Exclusion of plastid nucleoids and ribosomes from stromules in tobacco and Arabidopsis

Plant Journal

Volumn 69, Issue 3, 2012, Pages 399-410

  Newell, Christine A ^a   Natesan, Senthil K A ^a,c   Sullivan, James A ^a,d   Jouhet, Juliette ^a,e   Kavanagh, Tony A ^b   Gray, John C ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b TRINITY COLLEGE DUBLIN   (Ireland)

^c ILLUMINA INC   (United States)

^d QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^e CEA GRENOBLE   (France)

Author keywords

chloroplast; plastid DNA; plastid nucleoid; plastid ribosome; stromule

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS SEEDLINGS; ARABIDOPSIS THALIANA; CHLOROPLAST; EPIDERMAL CELLS; GENETIC INFORMATION; GREEN FLUORESCENT PROTEIN; LAC REPRESSOR; NICOTIANA TABACUM; NUCLEOIDS; PLASTID NUCLEOID; PLASTID RIBOSOME; RARE EVENT; RIBOSOMAL PROTEINS; STROMULE; TRANSGENIC TOBACCO;

CHLOROPHYLL; DNA; FLUORESCENCE; GENES; MACROMOLECULES; PLANTS (BOTANY); PROTEINS; TISSUE; TOBACCO;

DNA SEQUENCES;

CHLOROPLAST DNA; GREEN FLUORESCENT PROTEIN; PLANT DNA;

ARABIDOPSIS; ARTICLE; CONFOCAL MICROSCOPY; CYTOLOGY; GENETIC TRANSFORMATION; GENETICS; METABOLISM; PLASTID; RIBOSOME; TOBACCO; TRANSGENIC PLANT; TRANSPORT AT THE CELLULAR LEVEL;

ARABIDOPSIS; BIOLOGICAL TRANSPORT; DNA, CHLOROPLAST; DNA, PLANT; GREEN FLUORESCENT PROTEINS; MICROSCOPY, CONFOCAL; PLANTS, GENETICALLY MODIFIED; PLASTIDS; RIBOSOMES; TOBACCO; TRANSFORMATION, GENETIC;

ARABIDOPSIS; ARABIDOPSIS THALIANA; NICOTIANA TABACUM;

EID: 84856252709     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2011.04798.x     Document Type: Article

References (79)

1. Anderson, S., and, Smith, S.M., (1986) Synthesis of the small subunit of ribulose-bisphosphate carboxylase from genes cloned into plasmids containing the SP6 promoter. Biochem. J. 240, 709-715. (Pubitemid 17009987)
2. Baldev, A., Gaikwad, K., Kirti, P.D., Mohapatra, T., Prakash, S., and, Chopra, V.L., (1998) Recombination between chloroplast genomes of Trachystoma ballii and Brassica juncea following protoplast fusion. Mol. Gen. Genet. 260, 357-361. (Pubitemid 28552172)
3. Bechtold, N., Ellis, J., and, Pelletier, G., (1993) In planta Agrobacterium mediated gene transfer by infiltration of adult Arabidopsis thaliana plants. C. R. Acad. Sci. III Life Sci. 316, 1194-1199. (Pubitemid 23336519)
4. Bevan, M.W., (1984) Binary Agrobacterium vectors for plant transformation. Nucl. Acids Res. 12, 8711-8721.
5. Birch-Machin, I., Newell, C.A., Hibberd, J.M., and, Gray, J.C., (2004) Accumulation of rotavirus VP6 protein in chloroplasts of transplastomic tobacco is limited by protein stability. Plant Biotechnol. J. 2, 261-270. (Pubitemid 40199458)
6. Boardman, N.K., Francki, R.I.B., and, Wildman, S.G., (1965) Protein synthesis by cell-free extracts from tobacco leaves. II. Association of activity with chloroplast ribosomes. Biochemistry, 4, 872-876.
7. Bourett, T.M., Czymmek, K.J., and, Howard, R.J., (1999) Ultrastructure of chloroplast protuberances in rice leaves preserved by high-pressure freezing. Planta, 208, 472-479.
8. von Braun, S.S., Sabetti, A., Hanic-Joyce, P.J., Gu, J., Schleiff, E., and, Joyce, P.B.M., (2007) Dual targeting of the tRNA nucleotidyltransferase in plants: not just the signal. J. Exp. Bot. 58, 4083-4093. (Pubitemid 351323607)
9. Caplan, J.L., Mamillapalli, P., Burch-Smith, T.M., Czymmek, K., and, Dinesh-Kumar, S.P., (2008) Chloroplastic protein NRIP1 mediates innate immune receptor recognition of a viral effector. Cell, 132, 449-462. (Pubitemid 351191994)
10. Chua, N.-H., Blobel, G., Siekevitz, P., and, Palade, G.E., (1973) Attachment of chloroplast polysomes to thylakoid membranes in Chlamydomonas reinhardtii. Proc. Natl Acad. Sci. USA, 70, 1554-1558.
11. Chua, N.-H., Blobel, G., Siekevitz, P., and, Palade, G.E., (1976) Periodic variations in the ration of free to thylakoid-bound chloroplast ribosomes during the cell cycle of Chlamydomonas reinhardtii. J. Cell Biol. 71, 497-514.
12. Clark, E.M., Izhar, S., and, Hanson, M.R., (1985) Independent segregation of the plastid genome and cytoplasmic male sterility in petunia somatic hybrids. Mol. Gen. Genet. 199, 440-445.
13. Dean, C., and, Leech, R.M., (1982) Genome expression during normal leaf development. I. Cellular and chloroplast numbers and DNA, RNA, and protein levels in tissues of different ages within a seven-day-old wheat leaf. Plant Physiol. 69, 904-910.
14. Dundr, M., McNally, J.G., Cohen, J., and, Misteli, T., (2002) Quantitation of GFP-fusion proteins in single living cells. J. Struct. Biol. 140, 92-99. (Pubitemid 36139850)
15. Eilam, Y., Butler, R.D., and, Simon, E.W., (1971) Ribosomes and polysomes in cucumber leaves during growth and senescence. Plant Physiol. 47, 317-323.
16. Falk, H., (1969) Rough thylakoids: polysomes attached to chloroplast membranes. J. Cell Biol. 42, 582-586.
17. Fejes, E., Engeler, D., and, Maliga, P., (1990) Extensive homologous chloroplast DNA recombination in the pt14 Nicotiana somatic hybrid. Theor. Appl. Genet. 79, 28-32.
18. Fluhr, R., Aviv, D., Galun, E., and, Edelman, M., (1984) Generation of heteroplastidic Nicotiana cybrids by protoplast fusion-analysis for plastid recombinant types. Theor. Appl. Genet. 67, 491-497.
19. Gray, J.C., Sullivan, J., Hibberd, J.M., and, Hansen, M.R., (2001) Stromules: mobile protrusions and interconnections between plastids. Plant Biol. 3, 223-233. (Pubitemid 32667743)
20. Guirimand, G., Burlat, V., Oudin, A., Lanoue, A.S., St-Pierre, B., and, Courdavault, V., (2009) Optimization of the transient transformation of Catharanthus roseus cells by particle bombardment and its application to the subcellular localization of hydroxymethylbutenyl 4-phosphate synthase and geraniol 10-hydroxylase. Plant Cell Rep. 28, 1215-1234.
21. Gunning, B.E.S., (2005) Plastid stromules: video microscopy of their outgrowth, retraction, tensioning, anchoring, branching, bridging, and tip-shedding. Protoplasma, 225, 33-42.
22. Gunning, B.E.S., and, Steer, M.W., (1975) Ultrastructure and the Biology of Plant Cells. London: Edward Arnold, pp. 312.
23. Hans, J., Hause, B., Strack, D., and, Walter, M., (2004) Cloning, characterization, and immunolocalization of a mycorrhiza-inducible 1-deoxy-d-xylulose 5-phosphate reductoisomerase in arbuscule-containing cells of maize. Plant Physiol. 134, 614-624. (Pubitemid 38261535)
24. Hanson, M.R., and, Sattarzadeh, A., (2008) Dynamic morphology of plastids and stromules in angiosperm plants. Plant Cell Environ. 31, 646-657. (Pubitemid 351503410)
25. Haseloff, J., Siemering, K.R., Prasher, D.C., and, Hodge, E., (1997) Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly. Proc. Natl Acad. Sci. USA, 94, 2122-2127. (Pubitemid 27136838)
26. Hellens, R.P., Edwards, E.A., Leyland, N.R., Bean, S., and, Mullineaux, P.M., (2000) pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Mol. Biol. 42, 819-832. (Pubitemid 30399867)
27. Hibberd, J.M., Linley, P.J., Khan, M.S., and, Gray, J.C., (1998) Transient expression of green fluorescent protein in various plastid types following microprojectile bombardment. Plant J. 16, 627-632.
28. Horsch, R.B., Fry, J.E., Hoffman, N.L., Eichholtz, D., Rogers, S.G., and, Fraley, R.T., (1985) A simple and general method for transferring genes into plants. Science, 227, 1229-1231.
29. Huang, J., Taylor, J.P., Chen, J.-G., Uhrig, J.F., Schnell, D.J., Nakagawa, T., Korth, K.L., and, Jones, A.M., (2006) The plastid protein THYLAKOID FORMATION1 and the plasma membrane G-protein GPA1 interact in a novel sugar-signaling mechanism in Arabidopsis. Plant Cell, 18, 1226-1238. (Pubitemid 43956128)
30. Jacobson, A.B., Swift, H., and, Bogorad, L., (1963) Cytochemical studies concerning the occurrence and distribution of RNA in plastids of Zea mays. J. Cell Biol. 17, 557-570.
31. Jefferson, R.A., Kavanagh, T.A., and, Bevan, M.W., (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901-3907.
32. Jeong, S.Y., Rose, A., and, Meier, I., (2003) MFP1 is a thylakoid-associated, nucleoid-binding protein with a coiled-coil structure. Nucleic Acids Res. 31, 5175-5185. (Pubitemid 37441885)
33. Kandel-Kfir, M., Damari-Weissler, H., German, M.A., Gidoni, D., Mett, A., Belausov, E., Petreikov, M., Adir, N., and, Granot, D., (2006) Two newly identified membrane-associated and plastidic tomato HXKs: characteristics, predicted structure and intracellular localization. Planta, 224, 1341-1352. (Pubitemid 44769866)
34. Knoblauch, M., Hibberd, J.M., Gray, J.C., and, van Bel, A.J.E., (1999) A galinstan expansion femtosyringe for microinjection of eukaryotic organelles and prokaryotes. Nat. Biotechnol. 17, 906-909. (Pubitemid 29416667)
35. Köhler, R.H., and, Hanson, M.R., (2000) Plastid tubules of higher plants are tissue-specific and developmentally regulated. J. Cell Sci. 113, 81-89. (Pubitemid 30066335)
36. Köhler, R.H., Cao, J., Zipfel, W.R., Webb, W.W., and, Hanson, M.R., (1997) Exchange of protein molecules through connections between higher plant plastids. Science, 276, 2039-2042. (Pubitemid 27443608)
37. Köhler, R.H., Schwille, P., Webb, W.W., and, Hanson, M.R., (2000) Active protein transport through plastid tubules: velocity quantified by fluorescence correlation spectroscopy. J. Cell Sci. 113, 3921-3930. (Pubitemid 32194517)
38. Kuroiwa, T., (1991) The replication, differentiation and inheritance of plastids with special emphasis on the concept of organelle nuclei. Int. Rev. Cytol. 128, 1-62.
39. Kwok, E.Y., and, Hanson, M.R., (2003) Microfilaments and microtubules control the morphology and movement of non-green plastids and stromules in Nicotiana tabacum. Plant J. 35, 16-26. (Pubitemid 36821101)
40. Kwok, E.Y., and, Hanson, M.R., (2004a) GFP-labelled Rubisco and aspartate aminotransferase are present in plastid stromules and traffic between plastids. J Exp Bot. 55, 595-604. (Pubitemid 38335059)
41. Kwok, E.Y., and, Hanson, M.R., (2004b) Stromules and the dynamic nature of plastid morphology. J. Microsc. 214, 124-137. (Pubitemid 38553610)
42. Laemmli, U.K., (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
43. Lewis, P.J., Thaker, S.D., and, Errington, J., (2000) Compartmentalization of transcription and translation in Bacillus subtilis. EMBO J. 19, 710-718. (Pubitemid 30093744)
44. Llopis, P.M., Jackson, A.F., Sliusarenko, O., Surovtsev, I., Heinritz, J., Emonet, T., and, Jacobs-Wagner, C., (2010) Spatial organization of the flow of genetic information in bacteria. Nature, 466, 77-82.
45. Margulies, M.M., and, Michaels, A., (1974) Ribosomes bound to chloroplast membranes in Chlamydomonas reinhardtii. J. Cell Biol. 60, 65-77.
46. Margulies, M.M., and, Michaels, A., (1975) Free and membrane-bound polyribosomes in Chlamydomonas reinhardtii. Biochim. Biophys. Acta, 402, 297-308.
47. Mascarenhas, J., Weber, M.H., and, Graumann, P.L., (2001) Specific polar localization of ribosomes in Bacillus subtilis depends on active transcription. EMBO Rep. 2, 685-689. (Pubitemid 32798710)
48. Medgyesy, P., Fejes, E., and, Maliga, P., (1985) Interspecific chloroplast recombination in a Nicotiana somatic hybrid. Proc. Natl Acad. Sci. USA, 82, 6960-6964.
49. Millen, R.S., Olmstead, R.G., Adams, K.L., et al. (2001) Many parallel losses of infA from chloroplast DNA during angiosperm evolution with multiple independent transfers to the nucleus. Plant Cell, 13, 645-658. (Pubitemid 32265381)
50. Miller, O.L., Hamkalo, B.A., and, Thomas, C.A., (1970) Visualization of bacterial genes in action. Science, 169, 392-395.
51. Mühlbauer, S.K., and, Koop, H.-U., (2005) External control of transgene expression in tobacco plastids using the bacterial lac repressor. Plant J. 43, 941-946.
52. Natesan, S.K.A., Sullivan, J.A., and, Gray, J.C., (2005) Stromules: a characteristic cell-specific feature of plastid morphology. J Exp Bot. 56, 787-797. (Pubitemid 40428381)
53. Natesan, S.K.A., Sullivan, J.A., and, Gray, J.C., (2009) Myosin XI Is required for actin-associated movement of plastid stromules. Mol. Plant, 2, 1262-1272.
54. Newell, C.A., and, Gray, J.C., (2010) Binding of lac repressor-GFP fusion protein to lac operator sites inserted in the tobacco chloroplast genome examined by chromatin immunoprecipitation. Nucl. Acids Res. 38, e145.
55. Newell, C.A., Birch-Machin, I., Hibberd, J.M., and, Gray, J.C., (2003) Expression of green fluorescent protein from bacterial and plastid promoters in tobacco chloroplasts. Transgenic Res. 12, 631-634. (Pubitemid 37292450)
56. Niswender, K.D., Blackman, S.M., Rohde, L., Magnuson, M.A., and, Piston, D.W., (1995) Quantitative imaging of green fluorescent protein in cultured cells: comparison of microscopic techniques, used in fusion proteins and detection limits. J. Microsc. 180, 109-116.
57. Raab, S., Toth, Z., de Groot, C., Stamminger, T., and, Hoth, S., (2006) ABA-responsive RNA-binding proteins are involved in chloroplast and stromule function in Arabidopsis seedlings. Planta, 224, 900-914. (Pubitemid 44286380)
58. Ris, H., and, Plaut, W., (1962) Ultrastructure of DNA-containing areas in the chloroplast of Chlamydomonas. J. Cell Biol. 13, 383-391.
59. Robinow, C., and, Kellenberger, E., (1994) The bacterial nucleoid revisited. Microbiol. Rev. 58, 211-232.
60. Rokov-Plavec, J., Dulic, M., Duchene, A.-M., and, Weygand-Durasevic, I., (2008) Dual targeting of organellar seryl-tRNA synthetase to maize mitochondria and chloroplasts. Plant Cell Rep. 27, 1157-1168.
61. Sapir-Mir, M., Mett, A., Belausov, E., Tal-Meshulam, S., Frydman, A., Gidoni, D., and, Eyal, G., (2008) Peroxisomal localization of Arabidopsis isopentenyl diphosphate isomerases suggests that part of the plant isoprenoid mevalonic acid pathway is compartmentalized to peroxisomes. Plant Physiol. 148, 1219-1228. (Pubitemid 352847484)
62. Sato, N., Terasawa, K., Miyajima, K., and, Kabeya, Y., (2003) Organization, developmental dynamics and evolution of the plastid nucleoid. Int. Rev. Cytol. 232, 217-262. (Pubitemid 38009987)
63. Sattarzadeh, A., Krahmer, J., Germain, A.D., and, Hanson, M.R., (2009) A myosin XI tail domain homologous to the yeast myosin vacuole-binding domain interacts with plastids and stromules in Nicotiana benthamiana. Mol. Plant, 2, 1351-1358.
64. Schattat, M.H., Barton, K., Baudisch, B., Klossgen, R.B., and, Mathur, J., (2011) Plastid stromule branching coincides with contiguous ER dynamics. Plant Physiol. 155, 1667-1677.
65. Shen, W.J., and, Forde, B.G., (1989) Efficient transformation of Agrobacterium spp by high voltage electroporation. Nucl. Acids Res. 17, 8385.
66. Shu, X., Lev-Ram, V., Deerinck, T.J., Qi, Y., Ramko, E.B., Davidson, M.W., Jin, Y., Ellisman, M.H., and, Tsien, R.Y., (2011) A genetically encoded tag for correlated light and electron microscopy of intact cells, tissues, and organisms. PLoS Biol. 9, e1001041.
67. Stewart, G.S.A.B., Lubinsky-Mink, S., Jackson, C.G., Cassel, A., and, Kuhn, J., (1987) pHG165: a pBR322 copy number derivative of pUC8. Plasmid, 15, 172-181.
68. Suppanz, I., Sanighausen, E., and, Reske, R., (2007) An integrated physiological and genetic approach to the dynamics of FtsZ targeting and organisation in a moss, Physcomitrella patens. Protoplasma, 232, 1-9.
69. Tao, K.-L., and, Jagendorf, A.T., (1973) The ratio of free to membrane-bound chloroplast ribosomes. Biochim. Biophys. Acta, 324, 518-522.
70. Terasawa, K., and, Sato, N., (2005) Visualization of plastid nucleoids in situ using the PEND-GFP fusion protein. Plant Cell Physiol. 46, 649-660. (Pubitemid 40640939)
71. Than, N.D., and, Medgyesy, P., (1989) Limited chloroplast gene transfer via recombination overcomes plastome-genome incompatibility between Nicotiana tabacum and Solanum tuberosum. Plant Mol. Biol. 12, 87-93.
72. Tirlapur, U.K., Dahse, I., Reiss, B., Meurer, J., and, Oelmüller, R., (1999) Characterization of the activity of a plastid-targeted green fluorescent protein in Arabidopsis. Eur. J. Cell Biol. 78, 233-240. (Pubitemid 29201645)
73. Tobin, E.M., (1997) Renewing an old view of chloroplasts. Trends Plant Sci. 2, 405-406.
74. Tsien, R.Y., (1998) The green fluorescent protein. Annu. Rev. Biochem. 67, 509-544. (Pubitemid 28411137)
75. Valvekens, D., van Montagu, M., and, van Lijsebettens, M., (1988) Agrobacterium tumefaciens-mediated transformation of Arabidopsis thaliana root explants by using kanamycin selection. Proc. Natl Acad. Sci. USA, 85, 5536-5540.
76. Vitha, S., McAndrew, R.S., and, Osteryoung, K.W., (2001) FtsZ ring formation at chloroplast division sites in plants. J. Cell Biol. 153, 111-119. (Pubitemid 34280198)
77. Waters, M.T., Fray, R.G., and, Pyke, K.A., (2004) Stromule formation is dependent upon plastid size, plastid differentiation status and the density of plastids within the cell. Plant J. 39, 655-667. (Pubitemid 39081497)
78. Wildman, S.G., Hongladarom, T., and, Honda, S.I., (1962) Chloroplasts and mitochondria in living plant cells: cine photomicrographic studies. Science, 138, 434-436.
79. Yamamoto, T., Burke, J., Autz, G., and, Jagendorf, A.T., (1981) Bound ribosomes of pea chloroplast thylakoid membranes: location and release in vitro by high salt, puromycin, and RNase. Plant Physiol. 67, 940-949.