Nucleoid-enriched proteomes in developing plastids and chloroplasts from maize leaves: A new conceptual framework for nucleoid functions

Plant Physiology

Volumn 158, Issue 1, 2012, Pages 156-189

  Majeran, Wojciech ^a   Friso, Giulia ^a   Asakura, Yukari ^a   Qu, Xian ^a   Huang, Mingshu ^a   Ponnala, Lalit ^a   Watkins, Kenneth P ^b   Barkan, Alice ^b   van Wijk, Klaas J ^a  

^a Department of Obstetrics Gynecology   (United States)

^b UNIVERSITY OF OREGON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ZEA MAYS;

EID: 84855286345     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.111.188474     Document Type: Article

References (162)

1. Albrecht V, Ingenfeld A, Apel K (2008) Snowy cotyledon 2: the identification of a zinc finger domain protein essential for chloroplast development in cotyledons but not in true leaves. Plant Mol Biol 66: 599-608.
2. Aravind L, Koonin EV(2000) SAP: a putative DNA-binding motif involved in chromosomal organization. Trends Biochem Sci 25: 112-114.
3. Arsova B, Hoja U, Wimmelbacher M, Greiner E, Ustun S, Melzer M, Petersen K, Lein W, Bornke F (2010) Plastidial thioredoxin z interacts with two fructokinase-like proteins in a thiol-dependent manner: evidence for an essential role in chloroplast development in Arabidopsis and Nicotiana benthamiana. Plant Cell 22: 1498-1515.
4. 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.
5. Babiychuk E, Vandepoele K, Wissing J, Garcia-Diaz M, De Rycke R, Akbari H, Joubes J, Beeckman T, Jansch L, Frentzen M, et al (2011) Plastid gene expression and plant development require a plastidic protein of the mitochondrial transcription termination factor family. Proc Natl Acad Sci USA 108: 6674-6679.
6. 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.
7. Baker NR, Leech RM (1977) Development of photosystem I and photosystem II activities in leaves of light-grown maize (Zea mays). Plant Physiol 60: 640-644.
8. Bantscheff M, Schirle M, Sweetman G, Rick J, Kuster B (2007) Quantitative mass spectrometry in proteomics: a critical review. Anal Bioanal Chem 389: 1017-1031.
9. Barkan A (2011) Expression of plastid genes: organelle-specific elaborations on a prokaryotic scaffold. Plant Physiol 155: 1520-1532.
10. Belacel N, Wang Q, Cuperlovic-Culf M (2006) Clustering methods for microarray gene expression data. OMICS 10: 507-531.
11. 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 Mol Biol 51: 651-663.
12. 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 Mol Biol 69: 541-552.
13. Bordo D, Bork P (2002) The rhodanese/Cdc25 phosphatase superfamily: sequence-structure-function relations. EMBO Rep 3: 741-746.
14. Bräutigam K, Dietzel L, Pfannschmidt T (2010) Hypothesis: a binary redox control mode as universal regulator of photosynthetic light acclimation. Plant Signal Behav 5: 81-85.
15. Brutnell TP, Sawers RJ, Mant A, Langdale JA (1999) BUNDLE SHEATH DEFECTIVE2, a novel protein required for post-translational regulation of the rbcL gene of maize. Plant Cell 11: 849-864.
16. Bryant N, Lloyd J, Sweeney C, Myouga F, Meinke D (2011) Identification of nuclear genes encoding chloroplast-localized proteins required for embryo development in Arabidopsis. Plant Physiol 155: 1678-1689.
17. Burmann BM, Schweimer K, Luo X, Wahl MC, Stitt BL, Gottesman ME, Rösch P (2010) A NusE:NusG complex links transcription and translation. Science 328: 501-504.
18. Cámara Y, Asin-Cayuela J, Park CB, Metodiev MD, Shi Y, Ruzzenente B, Kukat C, Habermann B, Wibom R, Hultenby K, et al (2011) MTERF4 regulates translation by targeting the methyltransferase NSUN4 to the mammalian mitochondrial ribosome. Cell Metab 13: 527-539.
19. Cannon GC, Ward LN, Case CI, Heinhorst S (1999) The 68 kDa DNA compacting nucleoid protein from soybean chloroplasts inhibits DNA synthesis in vitro. Plant Mol Biol 39: 835-845.
20. Chatterjee M, Sparvoli S, Edmunds C, Garosi P, Findlay K, Martin C (1996) DAG, a gene required for chloroplast differentiation and palisade development in Antirrhinum majus. EMBO J 15: 4194-4207.
21. Chen KM, Holmström M, Raksajit W, Suorsa M, Piippo M, Aro EM(2010) Small chloroplast-targeted DnaJ proteins are involved in optimization of photosynthetic reactions in Arabidopsis thaliana. BMC Plant Biol 10: 43
22. Chen KM, Piippo M, Holmstrom M, Nurmi M, Pakula E, Suorsa M, Aro EM (2011) A chloroplast-targeted DnaJ protein AtJ8 is negatively regulated by light and has rapid turnover in darkness. J Plant Physiol 168: 1780-1783.
23. Chi-Ham CL, Keaton MA, Cannon GC, Heinhorst S (2002) The DNAcompacting protein DCP68 from soybean chloroplasts is ferredoxin: sulfite reductase and co-localizes with the organellar nucleoid. Plant Mol Biol 49: 621-631.
24. Chiu CC, Chen LJ, Li HM (2010) Pea chloroplast DnaJ-J8 and Toc12 are encoded by the same gene and localized in the stroma. Plant Physiol 154: 1172-1182.
25. Cipollone R, Ascenzi P, Visca P (2007) Common themes and variations in the rhodanese superfamily. IUBMB Life 59: 51-59.
26. Cosgriff S, Chintakayala K, Chim YT, Chen X, Allen S, Lovering AL, Grainger DC (2010) Dimerization and DNA-dependent aggregation of the Escherichia coli nucleoid protein and chaperone CbpA. Mol Microbiol 77: 1289-1300.
27. D'Andrea LD, Regan L (2003) TPR proteins: the versatile helix. Trends Biochem Sci 28: 655-662.
28. Day A, Madesis P (2007) DNA replication, recombination, and repair in plastids. In R Bock, ed, Cell and Molecular Biology of Plastids, Vol 19. Springer-Verlag, Berlin, pp 65-119.
29. Dillon SC, Dorman CJ (2010) Bacterial nucleoid-associated proteins, nucleoid structure and gene expression. Nat Rev Microbiol 8: 185-195.
30. Domon B, Aebersold R (2010) Options and considerations when selecting a quantitative proteomics strategy. Nat Biotechnol 28: 710-721.
31. Dong M, Yang LL, Williams K, Fisher SJ, Hall SC, Biggin MD, Jin J, Witkowska HE (2008) A "tagless" strategy for identification of stable protein complexes genome-wide by multidimensional orthogonal chromatographic separation and iTRAQ reagent tracking. J Proteome Res 7: 1836-1849.
32. Douglas SE (1998) Plastid evolution: origins, diversity, trends. Curr Opin Genet Dev 8: 655-661.
33. Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95: 14863-14868
34. Epshtein V, Dutta D, Wade J, Nudler E (2010) An allosteric mechanism of Rho-dependent transcription termination. Nature 463: 245-249.
35. Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G, Forslund K, et al (2010) The Pfam protein families database. Nucleic Acids Res 38: D211-D222
36. Flores-Pérez U, Sauret-Güeto S, Gas E, Jarvis P, Rodríguez-Concepción M (2008) A mutant impaired in the production of plastome-encoded proteins uncovers a mechanism for the homeostasis of isoprenoid biosynthetic enzymes in Arabidopsis plastids. Plant Cell 20: 1303-1315.
37. Franklin AE, Hoffman NE (1993) Characterization of a chloroplast homologue of the 54-kDa subunit of the signal recognition particle. J Biol Chem 268: 22175-22180
38. Friso G, Majeran W, Huang M, Sun Q, van Wijk KJ (2010) Reconstruction of metabolic pathways, protein expression, and homeostasis machineries across maize bundle sheath and mesophyll chloroplasts: large-scale quantitative proteomics using the first maize genome assembly. Plant Physiol 152: 1219-1250.
39. Garcia M, Myouga F, Takechi K, Sato H, Nabeshima K, Nagata N, Takio S, Shinozaki K, Takano H (2008) An Arabidopsis homolog of the bacterial peptidoglycan synthesis enzyme MurE has an essential role in chloroplast development. Plant J 53: 924-934.
40. Glynn JM, Yang Y, Vitha S, Schmitz AJ, Hemmes M, Miyagishima SY, Osteryoung KW (2009) PARC6, a novel chloroplast division factor, influences FtsZ assembly and is required for recruitment of PDV1 during chloroplast division in Arabidopsis. Plant J 59: 700-711.
41. Gowrishankar J, Harinarayanan R (2004) Why is transcription coupled to translation in bacteria? Mol Microbiol 54: 598-603.
42. Gray MW (1999) Evolution of organellar genomes. Curr Opin Genet Dev 9: 678-687.
43. Gutman BL, Niyogi KK (2009) Evidence for base excision repair of oxidative DNA damage in chloroplasts of Arabidopsis thaliana. J Biol Chem 284: 17006-17012
44. Hallick RB, Lipper C, Richards OC, Rutter WJ (1976) Isolation of a transcriptionally active chromosome from chloroplasts of Euglena gracilis. Biochemistry 15: 3039-3045.
45. Haswell ES, Meyerowitz EM (2006) MscS-like proteins control plastid size and shape in Arabidopsis thaliana. Curr Biol 16: 1-11.
46. Hilbert M, Karow AR, Klostermeier D (2009) The mechanism of ATPdependent RNA unwinding by DEAD box proteins. Biol Chem 390: 1237-1250.
47. Huang S, Taylor NL, Narsai R, Eubel H, Whelan J, Millar AH (2009) Experimental analysis of the rice mitochondrial proteome, its biogenesis, and heterogeneity. Plant Physiol 149: 719-734.
48. Jeong SY, Rose A, Meier I (2003) MFP1 is a thylakoid-associated, nucleoidbinding protein with a coiled-coil structure. Nucleic Acids Res 31: 5175-5185.
49. Kabeya Y, Nakanishi H, Suzuki K, Ichikawa T, Kondou Y, Matsui M, Miyagishima SY (2010) The YlmG protein has a conserved function related to the distribution of nucleoids in chloroplasts and cyanobacteria. BMC Plant Biol 10: 57
50. Kang YW, Lee JY, Jeon Y, Cheong GW, Kim M, Pai HS (2010) In vivo effects of NbSiR silencing on chloroplast development in Nicotiana benthamiana. Plant Mol Biol 72: 569-583.
51. Karcher D, Köster D, Schadach A, Klevesath A, Bock R (2009) The Chlamydomonas chloroplast HLP protein is required for nucleoid organization and genome maintenance. Mol Plant 2: 1223-1232.
52. Kato Y, Sakamoto W (2010) New insights into the types and function of proteases in plastids. Int Rev Cell Mol Biol 280: 185-218.
53. Khrouchtchova A, Hansson M, Paakkarinen V, Vainonen JP, Zhang S, Jensen PE, Scheller HV, Vener AV, Aro EM, Haldrup A (2005) A previously found thylakoid membrane protein of 14kDa (TMP14) is a novel subunit of plant photosystem I and is designated PSI-P. FEBS Lett 579: 4808-4812.
54. Kobayashi T, Takahara M, Miyagishima SY, Kuroiwa H, Sasaki N, Ohta N, Matsuzaki M, Kuroiwa T (2002) Detection and localization of a chloroplast-encoded HU-like protein that organizes chloroplast nucleoids. Plant Cell 14: 1579-1589.
55. Krause K, Krupinska K (2000) Molecular and functional properties of highly purified transcriptionally active chromosomes from spinach chloroplasts. Physiol Plant 109: 188-195.
56. Kroeger TS, Watkins KP, Friso G, van Wijk KJ, Barkan A (2009) A plantspecific RNA-binding domain revealed through analysis of chloroplast group II intron splicing. Proc Natl Acad Sci USA 106: 4537-4542.
57. Kuroiwa T (1973) Studies on mitochondrial structure and function in Physarium polycephalum. I. Fine structure, cytochemistry, and 3Huridine autoradiography of a central body in mitochondria. Exp Cell Res 78: 351-359.
58. Kuroiwa T (1991) The replication, differentiation, and inheritance of plastids with emphasis on the concept of organelle nuclei. Int Rev Cytol 128: 1-62.
59. Kuroiwa T, Fujie M, Kuroiwa H (1992) Studies on the behavior of mitochondrial DNA: synthesis of mitochondrial DNA occurs actively in a specific region just above the quiescent center in the root apical meristem of Pelargonium zonale. J Cell Sci 101: 483-493.
60. Kuroiwa T, Kawano S, Nishibayashi S, Sato C (1982) Epifluorescent microscopic evidence for maternal inheritance of chloroplast DNA. Nature 298: 481-483.
61. Kuroiwa T, Ohta T, Kuroiwa H, Shigeyuki K (1994) Molecular and cellular mechanisms of mitochondrial nuclear division and mitochondriokinesis. Microsc Res Tech 27: 220-232.
62. Leech RM, Rumsby MG, Thomson WW (1973) Plastid differentiation, acyl lipid, and fatty acid changes in developing green maize leaves. Plant Physiol 52: 240-245.
63. Lensch M, Herrmann RG, Sokolenko A (2001) Identification and characterization of SppA, a novel light-inducible chloroplast protease complex associated with thylakoid membranes. J Biol Chem 276: 33645-33651
64. Lezhneva L, Kuras R, Ephritikhine G, de Vitry C (2008) A novel pathway of cytochrome c biogenesis is involved in the assembly of the cytochrome b6f complex in Arabidopsis chloroplasts. J Biol Chem 283: 24608-24616
65. Li QS, Gupta JD, Hunt AG (1998) Polynucleotide phosphorylase is a component of a novel plant poly(A) polymerase. J Biol Chem273: 17539-17543
66. Liere K, Weihe A, Börner T (2011) The transcription machineries of plant mitochondria and chloroplasts: composition, function, and regulation. J Plant Physiol 168: 1345-1360.
67. Linder P (2006) Dead-box proteins: a family affair. Active and passive players in RNP-remodeling. Nucleic Acids Res 34: 4168-4180.
68. Liu H, Sadygov RG, Yates JR III (2004) A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal Chem 76: 4193-4201.
69. Liu X, Yu F, Rodermel S (2010a) Arabidopsis chloroplast FtsH, var2 and suppressors of var2 leaf variegation: a review. J Integr Plant Biol 52: 750-761.
70. Liu X, Yu F, Rodermel S (2010b) An Arabidopsis pentatricopeptide repeat protein, SUPPRESSOR OF VARIEGATION7, is required for FtsH-mediated chloroplast biogenesis. Plant Physiol 154: 1588-1601.
71. Lockshon D, Zweifel SG, Freeman-Cook LL, Lorimer HE, Brewer BJ, Fangman WL (1995) A role for recombination junctions in the segregation of mitochondrial DNA in yeast. Cell 81: 947-955.
72. Long TA, Brady SM, Benfey PN (2008) Systems approaches to identifying gene regulatory networks in plants. Annu Rev Cell Dev Biol 24: 81-103.
73. Ma J, Peng L, Guo J, Lu Q, Lu C, Zhang L (2007) LPA2 is required for efficient assembly of photosystem II in Arabidopsis thaliana. Plant Cell 19: 1980-1993.
74. Machida M, Takechi K, Sato H, Chung SJ, Kuroiwa H, Takio S, Seki M, Shinozaki K, Fujita T, Hasebe M, et al (2006) Genes for the peptidoglycan synthesis pathway are essential for chloroplast division in moss. Proc Natl Acad Sci USA 103: 6753-6758.
75. Majeran W, Cai Y, Sun Q, van Wijk KJ (2005) Functional differentiation of bundle sheath and mesophyll maize chloroplasts determined by comparative proteomics. Plant Cell 17: 3111-3140.
76. Majeran W, Friso G, Ponnala L, Connolly B, Huang M, Reidel E, Zhang C, Asakura Y, Bhuiyan NH, Sun Q, et al (2010) Structural and metabolic transitions of C4 leaf development and differentiation defined by microscopy and quantitative proteomics in maize. Plant Cell 22: 3509-3542.
77. Majeran W, Zybailov B, Ytterberg AJ, Dunsmore J, Sun Q, van Wijk KJ (2008) Consequences of C4 differentiation for chloroplast membrane proteomes in maize mesophyll and bundle sheath cells. Mol Cell Proteomics 7: 1609-1638.
78. Mann M, Kelleher NL (2008) Precision proteomics: the case for high resolution and high mass accuracy. Proc Natl Acad Sci USA 105: 18132-18138
79. Maréchal A, Parent JS, Véronneau-Lafortune F, Joyeux A, Lang BF, Brisson N (2009) Whirly proteins maintain plastid genome stability in Arabidopsis. Proc Natl Acad Sci USA 106: 14693-14698
80. Meier I, Phelan T, Gruissem W, Spiker S, Schneider D (1996) MFP1, a novel plant filament-like protein with affinity for matrix attachment region DNA. Plant Cell 8: 2105-2115.
81. Melonek J, Mulisch M, Schmitz-Linneweber C, Grabowski E, Hensel G, Krupinska K (2010) Whirly1 in chloroplasts associates with intron containing RNAs and rarely co-localizes with nucleoids. Planta 232: 471-481.
82. Meskauskiene R, Nater M, Goslings D, Kessler F, op den Camp R, Apel K (2001) FLU: a negative regulator of chlorophyll biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 98: 12826-12831
83. Meskauskiene R, Würsch M, Laloi C, Vidi PA, Coll NS, Kessler F, Baruah A, Kim C, Apel K (2009) A mutation in the Arabidopsis mTERF-related plastid protein SOLDAT10 activates retrograde signaling and suppresses 1O2-induced cell death. Plant J 60: 399-410.
84. Miyamura S, Nagata T, Kuroiwa T (1986) Quantitative fluorescence microscopy on dynamic changes of plastid nucleoids during wheat development. Protoplasma 133: 66-72.
85. Mori Y, Kimura S, Saotome A, Kasai N, Sakaguchi N, Uchiyama Y, Ishibashi T, Yamamoto T, Chiku H, Sakaguchi K (2005) Plastid DNA polymerases from higher plants, Arabidopsis thaliana. Biochem Biophys Res Commun 334: 43-50.
86. Myouga F, Hosoda C, Umezawa T, Iizumi H, Kuromori T, Motohashi R, Shono Y, Nagata N, Ikeuchi M, Shinozaki K (2008) A heterocomplex of iron superoxide dismutases defends chloroplast nucleoids against oxidative stress and is essential for chloroplast development in Arabidopsis. Plant Cell 20: 3148-3162.
87. Nagata N, Saito C, Sakai A, Kuroiwa H, Kuroiwa T (1999) The selective increase or decrease of organellar DNA in generative cells just after pollen mitosis one controls cytoplasmic inheritance. Planta 209: 53-65.
88. Nerozzi AM, Coleman AW (1997) Localization of plastid DNA replication on a nucleoid structure. Am J Bot 84: 1028-1041.
89. Nilsson R, Brunner J, Hoffman NE, van Wijk KJ (1999) Interactions of ribosome nascent chain complexes of the chloroplast-encoded D1 thylakoid membrane protein with cpSRP54. EMBO J 18: 733-742.
90. 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. Plant J 63: 766-777.
91. Old WM, Meyer-Arendt K, Aveline-Wolf L, Pierce KG, Mendoza A, Sevinsky JR, Resing KA, Ahn NG (2005) Comparison of label-free methods for quantifying human proteins by shotgun proteomics. Mol Cell Proteomics 4: 1487-1502.
92. 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. Mol Cell Proteomics 9: 1594-1615.
93. Olinares PDB, Kim J, Davis JI, van Wijk KJ (2011) Subunit stoichiometry, evolution, and functional implications of an asymmetric plant plastid ClpP/R protease complex in Arabidopsis. Plant Cell 23: 2348-2361.
94. O'Toole N, Hattori M, Andres C, Iida K, Lurin C, Schmitz-Linneweber C, Sugita M, Small I (2008) On the expansion of the pentatricopeptide repeat gene family in plants. Mol Biol Evol 25: 1120-1128.
95. Parent JS, Lepage E, Brisson N (2011) Divergent roles for the two PolI-like organelle DNA polymerases of Arabidopsis. Plant Physiol 156: 254-262.
96. Pellegrini M, Asin-Cayuela J, Erdjument-Bromage H, Tempst P, Larsson NG, Gustafsson CM (2009) MTERF2 is a nucleoid component in mammalian mitochondria. Biochim Biophys Acta 1787: 296-302.
97. Peng L, Ma J, Chi W, Guo J, Zhu S, Lu Q, Lu C, Zhang L (2006) LOW PSII ACCUMULATION1 is involved in efficient assembly of photosystem II in Arabidopsis thaliana. Plant Cell 18: 955-969.
98. 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. Plant Cell 18: 176-197.
99. Phinney BS, Thelen JJ (2005) Proteomic characterization of a Tritoninsoluble fraction from chloroplasts defines a novel group of proteins associated with macromolecular structures. J Proteome Res 4: 497-506.
100. Pontén F, Gry M, Fagerberg L, Lundberg E, Asplund A, Berglund L, Oksvold P, Björling E, Hober S, Kampf C, et al (2009) A global view of protein expression in human cells, tissues, and organs. Mol Syst Biol 5: 337
101. 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 Res 36: 5152-5165.
102. Proshkin S, Rahmouni AR, Mironov A, Nudler E (2010) Cooperation between translating ribosomes and RNA polymerase in transcription elongation. Science 328: 504-508.
103. Quesada V, Sarmiento-Manus R, Gonzalez-Bayon R, Hricova A, Perez-Marcos R, Gracia-Martinez E, Medina-Ruiz L, Leyva-Diaz E, Ponce MR, Micol JL (2011) Arabidopsis RUGOSA2 encodes an mTERF family member required for mitochondrion, chloroplast and leaf development. Plant J 68: 738-753.
104. Quintana LF, Campistol JM, Alcolea MP, Bañon-Maneus E, Sol-González A, Cutillas PR (2009) Application of label-free quantitative peptidomics for the identification of urinary biomarkers of kidney chronic allograft dysfunction. Mol Cell Proteomics 8: 1658-1673.
105. Richter CV, Bals T, Schünemann D (2010) Component interactions, regulation and mechanisms of chloroplast signal recognition particledependent protein transport. Eur J Cell Biol 89: 965-973.
106. Roberti M, Polosa PL, Bruni F, Manzari C, Deceglie S, Gadaleta MN, Cantatore P (2009) The MTERF family proteins: mitochondrial transcription regulators and beyond. Biochim Biophys Acta 1787: 303-311.
107. Robinow C, Kellenberger E (1994) The bacterial nucleoid revisited. Microbiol Rev 58: 211-232.
108. Rocak S, Linder P (2004) DEAD-box proteins: the driving forces behind RNA metabolism. Nat Rev Mol Cell Biol 5: 232-241.
109. Rochaix JD (2011) Regulation of photosynthetic electron transport. Biochim Biophys Acta 1807: 375-383.
110. Ruwe H, Kupsch C, Teubner M, Schmitz-Linneweber C (2011) The RNArecognition motif in chloroplasts. J Plant Physiol 168: 1361-1371.
111. Sakai A, Suzuki T, Nagata N, Sasaki N, Miyazawa Y, Saito C, Inada N, Nishimura Y, Kuroiwa T (1999) Comparative analysis of DNA synthesis activity in plastid-nuclei and mitochondrial-nuclei simultaneously isolated from cultured tobacco cells. Plant Sci 140: 9-19.
112. Sakai A, Takano H, Kuroiwa T (2004) Organelle nuclei in higher plants: structure, composition, function, and evolution. Int Rev Cytol 238: 59-118.
113. Sakai A, Yamashita H, Nemoto Y, Kawano S, Kuroiwa T (1991) Transcriptional activity of morphologically intact proplastid-nuclei (nucleoids) isolated from tobacco cultured cells. Plant Cell Physiol 32: 835-843.
114. Samaniego R, Jeong SY, Meier I, de la Espina SM (2006) Dual location of MAR-binding, filament-like protein 1 in Arabidopsis, tobacco, and tomato. Planta 223: 1201-1206.
115. Sandhu C, Hewel JA, Badis G, Talukder S, Liu J, Hughes TR, Emili A (2008) Evaluation of data-dependent versus targeted shotgun proteomic approaches for monitoring transcription factor expression in breast cancer. J Proteome Res 7: 1529-1541.
116. Sasaki N, Sakai A, Kawano S, Kuroiwa H, Kuroiwa T (1998) DNA synthesis in isolated mitochondrial nucleoids from plasmodia of Physarium polycephalum. Protoplasma 203: 221-231.
117. Sato N, Nakayama M, Hase T (2001) The 70-kDa major DNA-compacting protein of the chloroplast nucleoid is sulfite reductase. FEBS Lett 487: 347-350.
118. Sato N, Ohshima K, Watanabe A, Ohta N, Nishiyama Y, Joyard J, Douce R (1998) Molecular characterization of the PEND protein, a novel bZIP protein present in the envelope membrane that is the site of nucleoid replication in developing plastids. Plant Cell 10: 859-872.
119. Sato N, Rolland N, Block MA, Joyard J (1999) Do plastid envelope membranes play a role in the expression of the plastid genome? Biochimie 81: 619-629.
120. Sato N, Terasawa K, Miyajima K, Kabeya Y (2003) Organization, developmental dynamics, and evolution of plastid nucleoids. Int Rev Cytol 232: 217-262.
121. Schmitz-Linneweber C, Small I (2008) Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci 13: 663-670.
122. Schröter Y, Steiner S, Matthäi K, Pfannschmidt T (2010) Analysis of oligomeric protein complexes in the chloroplast sub-proteome of nucleic acid-binding proteins from mustard reveals potential redox regulators of plastid gene expression. Proteomics 10: 2191-2204.
123. Schult K, Meierhoff K, Paradies S, Töller T, Wolff P, Westhoff P (2007) The nuclear-encoded factor HCF173 is involved in the initiation of translation of the psbA mRNA in Arabidopsis thaliana. Plant Cell 19: 1329-1346.
124. Schweer J, Türkeri H, Kolpack A, Link G (2010) Role and regulation of plastid sigma factors and their functional interactors during chloroplast transcription: recent lessons from Arabidopsis thaliana. Eur J Cell Biol 89: 940-946.
125. Sekine K, Fujiwara M, NakayamaM, Takao T, Hase T, Sato N (2007) DNA binding and partial nucleoid localization of the chloroplast stromal enzyme ferredoxin:sulfite reductase. FEBS J 274: 2054-2069.
126. Selldén G, Leech RM (1981) Localization ofDNAinmature and youngwheat chloroplasts using the fluorescent probe 4#-6-diamidino-2-phenylindole. Plant Physiol 68: 731-734.
127. Shajani Z, Sykes MT, Williamson JR (2011) Assembly of bacterial ribosomes. Annu Rev Biochem 80: 501-526.
128. Shevchenko A, Wilm M, Vorm O, Mann M (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68: 850-858.
129. Smith CA (2006) Structure, function and dynamics in the mur family of bacterial cell wall ligases. J Mol Biol 362: 640-655.
130. Sodmergen S, Kawano S, Kuroiwa T (1991) Degradation of chloroplast DNA in second leaves of rice (Oryza sativa) before leaf yellowing. Protoplasma 160: 89-98.
131. Sokolenko A, Pojidaeva E, Zinchenko V, Panichkin V, Glaser VM, Herrmann RG, Shestakov SV (2002) The gene complement for proteolysis in the cyanobacterium Synechocystis sp. PCC 6803 and Arabidopsis thaliana chloroplasts. Curr Genet 41: 291-310.
132. Steiner S, Dietzel L, Schröter Y, Fey V, Wagner R, Pfannschmidt T (2009) The role of phosphorylation in redox regulation of photosynthesis genes psaA and psbA during photosynthetic acclimation of mustard. Mol Plant 2: 416-429.
133. Steiner S, Schroter Y, Pfalz J, Pfannschmidt T (2011) Identification of essential subunits in the plastid-encoded RNA polymerase complex reveals building blocks for proper plastid development. Plant Physiol 157: 1043-1055.
134. Stern DB, Goldschmidt-Clermont M, Hanson MR (2010) Chloroplast RNA metabolism. Annu Rev Plant Biol 61: 125-155.
135. Stern DB, Hanson MR, Barkan A (2004) Genetics and genomics of chloroplast biogenesis: maize as a model system. Trends Plant Sci 9: 293-301.
136. Sun Q, Zybailov B, Majeran W, Friso G, Olinares PD, van Wijk KJ (2009) PPDB, the Plant Proteomics Database at Cornell. Nucleic Acids Res 37: D969-D974
137. 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.
138. Suzuki T, Kawano S, Sakai A, Fujie M, Kuroiwa H, Nakamura H, Kuroiwa T (1992) Preferentialmitochondrial and plastid DNA synthesis before multiple cell divisions in Nicotiana tabacum. J Cell Sci 103: 831-837.
139. Takano H, Takechi K (2010) Plastid peptidoglycan. Biochim Biophys Acta 1800: 144-151.
140. Terasawa K, Sato N (2005a) Occurrence and characterization of PEND proteins in angiosperms. J Plant Res 118: 111-119.
141. Terasawa K, Sato N (2005b) Visualization of plastid nucleoids in situ using the PEND-GFP fusion protein. Plant Cell Physiol 46: 649-660.
142. Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, Krüger P, Selbig J, Müller LA, Rhee SY, Stitt M (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37: 914-939.
143. Tikkanen M, Aro EM (2011) Thylakoid protein phosphorylation in dynamic regulation of photosystem II in higher plants. Biochim Biophys Acta (in press)
144. Till B, Schmitz-Linneweber C, Williams-Carrier R, Barkan A (2001) CRS1 is a novel group II intron splicing factor that was derived from a domain of ancient origin. RNA 7: 1227-1238.
145. 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. Proc Natl Acad Sci USA 106: 6002-6007.
146. Tzafrir I, Pena-Muralla R, Dickerman A, Berg M, Rogers R, Hutchens S, Sweeney TC, McElver J, Aux G, Patton D, et al (2004) Identification of genes required for embryo development in Arabidopsis. Plant Physiol 135: 1206-1220.
147. Vainonen JP, Sakuragi Y, Stael S, Tikkanen M, Allahverdiyeva Y, Paakkarinen V, Aro E, Suorsa M, Scheller HV, Vener AV, et al (2008) Light regulation of CaS, a novel phosphoprotein in the thylakoid membrane of Arabidopsis thaliana. FEBS J 275: 1767-1777.
148. van Wijk KJ, Baginsky S (2011) Update on plastid proteomics in higher plants: current state and future goals. Plant Physiol 155: 1578-1588.
149. Wang Y, Duby G, Purnelle B, Boutry M (2000) Tobacco VDL gene encodes a plastid DEAD box RNA helicase and is involved in chloroplast differentiation and plant morphogenesis. Plant Cell 12: 2129-2142.
150. 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. Plant Cell 19: 2606-2623.
151. Watkins KP, Rojas M, Friso G, van Wijk KJ, Meurer J, Barkan A (2011) APO1 promotes the splicing of chloroplast group II introns and harbors a plantspecific zinc-dependent RNA binding domain. Plant Cell 23: 1082-1092.
152. Weber P, Fulgosi H, Piven I, Müller L, Krupinska K, Duong VH, Herrmann RG, Sokolenko A (2006) TCP34, a nuclear-encoded response regulator-like TPR protein of higher plant chloroplasts. J Mol Biol 357: 535-549.
153. Wetzel CM, Harmacek LD, Yuan LH, Wopereis JL, Chubb R, Turini P (2009) Loss of chloroplast protease SPPA function alters high light acclimation processes in Arabidopsis thaliana L. (Heynh.). J Exp Bot 60: 1715-1727.
154. Wilson ME, Jensen GS, Haswell ES (2011) Two mechanosensitive channel homologs influence division ring placement in Arabidopsis chloroplasts. Plant Cell 23: 2939-2949.
155. Xu YZ, Arrieta-Montiel MP, Virdi KS, de Paula WB, Widhalm JR, Basset GJ, Davila JI, Elthon TE, Elowsky CG, Sato SJ, et al (2011) MutS HOMOLOG1 is a nucleoid protein that alters mitochondrial and plastid properties and plant response to high light. Plant Cell 23: 3428-3441.
156. Yakubovskaya E, Mejia E, Byrnes J, Hambardjieva E, Garcia-Diaz M (2010) Helix unwinding and base flipping enable human MTERF1 to terminate mitochondrial transcription. Cell 141: 982-993.
157. Yamaguchi K, Subramanian AR (2003) Proteomic identification of all plastid-specific ribosomal proteins in higher plant chloroplast 30S ribosomal subunit. Eur J Biochem 270: 190-205.
158. Yang J, Schuster G, Stern DB (1996) CSP41, a sequence-specific chloroplast mRNA binding protein, is an endoribonuclease. Plant Cell 8: 1409-1420.
159. Yu F, Liu X, Alsheikh M, Park S, Rodermel S (2008) Mutations in SUPPRESSOR OF VARIEGATION1, a factor required for normal chloroplast translation, suppress var2-mediated leaf variegation in Arabidopsis. Plant Cell 20: 1786-1804.
160. Zhu J, Fu X, Koo YD, Zhu JK, Jenney FE Jr, Adams MW, Zhu Y, Shi H, Yun DJ, Hasegawa PM, et al (2007) An enhancer mutant of Arabidopsis salt overly sensitive 3 mediates both ion homeostasis and the oxidative stress response. Mol Cell Biol 27: 5214-5224.
161. Zybailov B, Coleman MK, Florens L, Washburn MP (2005) Correlation of relative abundance ratios derived from peptide ion chromatograms and spectrum counting for quantitative proteomic analysis using stable isotope labeling. Anal Chem 77: 6218-6224.
162. 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