Mutation of the pentatricopeptide repeat-SMR protein SVR7 impairs accumulation and translation of chloroplast ATP synthase subunits in Arabidopsis thaliana

Journal of Plant Research

Volumn 126, Issue 3, 2013, Pages 403-414

  Zoschke, Reimo ^a,b   Qu, Yujiao ^a   Zubo, Yan O ^a,c   Börner, Thomas ^a   Schmitz Linneweber, Christian ^a  

^a HUMBOLDT UNIVERSITY   (Germany)

^b UNIVERSITY OF OREGON   (United States)

^c Dartmouth College   (United States)

Author keywords

Arabidopsis; Chloroplast; Gene expression; Pentatricopeptide repeat (PPR) protein; SMR domain; Translation

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; EMBRYOPHYTA; ZEA MAYS;

EID: 84876670588     PISSN: 09189440     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10265-012-0527-1     Document Type: Article

References (64)

1. Asakura Y, Barkan A (2006) Arabidopsis orthologs of maize chloroplast splicing factors promote splicing of orthologous and species-specific group II introns. Plant Physiol 142: 1656-1663.
2. Asakura Y, Barkan A (2007) A CRM domain protein functions dually in group I and group II intron splicing in land plant chloroplasts. Plant Cell 19: 3864-3875.
3. Asakura Y, Bayraktar OA, Barkan A (2008) Two CRM protein subfamilies cooperate in the splicing of group IIB introns in chloroplasts. RNA 14: 2319-2332.
4. Barkan A (1993) Nuclear mutants of maize with defects in chloroplast polysome assembly have altered chloroplast RNA metabolism. Plant Cell 5: 389-402.
5. Barkan A (1998) Approaches to investigating nuclear genes that function in chloroplast biogenesis in land plants. Methods Enzymol 297: 38-57.
6. Barkan A (2011) Expression of plastid genes: organelle-specific elaborations on a prokaryotic scaffold. Plant Physiol 155: 1520-1532.
7. Barkan A, Walker M, Nolasco M, Johnson D (1994) A nuclear mutation in maize blocks the processing and translation of several chloroplast mRNAs and provides evidence for the differential translation of alternative mRNA forms. EMBO J 13: 3170-3181.
8. Beick S, Schmitz-Linneweber C, Williams-Carrier R, Jensen B, Barkan A (2008) The pentatricopeptide repeat protein PPR5 stabilizes a specific tRNA precursor in maize chloroplasts. Mol Cell Biol 28: 5337-5347.
9. Bock R, Timmis JN (2008) Reconstructing evolution: gene transfer from plastids to the nucleus. BioEssays 30: 556-566.
10. Boulouis A, Raynaud C, Bujaldon S, Aznar A, Wollman FA, Choquet Y (2011) The nucleus-encoded trans-acting factor MCA1 plays a critical role in the regulation of cytochrome f synthesis in Chlamydomonas chloroplasts. Plant Cell 23: 333-349.
11. Cai W, Okuda K, Peng L, Shikanai T (2011) PROTON GRADIENT REGULATION 3 recognizes multiple targets with limited similarity and mediates translation and RNA stabilization in plastids. Plant J 67: 318-327.
12. Cushing DA, Forsthoefel NR, Gestaut DR, Vernon DM (2005) Arabidopsis emb175 and other ppr knockout mutants reveal essential roles for pentatricopeptide repeat (PPR) proteins in plant embryogenesis. Planta 221: 424-436.
13. de Longevialle AF, 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. Plant J 56: 157-168.
14. Delannoy E, Stanley WA, Bond CS, Small ID (2007) Pentatricopeptide repeat (PPR) proteins as sequence-specificity factors in post-transcriptional processes in organelles. Biochem Soc Trans 35: 1643-1647.
15. Echeverria M, Lahmy S (1995) Identification of a 67 kDa protein that binds specifically to the pre-rRNA primary processing site in a higher plant. Nucleic Acids Res 23: 4963-4970.
16. Fukui K, Kuramitsu S (2011) Structure and function of the small MutS-related domain. Mol Biol Int 2011: 691735.
17. Gillman JD, Bentolila S, Hanson MR (2007) The petunia restorer of fertility protein is part of a large mitochondrial complex that interacts with transcripts of the CMS-associated locus. Plant J 49: 217-227.
18. Hammani K, des Francs-Small cc, Takenaka M, Tanz SK, Okuda k, Shikanai T, Brennicke A, Small I (2011) The pentatricopeptide repeat protein OTP87 is essential for RNA editing of nad7 and atp1 transcripts in Arabidopsis mitochondria. J Biol Chem 286: 21361-21371.
19. Hattori M, Miyake H, Sugita M (2007) A pentatricopeptide repeat protein is required for RNA processing of clpP pre-mRNA in moss chloroplasts. J Biol Chem 282: 10773-10782.
20. Kleine T, Maier UG, Leister D (2009) DNA transfer from organelles to the nucleus: the idiosyncratic genetics of endosymbiosis. Annu Rev Plant Biol 60: 115-138.
21. Koussevitzky S, Nott A, Mockler TC, Hong F, Sachetto-Martins G, Surpin M, Lim J, Mittler R, Chory J (2007) Signals from chloroplasts converge to regulate nuclear gene expression. Science 316: 715-719.
22. Lahmy S, Barneche F, Derancourt J, Filipowicz W, Delseny M, Echeverria M (2000) A chloroplastic RNA-binding protein is a new member of the PPR family. FEBS Lett 480: 255-260.
23. Liu X, Yu F, Rodermel S (2010) An Arabidopsis pentatricopeptide repeat protein, SUPPRESSOR OF VARIEGATION7, is required for FtsH-mediated chloroplast biogenesis. Plant Physiol 154: 1588-1601.
24. Lurin C, Andres C, Aubourg S, Bellaoui M, Bitton F, Bruyere C, Caboche M, Debast C, Gualberto J, Hoffmann B, Lecharny A, Le Ret M, Martin-Magniette ML, Mireau H, Peeters N, Renou JP, Szurek B, Taconnat L, Small I (2004) Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16: 2089-2103.
25. Maiwald D, Dietzmann A, Jahns P, Pesaresi P, Joliot P, Joliot A, Levin JZ, Salamini F, Leister D (2003) Knock-out of the genes coding for the Rieske protein and the ATP-synthase delta-subunit of Arabidopsis. Effects on photosynthesis, thylakoid protein composition, and nuclear chloroplast gene expression. Plant Physiol 133: 191-202.
26. Malik Ghulam M, Zghidi-Abouzid O, Lambert E, Lerbs-Mache S, Merendino L (2012) Transcriptional organization of the large and the small ATP synthase operons, atpI/H/F/A and atpB/E, in Arabidopsis thaliana chloroplasts. Plant Mol Biol 79: 259-272.
27. Margulis L (1970) Origin of eukaryotic cells: evidence and research implications for a theory of the origin and evolution of microbial, plant, and animal cells on the Precambrian earth. Yale University Press, New Haven.
28. Martin W (2003) Gene transfer from organelles to the nucleus: frequent and in big chunks. Proc Natl Acad Sci USA 100: 8612-8614.
29. Miyagi T, Kapoor S, Sugita M, Sugiura M (1998) Transcript analysis of the tobacco plastid operon rps2/atpI/H/F/A reveals the existence of a non-consensus type II (NCII) promoter upstream of the atpI coding sequence. Mol Gen Genet 257: 299-307.
30. Mochizuki N, Brusslan JA, Larkin R, Nagatani A, Chory J (2001) Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. Proc Natl Acad Sci USA 98: 2053-2058.
31. Moreira D, Philippe H (1999) Smr: a bacterial and eukaryotic homologue of the C-terminal region of the MutS2 family. Trends Biochem Sci 24: 298-300.
32. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassay with tobacco tissue culture. Physiol Plant 15: 473-497.
33. Oelmüller R, Mohr H (1986) Photooxidative destruction of chloroplasts and its consequences for expression of nuclear genes. Planta 167: 106-113.
34. Oelmüller R, Levitan I, Bergfeld R, Rajasekhar VK, Mohr H (1986) Expression of nuclear genes as affected by treatments acting on the plastids. Planta 168: 482-492.
35. Okuda K, Nakamura T, Sugita M, Shimizu T, Shikanai T (2006) A pentatricopeptide repeat protein is a site recognition factor in chloroplast RNA editing. J Biol Chem 281: 37661-37667.
36. Pfalz J, Liere K, Kandlbinder A, Dietz KJ, Oelmuller R (2006) pTAC2, -6, and -12 are components of the transcriptionally active plastid chromosome that are required for plastid gene expression. Plant Cell 18: 176-197.
37. 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 J 28: 2042-2052.
38. Prikryl J, Rojas M, Schuster G, Barkan A (2011) Mechanism of RNA stabilization and translational activation by a pentatricopeptide repeat protein. Proc Natl Acad Sci USA 108: 415-420.
39. 2 assimilation, and plant growth by overacidification of the thylakoid lumen. Plant Cell 23: 304-321.
40. Roy LM, Barkan A (1998) A SecY homologue is required for the elaboration of the chloroplast thylakoid membrane and for normal chloroplast gene expression. J Cell Biol 141: 385-395.
41. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
42. Schmitz-Linneweber C, Small I (2008) Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci 13: 663-670.
43. 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. Plant Cell 17: 2791-2804.
44. Schmitz-Linneweber C, Williams-Carrier RE, Williams-Voelker PM, Kroeger TS, Vichas A, Barkan A (2006) A pentatricopeptide repeat protein facilitates the trans-splicing of the maize chloroplast rps12 pre-mRNA. Plant Cell 18: 2650-2663.
45. Schöttler MA, Flügel C, Thiele W, Stegemann S, Bock R (2007) The plastome-encoded PsaJ subunit is required for efficient photosystem I excitation, but not for plastocyanin oxidation in tobacco. Biochem J 403: 251-260.
46. Schweer J, Loschelder H, Link G (2006) A promoter switch that can rescue a plant sigma factor mutant. FEBS Lett 580: 6617-6622.
47. Small ID, Peeters N (2000) The PPR motif-a TPR-related motif prevalent in plant organellar proteins. Trends Biochem Sci 25: 46-47.
48. Stahl DJ, Rodermel SR, Bogorad L, Subramanian AR (1993) Co-transcription pattern of an introgressed operon in the maize chloroplast genome comprising four ATP synthase subunit genes and the ribosomal rps2. Plant Mol Biol 21: 1069-1076.
49. Stern DB, Goldschmidt-Clermont M, Hanson MR (2010) Chloroplast RNA metabolism. Annu Rev Plant Biol 61: 125-155.
50. Susek RE, Ausubel FM, Chory J (1993) Signal transduction mutants of Arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development. Cell 74: 787-799.
51. 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. Plant J 40: 164-172.
52. Swiatecka-Hagenbruch M, Liere K, Börner T (2007) High diversity of plastidial promoters in Arabidopsis thaliana. Mol Genet Genom 277: 725-734.
53. Tasaki E, Hattori M, Sugita M (2010) The moss pentatricopeptide repeat protein with a DYW domain is responsible for RNA editing of mitochondrial ccmFc transcript. Plant J 62: 560-570.
54. Tzafrir I, Pena-Muralla R, Dickerman A, Berg M, Rogers R, Hutchens S, Sweeney TC, McElver J, Aux G, Patton D, Meinke D (2004) Identification of genes required for embryo development in Arabidopsis. Plant Physiol 135: 1206-1220.
55. Williams-Carrier R, Kroeger T, Barkan A (2008) Sequence-specific binding of a chloroplast pentatricopeptide repeat protein to its native group II intron ligand. RNA 14: 1930-1941.
56. Wobbe L, Schwarz C, Nickelsen J, Kruse O (2008) Translational control of photosynthetic gene expression in phototrophic eukaryotes. Physiol Plant 133: 507-515.
57. Woodson JD, Chory J (2008) Coordination of gene expression between organellar and nuclear genomes. Nat Rev Genet 9: 383-395.
58. Zehrmann A, Verbitskiy D, Hartel B, Brennicke A, Takenaka M (2011) PPR proteins network as site-specific RNA editing factors in plant organelles. RNA Biol 8: 67-70.
59. Zhelyazkova P, Sharma CM, Forstner KU, Liere K, Vogel J, Börner T (2012) The primary transcriptome of barley chloroplasts: numerous noncoding RNAs and the dominating role of the plastid-encoded RNA polymerase. Plant Cell 24: 123-136.
60. 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. Plant J 50: 710-722.
61. Zoschke R, Nakamura M, Liere K, Sugiura M, Börner T, Schmitz-Linneweber C (2010) An organellar maturase associates with multiple group II introns. Proc Natl Acad Sci USA 107: 3245-3250.
62. Zoschke R, Kroeger T, Belcher S, Schottler MA, Barkan A, Schmitz-Linneweber C (2012) The pentatricopeptide repeat-SMR protein ATP4 promotes translation of the chloroplast atpB/E mRNA. Plant J. doi: 10. 1111/j. 1365-313X. 2012. 05081. x.
63. Zubo YO, Kusnetsov VV, Börner T, Liere K (2011) Reverse protection assay: a tool to analyze transcriptional rates from individual promoters. Plant Methods 7: 47.
64. Zybailov B, Friso G, Kim J, Rudella A, Rodriguez VR, Asakura Y, Sun Q, van Wijk KJ (2009) Large scale comparative proteomics of a chloroplast Clp protease mutant reveals folding stress, altered protein homeostasis, and feedback regulation of metabolism. Mol Cell Proteom 8: 1789-1810.