proceedings of the National Academy of Sciences USA 95, 11637-11642.
42. Kishine M, Takabayashi A, Munekage Y, Shikanai T, Endo T, Sato F. 2004. Ribosomal RNA processing and an RNase R family member in chloroplasts of Arabidopsis. Plant Molecular Biology 55, 595-606. (Pubitemid 40653987)
43. Klaff P, Gruissem W. 1991. Changes in chloroplast mRNA stability during leaf development. The Plant Cell 3, 517-529. (Pubitemid 21913717)
44. Komatsu T, Kawaide H, Saito C, et al. 2010. The chloroplast protein BPG2 functions in brassinosteroid-mediated post-transcriptional accumulation of chloroplast rRNA. The Plant Journal 61, 409-422.
45. Lamontagne B, Larose S, Boulanger J, Elela SA. 2001. The RNase III family: a conserved structure and expanding functions in eukaryotic dsRNA metabolism. Current Issues in Molecular Biology 3, 71-78. (Pubitemid 33061770)
46. Leal-Klevezas DS, Martínez-Soriano JP, Nazar RN. 2000. Cotranscription of 5S rRNA-tRNA(Arg)(ACG) from Brassica napus chloroplasts and processing of their intergenic spacer. Gene 253, 303-311. (Pubitemid 30625221)
47. Leaver CJ. 1973. Molecular integrity of chloroplast ribosomal ribonucleic acid. Biochemical Journal 135, 237-240.
48. Lezhneva L, Meurer J. 2004. The nuclear factor HCF145 affects chloroplast psaA-psaB-rps14 transcript abundance in Arabidopsis thaliana. The Plant Journal 38, 740-753. (Pubitemid 38693454)
49. Lisitsky I, Schuster G. 1999. Preferential degradation of polyadenylated and polyuridinylated RNAs by the bacterial exoribonuclease polynucleotide phosphorylase. European Journal of Biochemistry 261, 468-474. (Pubitemid 29187493)
50. Long EO, Dawid IB. 1980. Repeated genes in eukaryotes. Annual Reviews of Biochemistry 49, 727-764.
51. Lu Y, Li C, Wang H, Chen H, Berg H, Xia Y. 2011. AtPPR2, an Arabidopsis pentatricopeptide repeat protein, binds to plastid 23S rRNA and plays an important role in the first mitotic division during gametogenesis and in cell proliferation during embryogenesis. The Plant Journal 67, 13-25.
52. Marchive C, Yehudai-Resheff S, Germain A, Fei Z, Jiang X, Judkins J, Wu H, Fernie AR, Fait A, Stern DB. 2009. Abnormal physiological and molecular mutant phenotypes link chloroplast polynucleotide phosphorylase to the phosphorus deprivation response in Arabidopsis. Plant Physiology 151, 905-924.
53. Mathy N, Bénard L, Pellegrini O, Daou R, Wen T, Condon C. 2007. 5'-to-3' exoribonuclease activity in bacteria: role of RNase J1 in rRNA maturation and 5' stability of mRNA. Cell 129, 681-692. (Pubitemid 46802375)
54. Meierhoff K, Felder S, Nakamura T, Bechtold N, Schuster G. 2003. HCF152, an Arabidopsis RNA binding pentatricopeptide repeat protein involved in the processing of chloroplast psbB-psbT-psbHpetB-petD RNAs. The Plant Cell 15, 1480-1495. (Pubitemid 36715187)
55. Meurer J, Lezhneva L, Amann K, Gödel M, Bezhani S, Sherameti I, Oelmüller R. 2002. A peptide chain release factor 2 affects the stability of UGA-containing transcripts in Arabidopsis chloroplasts. The Plant Cell 14, 3255-3269. (Pubitemid 36029145)
56. Mohanty BK, Kushner SR. 2007. Ribonuclease P processes polycistronic tRNA transcripts in Escherichia coli independent of ribonuclease E. Nucleic Acids Research 35, 7614-7625.
57. Monde RA, Schuster G, Stern DB. 2000. Processing and degradation of chloroplast mRNA. Biochimie 82, 573-582. (Pubitemid 30608453)
58. Morishita R, Kawagoshi A, Sawasaki T, Madin K, Ogasawara T, Oka T, Endo Y. 1999. Ribonuclease activity of rat liver perchloric acid-soluble protein, a potent inhibitor of protein synthesis. Journal of Biological Chemistry 274, 20688-20692.
59. Mörl M, Marchfelder A. 2001. The final cut. The importance of tRNA 3'-processing. EMBO Reports 2, 17-20. (Pubitemid 32229716)
60. Mudd EA, Sullivan S, Gisby MF, Mironov A, Kwon CS, Chung WI, Day A. 2008. A 125 kDa RNase E/G-like protein is present in plastids and is essential for chloroplast development and autotrophic growth in Arabidopsis. Journal of Experimental Botany 59, 2597-2610. (Pubitemid 351957487)
61. Nishimura K, Ashida H, Ogawa T, Yokota A. 2010. A DEAD box protein is required for formation of a hidden break in Arabidopsis chloroplast 23S rRNA. The Plant Journal 63, 766-777.
62. Nissen P, Hansen J, Ban N, Moore PB, Steitz TA. 2000. The structural basis of ribosome activity in peptide bond synthesis. Science 289, 920-930. (Pubitemid 30659940)
63. Ohtani N, Haruki M, Morikawa M, Kanaya S. 1999. Molecular diversities of RNases H. Journal of Bioscience and Bioengineering 88, 12-19. (Pubitemid 29394993)
64. Okuda K, Chateigner-Boutin AL, Nakamura T, Delannoy E, Sugita M, Myouga F, Motohashi R, Shinozaki K, Small I, Shikanai T. 2009. Pentatricopeptide repeat proteins with the DYW motif have distinct molecular functions in RNA editing and RNA cleavage in Arabidopsis chloroplasts. The Plant Cell 21, 146-156.
65. Olinares PD, Ponnala L, van Wijk KJ. 2010. Megadalton complexes in the chloroplast stroma of Arabidopsis thaliana characterized by size exclusion chromatography, mass spectrometry, and hierarchical clustering. Molecular and Cellular Proteomics 9, 1594-1615.
66. Pellegrini O, Nezzar J, Marchfelder A, Putzer H, Condon C. 2003. Endonucleolytic processing of CCA-less tRNA precursors by RNase Z in Bacillus subtilis. The EMBO Journal 22, 4534-4543. (Pubitemid 37087206)
67. Perrin R, Meyer EH, Zaepfel M, Kim YJ, Mache R, Grienenberger JM, Gualberto JM, Gagliardi D. 2004. Two exoribonucleases act sequentially to process mature 3'-ends of atp9 mRNAs in Arabidopsis mitochondria. Journal of Biological Chemistry 279, 25440-25446. (Pubitemid 38756801)
68. Pfalz J, Bayraktar OA, Prikryl J, Barkan A. 2009. Site-specific binding of a PPR protein defines and stabilizes 5' and 3' mRNA termini in chloroplasts. The EMBO Journal 28, 2042-2052.
69. Prikryl J, Rojas M, Schuster G, Barkan A. 2011. Mechanism of RNA stabilization and translational activation by a pentatricopeptide repeat protein. Proceedings of the National Academy of Sciences USA 108, 415-420.
70. Qi Y, Armbruster U, Schmitz-Linneweber C, Delannoy E, de Longevialle AF, Rühle T, Small I, Jahns P, Leister D. 2011. Arabidopsis CSP41 proteins form multimeric complexes that bind and stabilize distinct plastid transcripts. Journal of Experimental Botany 63, 1251-1270.
71. Richly E, Leister D. 2004. An improved prediction of chloroplast proteins reveals diversities and commonalities in the chloroplast proteomes of Arabidopsis and rice. Gene 329, 11-16. (Pubitemid 38366490)
72. Robbins JC, Heller WP, Hanson MR. 2009. A comparative genomics approach identifies a PPR-DYW protein that is essential for C-to-U editing of the Arabidopsis chloroplast accD transcript. RNA 15, 1142-1153.
73. Robertson HD, Webster RE, Zinder ND. 1968. Purification and properties of ribonuclease III from Escherichia coli. Journal of Biological Chemistry 243, 82-91.
74. Rott R, Zipor G, Portnoy V, Liveanu V, Schuster G. 2003. RNA polyadenylation and degradation in cyanobacteria are similar to the chloroplast but different from Escherichia coli. Journal of Biological Chemistry 278, 15771-15777. (Pubitemid 36799690)
75. Salone V, Rüdinger M, Polsakiewicz M, Hoffmann B, Groth-Malonek M, Szurek B, Small I, Knoop V, Lurin C. 2007. A hypothesis on the identification of the editing enzyme in plant organelles. FEBS Letters 581, 4132-4138. (Pubitemid 47301862)
76. Salvador ML, Suay L, Klein U. 2011. Messenger RNA degradation is initiated at the 5' end and follows sequence-and condition-dependent modes in chloroplasts. Nucleic Acids Research 39, 6213-6222.
77. Schein A, Sheffy-Levin S, Glaser F, Schuster G. 2008. The RNase E/G-type endoribonuclease of higher plants is located in the chloroplast and cleaves RNA similarly to the E. coli enzyme. RNA 14, 1057-1068. (Pubitemid 351717487)
78. Schmid M, Jensen TH. 2008. The exosome: a multipurpose RNA-decay machine. Trends in Biochemical Science 33, 501-510.
79. Schuster G, Stern D. 2009. RNA polyadenylation and decay in mitochondria and chloroplasts. Progress in Molecular Biology and Translational Science 85, 393-422.
80. Sharwood RE, Hotto AM, Bollenbach TJ, Stern DB. 2011. Overaccumulation of the chloroplast antisense RNA AS5 is correlated with decreased abundance of 5S rRNA in vivo and inefficient 5S rRNA maturation in vitro. RNA 17, 230-243.
81. Stoppel R, Lezhneva L, Schwenkert S, Torabi S, Felder S, Meierhoff K, Westhoff P, Meurer J. 2011. Recruitment of a ribosomal release factor for light-and stress-dependent regulation of petB transcript stability in Arabidopsis chloroplasts. The Plant Cell 23, 2680-2695.
82. Strittmatter G, Kössel H. 1984. Cotranscription and processing of 23S, 4.5S and 5S rRNA in chloroplasts from Zea mays. Nucleic Acids Research 12, 7633-7647.
83. Thomas BC, Li X, Gegenheimer P. 2000. Chloroplast ribonuclease P does not utilize the ribozyme-type pre-tRNA cleavage mechanism. RNA 6, 545-553. (Pubitemid 30212232)
84. Walter M, Kilian J, Kudla J. 2002. PNPase activity determines the efficiency of mRNA 3'-end processing, the degradation of tRNA and the extent of polyadenylation in chloroplasts. The EMBO Journal 21, 6905-6914. (Pubitemid 36014562)
85. Walter M, Piepenburg K, Schöttler MA, Petersen K, Kahlau S, Tiller N, Drechsel O, Weingartner M, Kudla J, Bock R. 2010. Knockout of the plastid RNase E leads to defective RNA processing and chloroplast ribosome deficiency. The Plant Journal 64, 851-863.
86. Watkins KP, Kroeger TS, Cooke AM, Williams-Carrier RE, Friso G, Belcher SE, van Wijk KJ, Barkan A. 2007. A ribonuclease III domain protein functions in group II intron splicing in maize chloroplasts. The Plant Cell 19, 2606-2623. (Pubitemid 47583848)
87. Yamaguchi K, Subramanian AR. 2000. The plastid ribosomal proteins. Identification of all the proteins in the 50 S subunit of an organelle ribosome (chloroplast). Journal of Biological Chemistry 275, 28466-28482.
88. Yamaguchi K, von Knoblauch K, Subramanian AR. 2000. The plastid ribosomal proteins. Identification of all the proteins in the 30 S subunit of an organelle ribosome (chloroplast). Journal of Biological Chemistry 275, 28455-28465.
89. Yang J, Schuster G, Stern DB. 1996. CSP41, a sequence-specific chloroplast mRNA binding protein, is an endoribonuclease. The Plant Cell 8, 1409-1420. (Pubitemid 26351947)
90. Yehudai-Resheff S, Hirsh M, Schuster G. 2001. Polynucleotide phosphorylase functions as both an exonuclease and a poly(A) polymerase in spinach chloroplasts. Molecular and Cellular Biology 21, 5408-5416. (Pubitemid 32702445)
91. Yehudai-Resheff S, Portnoy V, Yogev S, Adir N, Schuster G. 2003. Domain analysis of the chloroplast polynucleotide phosphorylase reveals discrete functions in RNA degradation, polyadenylation, and sequence homology with exosome proteins. The Plant Cell 15, 2003-2019. (Pubitemid 37144057)
92. Yu D, Deutscher MP. 1995. Oligoribonuclease is distinct from the other known exoribonucleases of Escherichia coli. Journal of Bacteriology 177, 4137-4139.
93. Zybailov B, Rutschow H, Friso G, Rudella A, Emanuelsson O, Sun Q, van Wijk KJ. 2008. Sorting signals, N-terminal modifications and abundance of the chloroplast proteome. PLoS One 3, e1994.