FtsHi1/ARC1 is an essential gene in Arabidopsis that links chloroplast biogenesis and division

Plant Journal

Volumn 72, Issue 5, 2012, Pages 856-867

  Kadirjan Kalbach, Deena K ^a   Yoder, David W ^a,c   Ruckle, Michael E ^a,b,d   Larkin, Robert M ^a,b   Osteryoung, Katherine W ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b Michigan State University   (United States)

^c PROMEGA CORPORATION   (United States)

^d ETH ZURICH   (Switzerland)

Author keywords

Arabidopsis thaliana; chloroplast biogenesis; embryogenesis; FtsHi; plastid development; plastid division

Indexed keywords

ARABIDOPSIS THALIANA; CHLOROPLAST BIOGENESIS; EMBRYOGENESIS; FTSHI; PLASTID DEVELOPMENT; PLASTID DIVISION;

BIOSYNTHESIS; GENES; GENETIC ENGINEERING; PLANTS (BOTANY); PROTEINS;

CHLOROPHYLL;

ARABIDOPSIS PROTEIN; FTSH PROTEIN, ARABIDOPSIS; METALLOPROTEINASE;

ARABIDOPSIS; ARTICLE; CHLOROPLAST; ESSENTIAL GENE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; PLANT SEED; SEEDLING; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHLOROPLASTS; GENE EXPRESSION REGULATION, PLANT; GENES, ESSENTIAL; METALLOENDOPEPTIDASES; MUTATION; PLANTS, GENETICALLY MODIFIED; SEEDLING; SEEDS;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84870064045     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12001     Document Type: Article

References (69)

1. Bailey, S., Thompson, E., Nixon, P.J., Horton, P., Mullineaux, C.W., Robinson, C., and, Mann, N.H., (2002) A critical role for the Var2 FtsH homologue of Arabidopsis thaliana in the photosystem II repair cycle in vivo. J. Biol. Chem. 277, 2006-2011.
2. Block, M.A., Douce, R., Joyard, J., and, Rolland, N., (2007) Chloroplast envelope membranes: a dynamic interface between plastids and the cytosol. Photosynth. Res. 92, 225-244.
3. Bryant, N., Lloyd, J., Sweeney, C., Myouga, F., and, Meinke, D., (2011) Identification of nuclear genes encoding chloroplast-localized proteins required for embryo development in Arabidopsis. Plant Physiol. 155, 1678-1689.
4. 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.
5. Cline, K., and, Dabney-Smith, C., (2008) Plastid protein import and sorting: different paths to the same compartments. Curr. Opin. Plant Biol. 11, 585-592.
6. Clough, S.J., and, Bent, A.F., (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
7. Curtis, M.D., and, Grossniklaus, U., (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133, 462-469.
8. Edwards, K., Johnstone, C., and, Thompson, C., (1991) A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acids Res. 19, 1349.
9. El-Kafafi, E.-S., Karamoko, M., Pignot-Paintrand, I., Grunwald, D., Mandaron, P., Lerbs-Mache, S., and, Falconet, D., (2008) Developmentally regulated association of plastid division protein FtsZ1 with thylakoid membranes in Arabidopsis thaliana. Biochem. J. 409, 87-94.
10. Ellis, J.R., and, Leech, R.M., (1985) Cell size and chloroplast size in relation to chloroplast replication in light-grown wheat leaves. Planta, 165, 120-125.
11. Emanuelsson, O., Brunak, S., von Heijne, G., and, Nielsen, H., (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2, 953-971.
12. Ferro, M., Brugiere, S., Salvi, D., et al. (2010) AT-CHLORO, a comprehensive chloroplast proteome database with subplastidial localization and curated information on envelope proteins. Mol. Cell. Proteomics, 9, 1063-1084.
13. Friso, G., Giacomelli, L., Ytterberg, A.J., Peltier, J.B., Rudella, A., Sun, Q., and, van Wijk, K.J., (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.
14. Fujiwara, M.T., Nakamura, A., Itoh, R., Shimada, Y., Yoshida, S., and, Møller, S.G., (2004) Chloroplast division site placement requires dimerization of the ARC11/AtMinD1 protein in Arabidopsis. J. Cell Sci. 117, 2399-2410.
15. Gao, H., Kadirjan-Kalbach, D., Froehlich, J.E., and, Osteryoung, K.W., (2003) ARC5, a cytosolic dynamin-like protein from plants, is part of the chloroplast division machinery. Proc Natl Acad Sci USA, 100, 4328-4333.
16. Garcia-Lorenzo, M., Pruzinska, A., and, Funk, C., (2008) ATP-dependent proteases in the plant chloroplast. In ATP-Dependent Proteases (, Kutejova, E., ed). Kerala, India: Research Signpost, pp. 145-176.
17. Glynn, J.M., Miyagishima, S., Yoder, D.W., Osteryoung, K.W., and, Vitha, S., (2007) Chloroplast division. Traffic, 8, 451-461.
18. 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.
19. 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.
20. Inaba, T., Alvarez-Huerta, M., Li, M., Bauer, J., Ewers, C., Kessler, F., and, Schnell, D.J., (2005) Arabidopsis TIC110 is essential for the assembly and function of the protein import machinery of plastids. Plant Cell, 17, 1482-1496.
21. Ito, K., and, Akiyama, Y., (2005) Cellular functions, mechanism of action, and regulation of FtsH protease. Annu. Rev. Microbiol. 59, 211-231.
22. Jander, G., Norris, S.R., Rounsley, S.D., Bush, D.F., Levin, I.M., and, Last, R.L., (2002) Arabidopsis map-based cloning in the post-genome era. Plant Physiol. 129, 440-450.
23. Janska, H., Piechota, J., and, Kwasniak, M., (2010) ATP-dependent proteases in biogenesis and maintenance of plant mitochondria. Biochim. Biophys. Acta, 1797, 1071-1075.
24. Karata, K., Inagawa, T., Wilkinson, A.J., Tatsuta, T., and, Ogura, T., (1999) Dissecting the role of a conserved motif (the second region of homology) in the AAA family of ATPases. Site-directed mutagenesis of the ATP-dependent protease FtsH. J. Biol. Chem. 274, 26225-26232.
25. 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.
26. Koo, A.J., and, Ohlrogge, J.B., (2002) The predicted candidates of Arabidopsis plastid inner envelope membrane proteins and their expression profiles. Plant Physiol. 130, 823-836.
27. Kovacheva, S., Bedard, J., Patel, R., Dudley, P., Twell, D., Rios, G., Koncz, C., and, Jarvis, P., (2005) In vivo studies on the roles of Tic110, Tic40 and Hsp93 during chloroplast protein import. Plant J. 41, 412-428.
28. Leonhard, K., Stiegler, A., Neupert, W., and, Langer, T., (1999) Chaperone-like activity of the AAA domain of the yeast Yme1 AAA protease. Nature, 398, 348-351.
29. Liu, X., Yu, F., and, Rodermel, S., (2010) Arabidopsis chloroplast FtsH, var2 and suppressors of var2 leaf variegation: a review. J. Integr. Plant Biol. 52, 750-761.
30. Mansfield, S.G., and, Briarty, L.G., (1991) Early embryogenesis in Arabidopsis thaliana. II. The developing embryo. Can. J. Bot. 69, 461-476.
31. Markwell, J., Osterman, J.C., and, Mitchell, J.L., (1995) Calibration of the Minolta SPAD-502 leaf chlorophyll meter. Photosynth. Res. 46, 467-472.
32. Marrison, J.L., Rutherford, S.M., Robertson, E.J., Lister, C., Dean, C., and, Leech, R.M., (1999) The distinctive roles of five different ARC genes in the chloroplast division process in Arabidopsis. Plant J. 18, 651-662.
33. 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.
34. Moldavski, O., Levin-Kravets, O., Ziv, T., Adam, Z., and, Prag, G., (2012) The hetero-hexameric nature of a chloroplast AAA+ FtsH protease contributes to its thermodynamic stability. PLoS ONE, 7, e36008.
35. Nakazawa, M., and, Matsui, M., (2003) Selection of hygromycin-resistant Arabidopsis seedlings. Biotechniques, 34, 28-30.
36. Neff, M.M., Turk, E., and, Kalishman, M., (2002) Web-based primer design for single nucleotide polymorphism analysis. Trends Genet. 18, 613-615.
37. Ogura, T., and, Wilkinson, A.J., (2001) AAA+ superfamily ATPases: common structure - diverse function. Genes Cells, 6, 575-597.
38. Ogura, T., Whiteheart, S.W., and, Wilkinson, A.J., (2004) Conserved arginine residues implicated in ATP hydrolysis, nucleotide-sensing, and inter-subunit interactions in AAA and AAA+ ATPases. J. Struct. Biol. 146, 106-112.
39. Okazaki, K., Kabeya, Y., Suzuki, K., Mori, T., Ichikawa, T., Matsui, M., Nakanishi, H., and, Miyagishima, S.Y., (2009) The PLASTID DIVISION1 and 2 components of the chloroplast division machinery determine the rate of chloroplast division in land plant cell differentiation. Plant Cell, 21, 1769-1780.
40. Ostersetzer, O., and, Adam, Z., (1997) Light-stimulated degradation of an unassembled Rieske FeS protein by a thylakoid-bound protease: the possible role of the FtsH protease. Plant Cell, 9, 957-965.
41. 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.
42. Piechota, J., Kolodziejczak, M., Juszczak, I., Sakamoto, W., and, Janska, H., (2010) Identification and characterization of high molecular weight complexes formed by matrix AAA proteases and prohibitins in mitochondria of Arabidopsis thaliana. J. Biol. Chem. 285, 12512-12521.
43. Pogson, B.J., and, Albrecht, V., (2011) Genetic dissection of chloroplast biogenesis and development: an overview. Plant Physiol. 155, 1545-1551.
44. Pyke, K.A., (1999) Plastid division and development. Plant Cell, 11, 549-556.
45. Pyke, K.A., and, Leech, R.M., (1991) Rapid image analysis screening procedure for identifying chloroplast number mutants in mesophyll cells of Arabidopsis thaliana (L.) Heynh. Plant Physiol. 96, 1193-1195.
46. Pyke, K.A., and, Leech, R.M., (1992) Chloroplast division and expansion is radically altered by nuclear mutations in Arabidopsis thaliana. Plant Physiol. 99, 1005-1008.
47. Pyke, K.A., and, Leech, R.M., (1994) A genetic analysis of chloroplast division and expansion in Arabidopsis thaliana. Plant Physiol. 104, 201-207.
48. Pyke, K.A., Rutherford, S.M., Robertson, E.J., and, Leech, R.M., (1994a) arc6, a fertile arabidopsis mutant with only two mesophyll cell chloroplasts. Plant Physiol. 106, 1169-1177.
49. Ruckle, M.E., Burgoon, L.D., Lawrence, L.A., Sinkler, C.A., and, Larkin, R.M., (2012) Plastids are major regulators of light signaling in Arabidopsis. Plant Physiol. 159, 366-390.
50. Sakamoto, W., (2006) Protein degradation machineries in plastids. Annu. Rev. Plant Biol. 57, 599-621.
51. Sakamoto, W., Zaltsman, A., Adam, Z., and, Takahashi, Y., (2003) Coordinated regulation and complex formation of yellow variegated1 and yellow variegated2, chloroplastic FtsH metalloproteases involved in the repair cycle of photosystem II in Arabidopsis thylakoid membranes. Plant Cell, 15, 2843-2855.
52. Sakamoto, W., Miura, E., Kaji, Y., Okuno, T., Nishizono, M., and, Ogura, T., (2004) Allelic characterization of the leaf-variegated mutation var2 identifies the conserved amino acid residues of FtsH that are important for ATP hydrolysis and proteolysis. Plant Mol. Biol. 56, 705-716.
53. Schmitz, A.J., Glynn, J.M., Olson, B.J., Stokes, K.D., and, Osteryoung, K.W., (2009) Arabidopsis FtsZ2-1 and FtsZ2-2 are functionally redundant, but FtsZ-based plastid division is not essential for chloroplast partitioning or plant growth and development. Mol. Plant, 2, 1211-1222.
54. Schwacke, R., Schneider, A., van der Graaff, E., Fischer, K., Catoni, E., Desimone, M., Frommer, W.B., Flugge, U.I., and, Kunze, R., (2003) ARAMEMNON, a novel database for Arabidopsis integral membrane proteins. Plant Physiol. 131, 16-26.
55. Shimada, H., Koizumi, M., Kuroki, K., Mochizuki, M., Fujimoto, H., Ohta, H., Masuda, T., and, Takamiya, K., (2004) ARC3, a chloroplast division factor, is a chimera of prokaryotic FtsZ and part of eukaryotic phosphatidylinositol-4- phosphate 5-kinase. Plant Cell Physiol. 45, 960-967.
56. Sokolenko, A., Pojidaeva, E., Zinchenko, V., Panichkin, V., Glaser, V.M., Herrmann, R.G., and, Shestakov, S.V., (2002) The gene complement for proteolysis in the cyanobacterium Synechocystis sp. PCC 6803 and Arabidopsis thaliana chloroplasts. Curr. Genet. 41, 291-310.
57. Vitha, S., McAndrew, R.S., and, Osteryoung, K.W., (2001) FtsZ ring formation at the chloroplast division site in plants. J. Cell Biol. 153, 111-119.
58. Vitha, S., Froehlich, J.E., Koksharova, O., Pyke, K.A., van Erp, H., and, Osteryoung, K.W., (2003) ARC6 is a J-domain plastid division protein and an evolutionary descendant of the cyanobacterial cell division protein Ftn2. Plant Cell, 15, 1918-1933.
59. Wagner, R., Aigner, H., and, Funk, C., (2012) FtsH proteases located in the plant chloroplast. Physiol. Plant. 145, 203-214.
60. Winter, D., Vinegar, B., Nahal, H., Ammar, R., Wilson, G.V., and, Provart, N.J., (2007) An "Electronic Fluorescent Pictograph" browser for exploring and analyzing large-scale biological data sets. PLoS ONE, 2, e718.
61. Wise, R.R., (2007) The diversity of plastid form and function. In The Structure and Function of Plastids, Advances in Photosynthesis and Respiration (, Wise, R.R., and, Hoober, J.K., eds). Dordrecht: Springer, pp. 3-26.
62. Wu, G.Z., and, Xue, H.W., (2010) Arabidopsis beta-ketoacyl-[acyl carrier protein] synthase is crucial for fatty acid synthesis and plays a role in chloroplast division and embryo development. Plant Cell, 22, 3726-3744.
63. Xu, C., Fan, J., Cornish, A.J., and, Benning, C., (2008) Lipid trafficking between the endoplasmic reticulum and the plastid in Arabidopsis requires the extraplastidic TGD4 protein. Plant Cell, 20, 2190-2204.
64. Yoder, D.W., Kadirjan-Kalbach, D., Olson, B.J., Miyagishima, S., Deblasio, S.L., Hangarter, R.P., and, Osteryoung, K.W., (2007) Effects of mutations in Arabidopsis FtsZ1 on plastid division, FtsZ ring formation and positioning, and FtsZ filament morphology in vivo. Plant Cell Physiol. 48, 775-791.
65. Yu, F., Park, S., and, Rodermel, S.R., (2004) The Arabidopsis FtsH metalloprotease gene family: interchangeability of subunits in chloroplast oligomeric complexes. Plant J. 37, 864-876.
66. Yu, F., Fu, A., Aluru, M., Park, S., Xu, Y., Liu, H., Liu, X., Foudree, A., Nambogga, M., and, Rodermel, S., (2007) Variegation mutants and mechanisms of chloroplast biogenesis. Plant, Cell Environ. 30, 350-365.
67. Zaltsman, A., Ori, N., and, Adam, Z., (2005) Two types of FtsH protease subunits are required for chloroplast biogenesis and Photosystem II repair in Arabidopsis. Plant Cell, 17, 2782-2790.
68. Zhang, M., Hu, Y., Jia, J., Li, D., Zhang, R., Gao, H., and, He, Y., (2009) CDP1, a novel component of chloroplast division site positioning system in Arabidopsis. Cell Res. 19, 877-886.
69. Zhang, D., Kato, Y., Zhang, L., Fujimoto, M., Tsutsumi, N., Sodmergen, and, Sakamoto, W., (2010) The FtsH protease heterocomplex in arabidopsis: dispensability of type-B protease activity for proper chloroplast development. Plant Cell, 22, 3710-3725.