Versatile roles of plastids in plant growth and development

Plant and Cell Physiology

Volumn 51, Issue 11, 2010, Pages 1847-1853

  Inaba, Takehito ^a   Ito Inaba, Yasuko ^a  

^a UNIVERSITY OF MIYAZAKI   (Japan)

Author keywords

Plastids

Indexed keywords

ARTICLE; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHOTOSYNTHESIS; PLANT; PLANT SEED; PLASTID; PRENATAL DEVELOPMENT; SIGNAL TRANSDUCTION;

PHOTOSYNTHESIS; PLANTS; PLASTIDS; SEEDS; SIGNAL TRANSDUCTION;

EID: 78349260838     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcq147     Document Type: Article

References (90)

1. Apuya, N.R., Yadegari, R., Fischer, R.L., Harada, J.J., Zimmerman, J.L. and Goldberg, R.B. (2001) The Arabidopsis embryo mutant schlepperless has a defect in the chaperonin-60alpha gene. Plant Physiol. 126:717-730.
2. Archibald, J.M. (2009) The puzzle of plastid evolution. Curr. Biol. 1 9 : R81-R88.
3. Artus, N.N., Uemura, M., Steponkus, P.L., Gilmour, S.J., Lin, C. and Thomashow, M.F. (1996) Constitutive expression of the cold-regulated Arabidopsis thaliana COR15a gene affects both chloroplast and protoplast freezing tolerance. Proc. Natl Acad. Sci. USA 9 3 :13404-13409.
4. Baldwin, A., Wardle, A., Patel, R., Dudley, P., Park, S.K., Twell, D., et al. (2005) A molecular-genetic study of the Arabidopsis Toc75 gene family. Plant Physiol. 138:715-733.
5. Banba, M., Gutjahr, C., Miyao, A., Hirochika, H., Paszkowski, U., Kouchi, H., et al. (2008) Divergence of evolutionary ways among common sym genes: CASTOR and CCaMK show functional conservation between two symbiosis systems and constitute the root of a common signaling pathway. Plant Cell Physiol. 4 9 :1659-1671.
6. Bauer, J., Chen, K., Hiltbunner, A., Wehrli, E., Eugster, M., Schnell, D., et al. (2000) The major protein import receptor of plastids is essential for chloroplast biogenesis. Nature 403:203-207.
7. Berg, M., Rogers, R., Muralla, R. and Meinke, D. (2005) Requirement of aminoacyl-tRNA synthetases for gametogenesis and embryo development in Arabidopsis. Plant J. 44: 866-878.
8. Budziszewski, G.J., Lewis, S.P., Glover, L.W., Reineke, J., Jones, G., Ziemnik, L.S., et al. (2001) Arabidopsis genes essential for seedling viability: isolation of insertional mutants and molecular cloning. Genetics 159:1765-1778.
9. Carol, P., Stevenson, D., Bisanz, C., Breitenbach, J., Sandmann, G., Mache, R., et al. (1999) Mutations in the Arabidopsis gene IMMUTANS cause a variegated phenotype by inactivating a chloroplast terminal oxidase associated with phytoene desaturation. Plant Cell 11:57-68.
10. Charpentier, M., Bredemeier, R., Wanner, G., Takeda, N., Schleiff, E. and Parniske, M. (2008) Lotus japonicus CASTOR and POLLUX are ion channels essential for perinuclear calcium spiking in legume root endosymbiosis. Plant Cell 20:3467-3479.
11. Chase, C.D. (2007) Cytoplasmic male sterility: a window to the world of plant mitochondrial-nuclear interactions. Trends Genet 23:81-90.
12. Chen, J., Burke, J.J., Velten, J. and Xin, Z. (2006) FtsH11 protease plays a critical role in Arabidopsis thermotolerance. Plant J. 48:73-84.
13. Chen, M., Choi, Y., Voytas, D.F. and Rodermel, S. (2000) Mutations in the Arabidopsis VAR2 locus cause leaf variegation due to the loss of a chloroplast FtsH protease. Plant J. 22:303-313.
14. Chen, Y., Asano, T., Fujiwara, M.T., Yoshida, S., Machida, Y. and Yoshioka, Y. (2009) Plant cells without detectable plastids are generated in the crumpled leaf mutant of Arabidopsis thaliana. Plant Cell Physiol. 50:956-969.
15. Chou, M.L., Fitzpatrick, L.M., Tu, S.L., Budziszewski, G., Potter-Lewis, S., Akita, M., et al. (2003) Tic40, a membrane-anchored co-chaperone homolog in the chloroplast protein translocon. EMBO J. 2 2 :2970-2980.
16. Dyall, S.D., Brown, M.T. and Johnson, P.J. (2004) Ancient invasions: from endosymbionts to organelles. Science 304:253-257.
17. Ferro, M., Salvi, D., Brugiere, S., Miras, S., Kowalski, S., Louwagie, M., et al. (2003) Proteomics of the chloroplast envelope membranes from Arabidopsis thaliana. Mol. Cell Proteomics 2:325-345.
18. Fitter, D.W., Martin, D.J., Copley, M.J., Scotland, R.W. and Langdale, J.A. (2002) GLK gene pairs regulate chloroplast development in diverse plant species. Plant J. 31:713-727.
19. Fourrier, N., Bedard, J., Lopez-Juez, E., Barbrook, A., Bowyer, J., Jarvis, P., et al. (2008) A role for SENSITIVE TO FREEZING2 in protecting chloroplasts against freeze-induced damage in Arabidopsis. Plant J. 55:734-745.
20. Friso, G., Giacomelli, L., Ytterberg, A.J., Peltier, J.B., Rudella, A., Sun, Q., et al. (2004) In-depth analysis of the thylakoid membrane proteome of Arabidopsis thaliana chloroplasts: new proteins, new functions, and a plastid proteome database. Plant Cell 16:478-499.
21. Froehlich, J.E., Wilkerson, C.G., Ray, W.K., McAndrew, R.S., Osteryoung, K.W., Gage, D.A., et al. (2003) Proteomic study of the Arabidopsis thaliana chloroplastic envelope membrane utilizing alternatives to traditional two-dimensional electrophoresis. J. Proteome Res. 2:413-425.
22. Fujii, S. and Toriyama, K. (2008a) DCW11, down-regulated gene 11 in CW-type cytoplasmic male sterile rice, encoding mitochondrial protein phosphatase 2c is related to cytoplasmic male sterility. Plant Cell Physiol. 49:633-640.
23. Fujii, S. and Toriyama, K. (2008b) Genome barriers between nuclei and mitochondria exemplified by cytoplasmic male sterility. Plant Cell Physiol. 49:1484-1494.
24. Fujii, S., Yamada, M. and Toriyama, K. (2009) Cytoplasmic male sterility-related protein kinase, OsNek3, is regulated downstream of mitochondrial protein phosphatase 2C, DCW11. Plant Cell Physiol. 50:828-837.
25. Giraud, E., Van Aken, O., Ho, L.H. and Whelan, J. (2009) The transcription factor ABI4 is a regulator of mitochondrial retrograde expression of ALTERNATIVE OXIDASE1a. Plant Physiol. 150:1286-1296.
26. Glynn, J.M., Froehlich, J.E. and Osteryoung, K.W. (2008) Arabidopsis ARC6 coordinates the division machineries of the inner and outer chloroplast membranes through interaction with PDV2 in the intermembrane space. Plant Cell 20:2460-2470.
27. Glynn, J.M., Miyagishima, S.Y., Yoder, D.W., Osteryoung, K.W. and Vitha, S. (2007) Chloroplast division. Traffic 8:451-461.
28. Homi, S., Takechi, K., Tanidokoro, K., Sato, H., Takio, S. and Takano, H. (2009) The peptidoglycan biosynthesis genes MurA and MraY are related to chloroplast division in the moss Physcomitrella patens. Plant Cell Physiol. 50:2047-2056.
29. Horiguchi, G., Kodama, H. and Iba, K. (2003) Mutations in a gene for plastid ribosomal protein S6-like protein reveal a novel developmental process required for the correct organization of lateral root meristem in Arabidopsis. Plant J. 33:521-529.
30. Hsu, S.C., Belmonte, M.F., Harada, J.J. and Inoue, K. (2010) Indispensable roles of plastids in Arabidopsis thaliana embryogenesis. Curr. Genomics 11:338-349.
31. Imaizumi-Anraku, H., Takeda, N., Charpentier, M., Perry, J., Miwa, H., Umehara, Y., et al. (2005) Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots. Nature 433:527-531.
32. Inaba, T. (2010) Bilateral communication between plastid and the nucleus: plastid protein import and plastid-to-nucleus retrograde signaling. Biosci. Biotechnol. Biochem. 74:471-476.
33. Inaba, T., Alvarez-Huerta, M., Li, M., Bauer, J., Ewers, C., Kessler, F., et al. (2005) Arabidopsis tic110 is essential for the assembly and function of the protein import machinery of plastids. Plant Cell 1 7 :1482-1496.
34. Inaba, T. and Schnell, D.J. (2008) Protein trafficking to plastids: one theme, many variations. Biochem. J. 413:15-28.
35. Ishikawa, M., Fujiwara, M., Sonoike, K. and Sato, N. (2009) Orthogenomics of photosynthetic organisms: bioinformatic and experimental analysis of chloroplast proteins of endosymbiont origin in Arabidopsis and their counterparts in Synechocystis. Plant Cell Physiol. 50:773-788.
36. Jarvis, P. (2008) Targeting of nucleus-encoded proteins to chloroplasts in plants. New Phytol. 179:257-285.
37. Jarvis, P., Chen, L.-J., Li, H., Peto, C.A., Fankhauser, C. and Chory, J. (1998) An Arabidopsis mutant defective in the plastid general protein import apparatus. Science 282:100-103.
38. Kakizaki, T., Matsumura, H., Nakayama, K., Che, F.S., Terauchi, R. and Inaba, T. (2009) Coordination of plastid protein import and nuclear gene expression by plastid-to-nucleus retrograde signaling. Plant Physiol. 151:1339-1353.
39. Kanervo, E., Singh, M., Suorsa, M., Paakkarinen, V., Aro, E., Battchikova, N., et al. (2008) Expression of protein complexes and individual proteins upon transition of etioplasts to chloroplasts in pea (Pisum sativum). Plant Cell Physiol. 49:396-410.
40. Kazama, T., Nakamura, T., Watanabe, M., Sugita, M. and Toriyama, K. (2008) Suppression mechanism of mitochondrial ORF79 accumulation by Rf1 protein in BT-type cytoplasmic male sterile rice. Plant J. 55:619-628.
41. Kessler, F. and Schnell, D. (2009) Chloroplast biogenesis: diversity and regulation of the protein import apparatus. Curr. Opin. Cell Biol. 2 1 :494-500.
42. Kim, C., Meskauskiene, R., Apel, K. and Laloi, C. (2008) No single way to understand singlet oxygen signalling in plants. EMBO Rep. 9:435-439.
43. Kim, J., Rudella, A., Ramirez Rodriguez, V., Zybailov, B., Olinares, P.D., and Van Wijk, K.J. (2009) Subunits of the plastid ClpPR protease complex have differential contributions to embryogenesis, plastid biogenesis, and plant development in Arabidopsis. Plant Cell 2 1 :1669-1692.
44. Kiss, J.Z., Hertel, R. and Sack, F.D. (1989) Amyloplasts are necessary for full gravitropic sensitivity in roots of Arabidopsis thaliana. Planta 177:198-206.
45. Kitajima, A., Asatsuma, S., Okada, H., Hamada, Y., Kaneko, K., Nanjo, Y., et al. (2009) The rice α -amylase glycoprotein is targeted from the Golgi apparatus through the secretory pathway to the plastids. Plant Cell 21:2844-2858.
46. Kleffmann, T., Russenberger, D., von Zychlinski, A., Christopher, W., Sjolander, K., Gruissem, W., et al. (2004) The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions. Curr. Biol. 14:354-362.
47. Kobayashi, K., Kondo, M., Fukuda, H., Nishimura, M. and Ohta, H. (2007) Galactolipid synthesis in chloroplast inner envelope is essential for proper thylakoid biogenesis, photosynthesis, and embryogenesis. Proc. Natl Acad. Sci. USA 104:17216-17221.
48. Koussevitzky, S., Nott, A., Mockler, T.C., Hong, F., Sachetto-Martins, G., Surpin, M., et al. (2007) Signals from chloroplasts converge to regulate nuclear gene expression. Science 316:715-719.
49. Kovacheva, S., Bedard, J., Patel, R., Dudley, P., Twell, D., Rios, G., et al. (2005) In vivo studies on the roles of Tic110, Tic40 and Hsp93 during chloroplast protein import. Plant J. 41:412-428.
50. Lee, U., Rioflorido, I., Hong, S.W., Larkindale, J., Waters, E.R. and Vierling, E. (2007) The Arabidopsis ClpB/Hsp100 family of proteins: chaperones for stress and chloroplast development. Plant J. 49:115-127.
51. Li, H.M. and Chiu, C.C. (2010) Protein transport into chloroplasts. Annu. Rev. Plant Biol. 61:157-180.
52. Machida, M., Takechi, K., Sato, H., Chung, S.J., Kuroiwa, H., Takio, S., et al. (2006) Genes for the peptidoglycan synthesis pathway areessential for chloroplast division in moss. Proc. Natl Acad. Sci. USA 103:6753-6758.
53. Masuda, S., Mizusawa, K., Narisawa, T., Tozawa, Y., Ohta, H. and Takamiya, K. (2008) The bacterial stringent response, conserved in chloroplasts, controls plant fertilization. Plant Cell Physiol. 4 9 :135-141.
54. Miras, S., Salvi, D., Piette, L., Seigneurin-Berny, D., Grunwald, D., Reinbothe, C., et al. (2007) Toc159- and Toc75-independent import of a transit sequence-less precursor into the inner envelope of chloroplasts. J. Biol. Chem. 282:29482-29492.
55. Miyagishima, S.Y., Froehlich, J.E. and Osteryoung, K.W. (2006) PDV1 and PDV2 mediate recruitment of the dynamin-related protein ARC5 to the plastid division site. Plant Cell 18:2517-2530.
56. Morita, M.T. (2010) Directional gravity sensing in gravitropism. Annu. Rev. Plant Biol. 61:705-720.
57. Morita, M.T. and Tasaka, M. (2004) Gravity sensing and signaling. Curr. Opin. Plant Biol. 7:712-718.
58. Munoz-Bertomeu, J., Cascales-Minana, B., Mulet, J.M., Baroja-Fernandez, E., Pozueta-Romero, J., Kuhn, J.M., et al. (2009) Plastidial glyceraldehyde-3-phosphate dehydrogenase deficiency leads to altered root development and affects the sugar and amino acid balance in Arabidopsis. Plant Physiol. 151:541-558.
59. Myouga, F., Akiyama, K., Motohashi, R., Kuromori, T., Ito, T., Iizumi, H., et al. (2010) The Chloroplast Function Database: a large-scale collection of Arabidopsis Ds/Spm- or T-DNA-tagged homozygous lines for nuclear-encoded chloroplast proteins, and their systematic phenotype analysis. Plant J. 61:529-542.
60. Myouga, F., Motohashi, R., Kuromori, T., Nagata, N. and Shinozaki, K. (2006) An Arabidopsis chloroplast-targeted Hsp101 homologue, APG6, has an essential role in chloroplast development as well as heat-stress response. Plant J. 48:249-260.
61. Nada, A. and Soll, J. (2004) Inner envelope protein 32 is imported into chloroplasts by a novel pathway. J. Cell Sci. 117:3975-3982.
62. Nakamura, H., Muramatsu, M., Hakata, M., Ueno, O., Nagamura, Y., Hirochika, H.,etal.(2009) Ectopic overexpressionofthe transcription factor OsGLK1 induces chloroplast development in non-green rice cells. Plant Cell Physiol. 50:1933-1949.
63. Nakayama, K., Okawa, K., Kakizaki, T., Honma, T., Itoh, H. and Inaba, T. (2007) Arabidopsis Cor15am is a chloroplast stromal protein that has cryoprotective activity and forms oligomers. Plant Physiol. 144:513-523.
64. Nanjo, Y., Oka, H., Ikarashi, N., Kaneko, K., Kitajima, A., Mitsui, T., et al. (2006) Rice plastidial N-glycosylated nucleotide pyrophosphatase/ phosphodiesterase is transported from the ER-golgi to the chloroplast through the secretory pathway. Plant Cell 18:2582-2592.
65. Okawa, K., Nakayama, K., Kakizaki, T., Yamashita, T. and Inaba, T. (2008) Identification and characterization of Cor413im proteins as novel components of the chloroplast inner envelope. Plant Cell Environ. 31:1470-1483.
66. Osteryoung, K.W., Stokes, K.D., Rutherford, S.M., Percival, A.L. and Lee, W.Y. (1998) Chloroplast division in higher plants requires members of two functionally divergent gene families with homology to bacterial ftsZ. Plant Cell 10:1991-2004.
67. Packer, L. and Douce, R. (eds) (1987) Plant Cell Membranes. Methods Enzymol. 148
68. Sakakibara, H., Kasahara, H., Ueda, N., Kojima, M., Takei, K., Hishiyama, S., et al. (2005) Agrobacterium tumefaciens increases cytokinin production in plastids by modifying the biosynthetic pathway in the host plant. Proc. Natl Acad. Sci. USA 102:9972-9977.
69. Sakamoto, W. (2003) Leaf-variegated mutations and their responsible genes in Arabidopsis thaliana. Genes Genet Syst. 78:1-9.
70. Sakamoto, W., Miyagishima, S.Y. and Jarvis, P. (2008) Chloroplast biogenesis: control of plastid development, protein import, division and inheritance. In The Arabidopsis Book. doi: 10.1199/tab.0110. American Society of Plant Biologists, Rockville, MD.
71. Sakamoto, W., Tamura, T., Hanba-Tomita, Y. and Murata, M. (2002) The VAR1 locus of Arabidopsis encodes a chloroplastic FtsH and is responsible for leaf variegation in the mutant alleles. Genes Cells 7 :769-780.
72. Sakamoto, W., Uno, Y., Zhang, Q., Miura, E., Kato, Y. and Sodmergen (2009) Arrested differentiation of proplastids into chloroplasts in variegated leaves characterized by plastid ultrastructure and nucleoid morphology. Plant Cell Physiol. 50:2069-2083.
73. Soll, J. and Schleiff, E. (2004) Protein import into chloroplasts. Nat. Rev. Mol. Cell Biol. 5:198-208.
74. Staehelin, L.A. and Newcomb, E.H. (2000) Membrane structure and membrane organelles. In Biochemistry and Molecular Biology of Plants. Edited by Buchanan, B.B., Gruissem, W. and Jones, R.L. pp. 2-50. American Society of Plant Physiologists, Rockville, MD.
75. Stanga, J.P., Boonsirichai, K., Sedbrook, J.C., Otegui, M.S. and Masson, P.H. (2009) A role for the TOC complex in Arabidopsis root gravitropism. Plant Physiol. 149:1896-1905.
76. Su, P.H. and Li, H.M. (2008) Arabidopsis stromal 70-kD heat shock proteins are essential for plant development and important for thermotolerance of germinating seeds. Plant Physiol. 146:1231-1241.
77. Sweetlove, L.J., Lytovchenko, A., Morgan, M., Nunes-Nesi, A., Taylor, N.L., Baxter, C.J., et al. (2006) Mitochondrial uncoupling protein is required for efficient photosynthesis. Proc. Natl Acad. Sci. USA 103:19587-19592.
78. Takano, H. and Takechi, K. (2010) Plastid peptidoglycan. Biochim. Biophys. Acta 1800:144-151.
79. Takechi, K., Sodmergen, Murata, M., Motoyoshi, F. and Sakamoto, W. (2000) The YELLOW VARIEGATED (VAR2) locus encodes a homologue of FtsH, an ATP-dependent protease in Arabidopsis. Plant Cell Physiol. 41:1334-1346.
80. Tang, L.Y., Nagata, N., Matsushima, R., Chen, Y., Yoshioka, Y. andSakamoto, W. (2009) Visualization of plastids in pollen grains:involvement of FtsZ1 in pollen plastid division. Plant Cell Physiol. 5 0 :904-908.
81. Villarejo, A., Buren, S., Larsson, S., Dejardin, A., Monne, M., Rudhe, C.,et al. (2005) Evidence for a protein transported through the secretorypathway en route to the higher plant chloroplast. Nat. Cell Biol. 7 :1224-1231.
82. Vitha, S., Yang, M., Sack, F.D. and Kiss, J.Z. (2007) Gravitropism inthe starch excess mutant of Arabidopsis thaliana. Amer. J. Bot. 9 4 :590-598.
83. Waters, M.T. and Langdale, J.A. (2009) The making of a chloroplast. EMBO J. 28:2861-2873.
84. Waters M.T. Wang P. Korkaric M. Capper R.G. Saunders, N.J.and Langdale, J.A. (2009) GLK transcription factors coordinateexpression of the photosynthetic apparatus in Arabidopsis. PlantCell 21 1109-1128.
85. Woodson, J.D. and Chory, J. (2008) Coordination of gene expressionbetween organellar and nuclear genomes. Nat. Rev. Genet. 9:383-395.
86. Wu, D., Wright, D.A., Wetzel, C., Voytas, D.F. and Rodermel, S. (1999)The IMMUTANS variegation locus of Arabidopsis defines amitochondrial alternative oxidase homolog that functions duringearly chloroplast biogenesis. Plant Cell 11:43-55.
87. Yang, Y., Glynn, J.M., Olson, B.J., Schmitz, A.J. and Osteryoung, K.W.(2008) Plastid division: across time and space. Curr. Opin. Plant Biol.11:577-584.
88. Yoshida, K., Watanabe, C., Kato, Y., Sakamoto, W. and Noguchi, K.(2008) Influence of chloroplastic photo-oxidative stress on mitochondrial alternative oxidase capacity and respiratoryproperties: a case study with Arabidopsis yellow variegated 2. PlantCell Physiol. 49:592-603.
89. Yoshida, Y., Kuroiwa, H., Misumi, O., Yoshida, M., Ohnuma, M.,Fujiwara, T., et al. (2010) Chloroplasts divide by contraction ofa bundle of nanofilaments consisting of polyglucan. Science 329:949-953.
90. Yun, M.S. and Kawagoe, Y. (2009) Amyloplast division progressessimultaneously at multiple sites in the endosperm of rice. Plant CellPhysiol. 50:1617-1626.