Arabidopsis CSP41 proteins form multimeric complexes that bind and stabilize distinct plastid transcripts

Journal of Experimental Botany

Volumn 63, Issue 3, 2012, Pages 1251-1270

  Qi, Yafei ^a   Armbruster, Ute ^a,e   Schmitz Linneweber, Christian ^b   Delannoy, Etienne ^c   De Longevialle, Andeol Falcon ^c,f   Rühle, Thilo ^a   Small, Ian ^c   Jahns, Peter ^d   Leister, Dario ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b HUMBOLDT UNIVERSITY   (Germany)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^d HEINRICH HEINE UNIVERSITY   (Germany)

^e Institution for Science   (United States)

^f UNIVERSITÉ D EVRY VAL D ESSONNE   (France)

Author keywords

Arabidopsis; chloroplast; gene expression; RNA; RNA binding protein; transcription; translation

Indexed keywords

ARABIDOPSIS PROTEIN; CHLOROPLAST RNA; PLANT RNA;

ARTICLE; CHLOROPLAST; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; PLASTID; PROTEIN MULTIMERIZATION;

ARABIDOPSIS PROTEINS; CHLOROPLASTS; GENE EXPRESSION REGULATION, PLANT; PLASTIDS; PROTEIN MULTIMERIZATION; RNA, CHLOROPLAST; RNA, PLANT;

ARABIDOPSIS; ARABIDOPSIS THALIANA; EUKARYOTA; SPINACIA OLERACEA;

EID: 84856865331     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/err347     Document Type: Article

References (72)

1. Allison LA, Simon LD, Maliga P. 1996. Deletion of rpoB reveals a second distinct transcription system in plastids of higher plants. EMBO Journal 15, 2802-2809.
2. Alonso JM, Stepanova AN, Leisse TJ, et al. 2003. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301, 653-657.
3. Armbruster U, Zühlke J, Rengstl B, et al. 2010. The Arabidopsis thylakoid protein PAM68 is required for efficient D1 biogenesis and photosystem II assembly. The Plant Cell 22, 3439-3460.
4. Baker ME, Grundy WN, Elkan CP. 1998. Spinach CSP41, an mRNA-binding protein and ribonuclease, is homologous to nucleotide-sugar epimerases and hydroxysteroid dehydrogenases. Biochemical and Biophysical Research Communications 248, 250-254.
5. Barkan A, Goldschmidt-Clermont M. 2000. Participation of nuclear genes in chloroplast gene expression. Biochimie 82, 559-572.
6. 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.
7. Berry JO, Breiding DE, Klessig DF. 1990. Light-mediated control of translational initiation of ribulose-1, 5-bisphosphate carboxylase in amaranth cotyledons. The Plant Cell 2, 795-803.
8. 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.
9. Bollenbach TJ, Stern DB. 2003a. Divalent metal-dependent catalysis and cleavage specificity of CSP41, a chloroplast endoribonuclease belonging to the short chain dehydrogenase/reductase superfamily. Nucleic Acids Research 31, 4317-4325.
10. Bollenbach TJ, Stern DB. 2003b. Secondary structures common to chloroplast mRNA 3#-untranslated regions direct cleavage by CSP41, an endoribonuclease belonging to the short chain dehydrogenase/reductase superfamily. Journal of Biological Chemistry 278, 25832-25838.
11. 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.
12. Chateigner-Boutin AL, des Francs-Small CC, Delannoy E, Kahlau S, Tanz SK, de Longevialle AF, Fujii S, Small I. 2011. OTP70 is a pentatricopeptide repeat protein of the E subgroup involved in splicing of the plastid transcript rpoC1. The Plant Journal 65, 532-542.
13. Chateigner-Boutin AL, Ramos-Vega M, Guevara-Garcia A, et al. 2008. CLB19, a pentatricopeptide repeat protein required for editing of rpoA and clpP chloroplast transcripts. The Plant Journal 56, 590-602.
14. Chi W, Ma J, Zhang D, Guo J, Chen F, Lu C, Zhang L. 2008. The pentratricopeptide repeat protein DELAYED GREENING1 is involved in the regulation of early chloroplast development and chloroplast gene expression in Arabidopsis. Plant Physiology 147, 573-584.
15. Choquet Y, Wollman FA. 2002. Translational regulations as specific traits of chloroplast gene expression. FEBS Letters 529, 39-42.
16. Clough SJ, Bent AF. 1998. Floral dipa: simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal 16, 735-743.
17. DalCorso G, Pesaresi P, Masiero S, Aseeva E, Schünemann D, Finazzi G, Joliot P, Barbato R, Leister D. 2008. A complex containing PGRL1 and PGR5 is involved in the switch between linear and cyclic electron flow in Arabidopsis. Cell 132, 273-285.
18. Delannoy E, Le Ret M, Faivre-Nitschke E, Estavillo GM, Bergdoll M, Taylor NL, Pogson BJ, Small I, Imbault P, Gualberto JM. 2009. Arabidopsis tRNA adenosine deaminase arginine edits the wobble nucleotide of chloroplast tRNAArg(ACG) and is essential for efficient chloroplast translation. The Plant Cell 21, 2058-2071.
19. de Longevialle FA, Hendrickson L, Taylor NL, Delannoy E, Lurin C, Badger M, Millar AH, Small I. 2008. The pentatricopeptide repeat gene OTP51 with two LAGLIDADG motifs is required for the cis-splicing of plastid ycf3 intron 2 in Arabidopsis thaliana. The Plant Journal 56, 157-168.
20. Färber A, Young AJ, Ruban AV, Horton P, Jahns P. 1997. Dynamics of xanthophyll-cycle activity in different antenna subcomplexes in the photosynthetic membranes of higher plants (the relationship between zeaxanthin conversion and nonphotochemical fluorescence quenching). Plant Physiology 115, 1609-1618.
21. Fettke J, Nunes-Nesi A, Fernie AR, Steup M. 2011. Identification of a novel heteroglycan-interacting protein, HIP 1.3, from Arabidopsis thaliana. Journal of Plant Physiology 168, 1415-1425.
22. Finkemeier I, Laxa M, Miguet L, Howden AJ, Sweetlove LJ. 2011. Proteins of diverse function and subcellular location are lysine acetylated in Arabidopsis. Plant Physiology 155, 1779-1790.
23. Genty B, Briantais JM, Baker NR. 1989. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990, 87-92.
24. Goulas E, Schubert M, Kieselbach T, Kleczkowski LA, Gardestrom P, Schröder W, Hurry V. 2006. The chloroplast lumen and stromal proteomes of Arabidopsis thaliana show differential sensitivity to short-and long-term exposure to low temperature. The Plant Journal 47, 720-734.
25. Hajdukiewicz PT, Allison LA, Maliga P. 1997. The two RNA polymerases encoded by the nuclear and the plastid compartments transcribe distinct groups of genes in tobacco plastids. EMBO Journal 16, 4041-4048.
26. Hassidim M, Yakir E, Fradkin D, Hilman D, Kron I, Keren N, Harir Y, Yerushalmi S, Green RM. 2007. Mutations in CHLOROPLAST RNA BINDING provide evidence for the involvement of the chloroplast in the regulation of the circadian clock in Arabidopsis. The Plant Journal 51, 551-562.
27. Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, Oertle L, Widmayer P, Gruissem W, Zimmermann P. 2008. Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes. Advances in Bioinformatics 2008, 420747.
28. Ihnatowicz A, Pesaresi P, Varotto C, Richly E, Schneider A, Jahns P, Salamini F, Leister D. 2004. Mutants for photosystem I subunit D of Arabidopsis thaliana: effects on photosynthesis, photosystem I stability and expression of nuclear genes for chloroplast functions. The Plant Journal 37, 839-852.
29. Ishizaki Y, Tsunoyama Y, Hatano K, Ando K, Kato K, Shinmyo A, Kobori M, Takeba G, Nakahira Y, Shiina T. 2005. A nuclear-encoded sigma factor, Arabidopsis SIG6, recognizes sigma-70 type chloroplast promoters and regulates early chloroplast development in cotyledons. The Plant Journal 42, 133-144.
30. Karimi M, Inze D, Depicker A. 2002. GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends in Plant Sciences 7, 193-195.
31. Klaff P, Gruissem W. 1991. Changes in chloroplast mRNA stability during leaf development. The Plant Cell 3, 517-529.
32. Klein RR, Mason HS, Mullet JE. 1988. Light-regulated translation of chloroplast proteins. I. Transcripts of psaA-psaB, psbA, and rbcL are associated with polysomes in dark-grown and illuminated barley seedlings. Journal of Cell Biology 106, 289-301.
33. Kunst L. 1998. Preparation of physiologically active chloroplasts from Arabidopsis. Methods in Molecular Biology 82, 43-48.
34. Leister D, Varotto C, Pesaresi P, Niwergall A, Salamini F. 1999. Large-scale evaluation of plant growth in Arabidopsis thaliana by non-invasive image analysis. Plant Physiology and Biochemistry 37, 671-678.
35. Li Y, Rosso MG, Strizhov N, Viehoever P, Weisshaar B. 2003. GABI-Kat SimpleSearch: a flanking sequence tag (FST) database for the identification of T-DNA insertion mutants in Arabidopsis thaliana. Bioinformatics 19, 1441-1442.
36. Liere K, Kaden D, Maliga P, Börner T. 2004. Overexpression of phage-type RNA polymerase RpoTp in tobacco demonstrates its role in chloroplast transcription by recognizing a distinct promoter type. Nucleic Acids Research 32, 1159-1165.
37. Lohrig K, Müller B, Davydova J, Leister D, Wolters DA. 2009. Phosphorylation site mapping of soluble proteins: bioinformatical filtering reveals potential plastidic phosphoproteins in Arabidopsis thaliana. Planta 229, 1123-1134.
38. Manuell A, Beligni MV, Yamaguchi K, Mayfield SP. 2004. Regulation of chloroplast translation: interactions of RNA elements, RNA-binding proteins and the plastid ribosome. Biochemical Society Transactions 32, 601-605.
39. Marchand C, Le Marechal P, Meyer Y, Decottignies P. 2006. Comparative proteomic approaches for the isolation of proteins interacting with thioredoxin. Proteomics 6, 6528-6537.
40. Marin-Navarro J, Manuell AL, Wu J, Mayfield SP. 2007. Chloroplast translation regulation. Photosynthesis Research 94, 359-374.
41. Marques JP, Schattat MH, Hause G, Dudeck I, Klosgen RB. 2004. In vivo transport of folded EGFP by the DpH/TAT-dependent pathway in chloroplasts of Arabidopsis thaliana. Journal of Experimental Botany 55, 1697-1706.
42. Martinez-Garcia JF, Monte E, Quail PH. 1999. A simple, rapid and quantitative method for preparing Arabidopsis protein extracts for immunoblot analysis. The Plant Journal 20, 251-257.
43. Okuda K, Myouga F, Motohashi R, Shinozaki K, Shikanai T. 2007. Conserved domain structure of pentatricopeptide repeat proteins involved in chloroplast RNA editing. Proceedings of the National Academy of Sciences, USA 104, 8178-8183.
44. Olinares PD, Ponnola 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.
45. Peltier JB, Cai Y, Sun Q, Zabrouskov V, Giacomelli L, Rudella A, Ytterberg AJ, Rutschow H, van Wijk KJ. 2006. The oligomeric stromal proteome of Arabidopsis thaliana chloroplasts. Molecular and Cellular Proteomics 5, 114-133.
46. Pesaresi P, Varotto C, Meurer J, Jahns P, Salamini F, Leister D. 2001. Knock-out of the plastid ribosomal protein L11 in Arabidopsis: effects on mRNA translation and photosynthesis. The Plant Journal 27, 179-189.
47. 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. EMBO Journal 28, 2042-2052.
48. Pfalz J, Liere K, Kandlbinder A, Dietz KJ, Oelmüller R. 2006. pTAC2,-6, and-12 are components of the transcriptionally active plastid chromosome that are required for plastid gene expression. The Plant Cell 18, 176-197.
49. Pfannschmidt T, Ogrzewalla K, Baginsky S, Sickmann A, Meyer HE, Link G. 2000. The multisubunit chloroplast RNA polymerase A from mustard (Sinapis alba L.). Integration of a prokaryotic core into a larger complex with organelle-specific functions. European Journal of Biochemistry 267, 253-261.
50. Prikryl J, Watkins KP, Friso G, van Wijk KJ, Barkan A. 2008. A member of the Whirly family is a multifunctional RNA-and DNA-binding protein that is essential for chloroplast biogenesis. Nucleic Acids Research 36, 5152-5165.
51. Raab S, Toth Z, de Groot C, Stamminger T, Hoth S. 2006. ABA-responsive RNA-binding proteins are involved in chloroplast and stromule function in Arabidopsis seedlings. Planta 224, 900-914.
52. Reiland S, Finazzi G, Endler A, et al. 2011. Comparative phosphoproteome profiling reveals a function of the STN8 kinase in fine-tuning of cyclic electron flow (CEF). Proceedings of the National Academy of Sciences, USA 108, 12955-12960.
53. Reiland S, Messerli G, Baerenfaller K, Gerrits B, Endler A, Grossmann J, Gruissem W, Baginsky S. 2009. Large-scale Arabidopsis phosphoproteome profiling reveals novel chloroplast kinase substrates and phosphorylation networks. Plant Physiology 150, 889-903.
54. Rios G, Lossow A, Hertel B, et al. 2002. Rapid identification of Arabidopsis insertion mutants by non-radioactive detection of T-DNA tagged genes. The Plant Journal 32, 243-253.
55. Sambrook J, Russell DW. 2001. Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
56. Schägger H, von Jagow G. 1987. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Analytical Biochemistry 166, 368-379.
57. Schägger H, von Jagow G. 1991. Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Analytical Biochemistry 199, 223-231.
58. Schmitz-Linneweber C, Williams-Carrier R, Barkan A. 2005. RNA immunoprecipitation and microarray analysis show a chloroplast pentatricopeptide repeat protein to be associated with the 5# region of mRNAs whose translation it activates. The Plant Cell 17, 2791-2804.
59. Schweer J, Loschelder H, Link G. 2006. A promoter switch that can rescue a plant sigma factor mutant. FEBS Letters 580, 6617-6622.
60. Ströher E, Dietz KJ. 2008. The dynamic thiol-disulphide redox proteome of the Arabidopsis thaliana chloroplast as revealed by differential electrophoretic mobility. Physiologica Plantarum 133, 566-583.
61. Sturn A, Quackenbush J, Trajanoski Z. 2002. Genesis: cluster analysis of microarray data. Bioinformatics 18, 207-208.
62. Sun Q, Zybailov B, Majeran W, Friso G, Olinares PD, van Wijk KJ. 2009. PPDB, the Plant Proteomics Database at Cornell. Nucleic Acids Research 37, D969-D974.
63. Suzuki JY, Ytterberg AJ, Beardslee TA, Allison LA, Wijk KJ, Maliga P. 2004. Affinity purification of the tobacco plastid RNA polymerase and in vitro reconstitution of the holoenzyme. The Plant Journal 40, 164-172.
64. Tillich M, Hardel SL, Kupsch C, Armbruster U, Delannoy E, Gualberto JM, Lehwark P, Leister D, Small ID, Schmitz-Linneweber C. 2009. Chloroplast ribonucleoprotein CP31A is required for editing and stability of specific chloroplast mRNAs. Proceedings of the National Academy of Sciences, USA 106, 6002-6007.
65. Wolfe KH, Morden CW, Palmer JD. 1991. Ins and outs of plastid genome evolution. Current Opinion in Genetics and Development 1, 523-529.
66. Yamaguchi K, Beligni MV, Prieto S, Haynes PA, McDonald WH, Yates 3rd JR, Mayfield SP. 2003. Proteomic characterization of the Chlamydomonas reinhardtii chloroplast ribosome. Identification of proteins unique to the 70S ribosome. Journal of Biological Chemistry 278, 33774-33785.
67. Yang J, Schuster G, Stern DB. 1996. CSP41, a sequence-specific chloroplast mRNA binding protein, is an endoribonuclease. The Plant Cell 8, 1409-1420.
68. Yang J, Stern DB. 1997. The spinach chloroplast endoribonuclease CSP41 cleaves the 3#-untranslated region of petD mRNA primarily within its terminal stem-loop structure. Journal of Biological Chemistry 272, 12874-12880.
69. Yang J, Usack L, Monde RA, Stern DB. 1995. The 41 kDa protein component of the spinach chloroplast petD mRNA 3# stem-loop:protein complex is a nuclear encoded chloroplast RNA-binding protein. Nucleic Acids Symposium Series 33, 237-239.
70. Yohn CB, Cohen A, Danon A, Mayfield SP. 1996. Altered mRNA binding activity and decreased translational initiation in a nuclear mutant lacking translation of the chloroplast psbA mRNA. Molecular and Cellular Biology 16, 3560-3566.
71. Zerges W. 2000. Translation in chloroplasts. Biochimie 82, 583-601.
72. Zoschke R, Liere K, Börner T. 2007. From seedling to mature plant: Arabidopsis plastidial genome copy number, RNA accumulation and transcription are differentially regulated during leaf development. The Plant Journal 50, 710-722.