Happy on norflurazon (hon) mutations implicate perturbance of plastid homeostasis with activating stress acclimatization and changing nuclear gene expression in norflurazon-treated seedlings

Plant Journal

Volumn 65, Issue 5, 2011, Pages 690-702

  Saini, Geetanjali ^a   Meskauskiene, Rasa ^a   Pijacka, Wioletta ^a   Roszak, Pawel ^a   Sjögren, Lars L E ^b   Clarke, Adrian K ^b   Straus, Marco ^c   Apel, Klaus ^a,c  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

^c United States Department of Agriculture Agricultural Research Service and Boyce Thompson Institute for Plant Research   (United States)

Author keywords

Arabidopsis; chloroplast; hon mutants; norflurazon; plastid homeostasis; retrograde signaling

Indexed keywords

ARABIDOPSIS; CHLOROPLAST; HON MUTANTS; NORFLURAZON; PLASTID HOMEOSTASIS; RETROGRADE SIGNALING;

CHLOROPHYLL; ENCODING (SYMBOLS); GENE ENCODING; PHYSIOLOGY; PROTEINS; SEED; SIGNALING;

GENE EXPRESSION;

NORFLURAZON; PLANT DNA; PYRIDAZINE DERIVATIVE;

ACCLIMATIZATION; ARABIDOPSIS; ARTICLE; CHLOROPLAST; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENETICS; HOMEOSTASIS; LIGHT HARVESTING SYSTEM; METABOLISM; MOLECULAR CLONING; MUTATION; OXIDATIVE STRESS; SEEDLING; SIGNAL TRANSDUCTION;

ACCLIMATIZATION; ARABIDOPSIS; CHLOROPLASTS; CLONING, MOLECULAR; DNA, PLANT; GENE EXPRESSION REGULATION, PLANT; GENETIC COMPLEMENTATION TEST; HOMEOSTASIS; LIGHT-HARVESTING PROTEIN COMPLEXES; MUTATION; OXIDATIVE STRESS; PYRIDAZINES; SEEDLING; SIGNAL TRANSDUCTION;

ARABIDOPSIS;

EID: 79952028134     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2010.04454.x     Document Type: Article

References (52)

1. Albrecht, V., Ingenfeld, A., and, Apel, K., (2006) Characterization of the snowy cotyledon 1 mutant of Arabidopsis thaliana: the impact of chloroplast elongation factor G on chloroplast development and plant vitality. Plant Mol. Biol. 60, 507-518. (Pubitemid 43363227)
2. Ankele, E., Kindgren, P., Pesquet, E., and, Strand, A., (2007) In vivo visualization of Mg-protoporphyrin IX, a coordinator of photosynthetic gene expression in the nucleus and the chloroplast. Plant Cell, 19, 1964-1979. (Pubitemid 47218852)
3. Ball, L., Accotto, G.P., Bechtold, U., et al. (2004) Evidence for a direct link between glutathione biosynthesis and stress defense gene expression in Arabidopsis. Plant Cell, 16, 2448-2462. (Pubitemid 39247084)
4. Baruah, A., Simkova, K., Apel, K., and, Laloi, C., (2009) Arabidopsis mutants reveal multiple singlet oxygen signaling pathways involved in stress response and development. Plant Mol. Biol. 70, 547-563.
5. Chamovitz, D., Pecker, I., and, Hirschberg, J., (1991) The molecular basis of resistance to the herbicide norflurazon. Plant Mol. Biol. 16, 967-974.
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. Cogdell, R.J., and, Frank, H.A., (1987) How carotenoids function in photosynthetic membranes. Biochim. Biophys. Acta, 895, 63-79.
8. Coll, N.S., Danon, A., Meurer, J., Cho, W.K., and, Apel, K., (2009) Characterization of soldat8, a suppressor of singlet oxygen-induced cell death in Arabidopsis seedlings. Plant Cell Physiol. 50, 707-718.
9. Danon, A., Miersch, O., Felix, G., op den Camp, R., and, Apel, K., (2005) Concurrent activation of cell death-regulating signaling pathways by singlet oxygen in Arabidopsis thaliana. Plant J. 41, 68-80.
10. Dietz, K.-J., (2003) Redox control, redox signaling and redox homeostasis in plant cells. Int. Rev. Cytol. 228, 141-193. (Pubitemid 37484734)
11. Gadjieva, R., Axelsson, E., Olsson, U., and, Hanson, M., (2005) Analysis of gun phenotype in barley magnesium chelatase and Mg-protoporphyrin IX monomethyl ester cyclase mutants. Plant Physiol. Biochem. 43, 901-908. (Pubitemid 41785445)
12. Goslings, D., Meskauskiene, R., Kim, C., Lee, K.P., Nater, M., and, Apel, K., (2004) Concurrent interactions of heme and FLU with Glut RNA reductase (HEMA1), the target of metabolic feedback inhibition of tetrapyrrole biosynthesis, in dark- and light-grown Arabidopsis plants. Plant J. 40, 957-967. (Pubitemid 40047634)
13. Heiber, I., Stroher, E., Raatz, B., Busse, I., Kahmann, U., Bevan, M.W., Dietz, K.-J., and, Baier, M., (2007) The redox imbalanced mutants of Arabidopsis differentiate signaling pathways for redox regulation of chloroplast antioxidant enzymes. Plant Physiol. 143, 1774-1788. (Pubitemid 46849486)
14. 2-mediated retrograde signaling during late embryogenesis predetermines plastid differentiation in seedlings by recruiting abscisic acid. Proc. Natl Acad. Sci. USA, 106, 9920-9924.
15. Koussevitzky, S., Nott, A., Mockler, T.C., Hong, F., Sachetto-Martins, G., Surpin, M., Lim, J., Mittler, R., and, Chory, J., (2007a) Signals from chloroplasts converge to regulate nuclear gene expression. Science, 316, 715-719. (Pubitemid 46717673)
16. Koussevitzky, S., Stanne, T.M., Peto, C.A., Giap, T., Sjögren, L.L., Zhao, Y., Clarke, A.K., and, Chory, J., (2007b) An Arabidopsis thaliana virescent mutant reveals a role for ClpR1 in plastid development. Plant Mol. Biol. 63, 85-96. (Pubitemid 44950234)
17. Krause, G.H., and, Weis, E., (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42, 313-349. (Pubitemid 21903935)
18. Laemmli, U.K., (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
19. Larkin, R.M., Alonso, J.M., Ecker, J.R., and, Chory, J., (2003) GUN4, a regulator of chlorophyll synthesis and intracellular signaling. Science, 299, 902-906. (Pubitemid 36182451)
20. Lichtenthaler, H.K., (1987) Chlorophyll and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol. 148, 331-382.
21. Liu, X., Yu, F., and, Rodermel, S., (2010) An Arabidopsis pentatricopeptide repeat protein, SUPPRESSOR OF VARIEGATION7, is required for FtsH-mediated chloroplast biogenesis. Plant Physiol. 154, 1588-1601.
22. Mayfield, S.-P., and, Taylor, W.C., (1984) Carotenoid-deficient maize seedlings fail to accumulate light-harvesting chlorophyll a/b binding protein (LHCP) mRNA. Eur. J. Biochem. 144, 79-84.
23. 2-induced cell death. Plant J. 60, 399-410.
24. Miura, E., Kato, Y., Matsushima, R., Albrecht, V., Laalami, S., and, Sakamoto, W., (2007) The balance between protein synthesis and degradation in chloroplasts determines leaf variegation in Arabidopsis yellow variegated mutants. Plant Cell, 19, 1313-1328. (Pubitemid 46941656)
25. Mochizuki, N., Tanaka, R., Tanaka, A., Masuda, T., and, Nagatani, A., (2008) The steady-state level of Mg-protoporphyrin IX is not a determinant of plastid-to-nucleus signaling in Arabidopsis. Proc. Natl Acad. Sci. USA, 105, 15184-15189.
26. Moulin, M., McCormac, A.C., Terry, M.J., and, Smith, A.G., (2008) Tetrapyrrole profiling in Arabidopsis seedlings reveals that retrograde plastid nuclear signaling is not due to Mg-protoporphyrin IX accumulation. Proc. Natl Acad. Sci. USA, 105, 15178-15183.
27. Norris, S.R., Barette, T.R., and, DellaPenna, D.C., (1995) Genetic dissection of carotenoid synthesis in Arabidopsis defines plastoquinone as an essential component of phytoene desaturation. Plant Cell, 7, 2139-2149. (Pubitemid 2615572)
28. Nott, A., Jung, H.-S., Koussevitzky, S., and, Chory, J., (2006) Plastid-to-nucleus retrograde signaling. Annu. Rev. Plant Biol. 57, 739-759. (Pubitemid 44061043)
29. Owens, R.M., Pritchard, G., Skipp, P., Hodey, M., Connell, S.R., Nierhaus, K.H., and, OConnor, C.D., (2004) A dedicated translation factor controls the synthesis of the global regulator Fis. EMBO J. 23, 3375-3385. (Pubitemid 39209161)
30. Park, S., and, Rodermel, S.R., (2004) Mutations in ClpC2/Hsp100 suppress the requirement for Ftsh in thylakoid membrane biogenesis. Proc. Natl Acad. Sci. USA, 101, 12765-12770. (Pubitemid 39122097)
31. Peltier, J.B., Ripoll, D.R., Friso, G., Rudella, A., Cai, Y., Yttterberg, A.J., Giacomelli, L., Pillardy, J., and, van Wijk, K.J., (2004) Clp protease complexes from photosynthetic and non-photosynthetic plasids and mitochondria of plants, their predicted three-dimensional structures, and functional implications. J. Biol. Chem. 279, 4768-4781. (Pubitemid 38199072)
32. Pfannschmidt, T., (2003) Chloroplast redox signals: how photosynthesis controls its own genes. Trends Plant Sci. 8, 33-41. (Pubitemid 36725965)
33. Plumley, F.G., and, Schmidt, G.W., (1987) Reconstitution of chlorophyll a/b light-harvesting complexes: xanthophyll-dependent assembly and energy transfer. Proc. Natl Acad. Sci. USA, 84, 146-150.
34. Rebeiz, C.A., Montazer-Zouhoor, A., Mayasich, J.M., Tripathy, B.C., Wu, S.-M., and, Rebeiz, C., (1988) Photodynamic herbicides. Recent developments and molecular basis of selectivity. CRC Crit. Rev. Plant Sci. 6, 385-436.
35. Reinsberg, D., Ottmann, K., Booth, P.J., and, Paulsen, H., (2001) Effects of chlorophyll a, chlorophyll b, and xanthophylls on the in vitro assembly of the major light-harvesting chlorophyll a/b complex, LHCIIb. J. Mol. Biol. 308, 59-67. (Pubitemid 33027627)
36. Richly, E., Dietzmann, A., Biehl, A., Kurth, J., Laloi, C., Apel, K., Salamini, F., and, Leister, D., (2003) Covariations in the nuclear chloroplast transcriptome reveal a regulatory master-switch. EMBO Rep. 4, 491-498. (Pubitemid 36789848)
37. Rudella, A., Friso, G., Alonso, J.M., Ecker, J.R., and, van Wijk, K.J., (2006) Downregulation of ClpR2 leads to reduced accumulation of the ClpPRS protease complex and defects in chloroplast biogenesis in Arabidopsis. Plant Cell, 18, 1704-1721. (Pubitemid 44025554)
38. Runge, S., van Cleve, B., Lebedev, N., Armstrong, G., and, Apel, K., (1995) Isolation and classification of chlorophyll-deficient xantha mutants of Arabidopsis thaliana. Planta, 197, 490-500.
39. Schmidt, R., and, Mohr, H., (1981) Time-dependent changes in responsiveness to light of phytochrome-mediated anthocyanin synthesis. Plant Cell Environ. 4, 433-437.
40. Sjögren, L.L., Stanne, T.M., Zheng, B., Sutinen, S., and, Clarke, A.K., (2006) Structural and functional insights into the chloroplast ATP-dependent Clp protease in Arabidopsis. Plant Cell, 18, 2635-2649. (Pubitemid 44749894)
41. Smith, C.W., Chu, T.T., and, Nadal-Ginard, B., (1993) Scanning and competition between AGs are involved in 3 splice site selection in mammalian introns. Mol. Cell. Biol. 13, 4939-4952. (Pubitemid 23220399)
42. Stanne, T.M., Sjögren, L.L.E., Koussevitzky, S., and, Clarke, A.K., (2009) Identification of new protein substrates for the chloroplast ATP-dependent Clp protease supports its constitutive role in Arabidopsis. Biochem. J. 417, 257-268.
43. Strand, A., Asami, T., Alonso, J., Ecker, J.R., and, Chory, J., (2003) Chloroplast-to-nucleus communication triggered by accumulation of Mg-protoporphyrin IX. Nature, 421, 79-83. (Pubitemid 36077088)
44. Sullivan, J.A., and, Gray, J.C., (1999) Plastid translation is required for the expression of nuclear photosynthesis genes in the dark and in roots of the pea lip1 mutant. Plant Cell, 11, 901-910.
45. Surpin, M., Larkin, R.M., and, Chory, J., (2002) Signal transduction between the chloroplast and the nucleus. Plant Cell, 14, S327-S338. (Pubitemid 34609247)
46. Susek, R.E., Ausubel, F.M., and, Chory, J., (1993) Signal transduction mutants of Arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development. Cell, 74, 787-799. (Pubitemid 23270599)
47. Tatsuzawa, H., Maruyama, T., Misawa, N., Fujimori, K., and, Nakano, M., (2000) Quenching of singlet oxygen by carotenoids produced in Escherichia coli- attenuation of singlet oxygen-mediated bacterial killing by carotenoids. FEBS Lett. 484, 280-284.
48. Voigt, C., Oster, U., Boernke, F., Jahns, P., Dietz, K.-J., Leister, D., and, Kleine, T., (2010) In-depth analysis of the distinctive effects of norflurazon implies that tetrapyrrole biosynthesis, organellar gene expression and ABA cooperate in the GUN-type of plastid signaling. Physiol. Plant. 138, 503-519.
49. Wagner, D., Przybyla, D., op den Camp, R., et al. (2004) The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana. Science, 306, 1183-1185. (Pubitemid 39488997)
50. Wang, F., Zhong, N.Q., Gao, P., Wang, G.L., Wang, H.Y., and, Xia, G.X., (2008) SsTypA1, a chloroplast-specific TypA/BipA-type GTPase from the halophytic plant Suaeda salsa, plays a role in oxidative stress tolerance. Plant Cell Environ. 31, 982-994. (Pubitemid 351813367)
51. Yu, F., Liu, X., Alsheikh, M., Park, S., and, 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. (Pubitemid 352844533)
52. Zybailov, B., Friso, G., Kim, J., Rudella, A., Rodriguez, V.R., Asakura, Y., Sun, Q., and, van Wijk, K.J., (2009) Large scale comparative proteomics of a chloroplast Clp protease mutant reveals folding stress, altered protein homeostasis, and feedback regulation of metabolism. Mol. Cell Proteomics, 8, 1789-1810.