The radical induced cell death protein 1 (RCD1) supports transcriptional activation of genes for chloroplast antioxidant enzymes

Frontiers in Plant Science

Volumn 5, Issue , 2014, Pages

  Hiltscher, Heiko ^a   Rudnik, Radoslaw ^b   Shaikhali, Jehad ^c,d   Heiber, Isabelle ^c   Mellenthin, Marina ^a   Meirelles Duarte, Iuri ^a   Schuster, Günter ^a   Kahmann, Uwe ^c   Baier, Margarete ^a,b,c  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

^c BIELEFELD UNIVERSITY   (Germany)

^d SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

Antioxidant system; Arabidopsis; Chloroplast; RCD1; ROS

Indexed keywords

EID: 84907287478     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00475     Document Type: Article

References (55)

1. Ahlfors, R., Lang, S., Overmyer, K., Jaspers, P., Brosche, M., Tauriainen, A., et al. (2004). Arabidopsis RADICAL-INDUCED CELL DEATH1 belongs to the WWE protein-protein interaction domain protein family and modulates abscisic acid, ethylene, and methyl jasmonate responses. Plant Cell 16, 1925-1937. doi: 10.1105/tpc.021832
2. Armengaud, P., Zambaux, K., Hills, A., Sulpice, R., Pattison, R. J., Blatt, M. R., et al. (2009). EZ-Rhizo: Integrated software for the fast and accurate measurement of root system architecture. Plant J. 57, 945-956. doi: 10.1111/j.1365313X.2008.03739.x
3. Arvidsson, S., Kwasniewski, M., Riano-Pachon, D. M., and Mueller-Roeber, B. (2008). QuantPrime - A flexible tool for reliable high-throughput primer design for quantitative PCR. BMC Bioinformatics 9:465. doi: 10.1186/1471-2105-9-465
4. Ausubel, F. M., Berndt, K. D., and Holmgren, A. (2001). Current Protocol in Molecular Biology. New York, NY: Wiley. doi: 10.1002/0471142727
5. Baier, M., and Dietz, K.-J. (1999). The costs and benefits of oxygen for photosyn-thesizing plant cells. Prog. Bot. 60, 282-314. doi: 10.1007/978-3-642-59940-8_11
6. Baier, M., and Dietz, K.-J. (2005). Chloroplasts as source and target of cellular redox regulation: A discussion of chloroplast-to-nucleus signals in context of plant physiology and evolution. J. Exp. Bot. 56, 1449-1462. doi: 10.1093/jxb/eri161
7. Baier, M., Noctor, G., Foyer, C. H., and Dietz, K. J. (2000). Antisense suppression of 2-cysteine peroxiredoxin in Arabidopsis specifically enhances the activities and expression of enzymes associated with ascorbate metabolism but not glutathione metabolism. Plant Physiol. 124, 823-832. doi: 10.1104/pp.124.2.823
8. Baier, M., Ströher, E., and Dietz, K. J. (2004). The acceptor availability at photosystem I and ABA control nuclear expression of 2-Cys peroxiredoxin-A in Arabidopsis thaliana. Plant Cell Physiol. 45, 997-1006. doi: 10.1093/pcp/pch114
9. Baxter, A., Mittler, R., and Suzuki, N. (2014). ROS as key players in plant stress signalling. J. Exp. Bot. 65, 1229-1240. doi: 10.1093/jxb/ert375
10. Bechtold, U., Richard, O., Zamboni, A., Gapper, C., Geisler, M., Pogson, B., et al. (2008). Impact of chloroplastic- and extracellular-sourced ROS on high light-responsive gene expression in Arabidopsis. J. Exp. Bot. 59, 121-133. doi: 10.1093/jxb/erm289
11. Becker, B., Holtgrefe, S., Jung, S., Wunrau, C., Kandlbinder, A., Baier, M., et al. (2006). Influence of the photoperiod on redox regulation and stress responses in Arabidopsis thaliana L. (Heynh.) plants under long- and short-day conditions Planta 224, 380-393. doi: 10.1007/s00425-006-0222-3
12. Belles-Boix, E., Babiychuk, E., Van Montagu, M., Inze, D., and Kushnir, S. (2000). CEO1, a new protein fromArabidopsis thaliana, protects yeast against oxidative damage. FEBS Lett. 482, 19-24. doi: 10.1016/S0014-5793(00)02016-0
13. Cheng, J.-C., Seeley, K. A., and Sung, Z. R. (1995). RML1 and RML2, Arabidopsis genes required for cell proliferation at the root tip. Plant Physiol. 107, 365-376. doi: 10.1104/pp.107.2.365
14. Dominguez, E., Heredia-Guerrero, J. A., and Heredia, A. (2011). The biophysical design of plant cuticles: an overview. New Phytol. 189, 938-949. doi: 10.1111/j.1469-8137.2010.03553.x
15. Foyer, C. H., Lelandais, M., and Kunert, K. J. (1994). Photooxidative stress in plants. Physiol. Plant. 92, 696-717. doi: 10.1111/j.1399-3054.1994.tb03042.x
16. Foyer, C. H., and Noctor, G. (2005). Redox homeostasis and antioxidant signaling: A metabolic interface between stress perception and physiological responses. Plant Cell 17, 1866-1875. doi: 10.1105/tpc.105.033589
17. Fujibe, T., Saji, H., Arakawa, K., Yabe, N., Takeuchi, Y., and Yamamoto, K. T. (2004). A methyl viologen-resistant mutant of Arabidopsis, which is allelic to ozone-sensitive rcd1, is tolerant to supplemental ultraviolet-B irradiation. Plant Physiol. 134, 275-285. doi: 10.1104/pp.103.033480
18. Fujibe, T., Saji, H., Watahiki, M. K., and Yamamoto, K. T. (2006). Overexpression of the Radical-induced Cell Death 1 (Rcd1) Gene of Arabidopsis causes weak RCD1 phenotype with compromised oxidative-stress responses. Biosci. Biotechnol. Biochem. 70, 1827-1831.
19. Heiber, I., Ströher, E., Raatz, B., Busse, I., Kahmann, U., Bevan, M. W., et al. (2007). The redox imbalanced mutants of Arabidopsis differentiate signaling pathways for redox regulation of chloroplast antioxidant enzymes. Plant Physiol. 143, 1774-1788. doi: 10.1104/pp.106.093328
20. Horling, F., Lamkemeyer, P., König, J., Finkemeier, I., Kandlbinder, A., Baier, M., et al. (2003). Divergent light-, ascorbate-, and oxidative stress-dependent regulation of expression of the peroxiredoxin gene family in Arabidopsis. Plant Physiol. 131, 317-325. doi: 10.1104/pp.010017
21. 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. doi: 10.1104/pp.003533
22. Jaspers, P., Blomster, T., Brosché, M., Salojärvi, J., Ahlfors, R., Vainonen, J. P., et al. (2009). Unequally redundant RCD1 and SRO1 mediate stress and developmental responses and interact with transcription factors. Plant J. 60, 268-279. doi: 10.1111/j.1365-313X.2009.03951.x
23. Jaspers, P., Brosche, M., Overmyer, K., and Kangasjärvi, J. (2010). The transcription factor interacting protein RCD1 contains a novel conserved domain. Plant Signal. Behav. 5, 78-80. doi: 10.4161/psb.5.1.10293
24. Juszczak, I., Rudnik, R., Pietzenuk, B., and Baier, M. (2012). Natural genetic variation in the expression regulation of the chloroplast antioxidant system among Arabidopsis thaliana accessions. Physiol. Plant. 146, 53-70. doi: 10.1111/j.1399-3054.2012.01602.x
25. Kangasjärvi, S., Lepisto, A., Hannikainen, K., Piippo, M., Luomala, E. M., Aro, E. M., et al. (2008). Diverse roles for chloroplast stromal and thylakoid-bound ascorbate peroxidases in plant stress responses. Biochem. J. 412, 275-285. doi: 10.1042/BJ20080030
26. Karpinski, S., Escobar, C., Karpinska, B., Creissen, G., and Mullineaux, P. M. (1997). Photosynthetic electron transport regulates the expression of cytosolic ascorbate peroxidase genes in Arabidopsis excess light stress. Plant Cell 9, 627-640. doi: 10.1105/tpc.9.4.627
27. Katiyar-Agarwal, S., Zhu, J., Kim, K., Agarwal, M., Fu, X., Huang, A., et al. (2006). The plasma membrane Na+/H+ antiporter SOS1 interacts with RCD1 and functions in oxidative stress tolerance in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 103, 18816-18821. doi: 10.1073/pnas.0604711103
28. König, J., Baier, M., Horling, F., Kahmann, U., Harris, G., Schürmann, P., et al. (2002). The plant-specific function of 2-Cys peroxiredoxin-mediated detoxification of peroxides in the redox-hierarchy of photosynthetic electron flux. Proc. Natl. Acad. Sci. U.S.A. 99, 5738-5743. doi: 10.1073/pnas.072644999
29. Lee, J., Godon, C., Lagniel, G., Spector, D., Garin, J., Labarre, J., et al. (1999). Yap1 and Skn1 control specialized oxidative stress response regulons in yeast. J. Biol. Chem. 274, 16040-16046. doi: 10.1074/jbc.274.23.16040
30. Li, B., and Fields, S. (1993). Identification of mutations in p53 that affect its binding to SV40 large T antigen by using the yeast-two-hybrid system. FASEB J. 7, 957-963.
31. Li, L., Elledge, S. J., Peterson, C. A., Bales, E. S., and Legerski, R. J. (1994). Specific association between the human Dna-Repair proteins Xpa and Ercc1. Proc. Natl. Acad. Sci. U.S.A. 91, 5012-5016. doi: 10.1073/pnas.91.11.5012
32. Mehler, A. H. (1951). Studies on reactions of illuminated chloroplasts. II. Stimulation and inhibition of reactions with molecular oxygen. Arch. Biochem. Biophys. 33, 339-351. doi: 10.1016/0003-9861(51)90012-4
33. Miller, G., Shulaev, V., and Mittler, R. (2008). Reactive oxygen signaling and abiotic stress. Physiol. Plant. 133, 481-489. doi: 10.1111/j.1399-3054.2008.01090.x
34. Mittler, R., Kim, Y., Song, L. H., Coutu, J., Coutu, A., Ciftci-Yilmaz, S., et al. (2006). Gain- and loss-of-function mutations in Zat10 enhance the tolerance of plants to abiotic stress. Febs Lett. 580, 6537-6542. doi: 10.1016/j.febslet.2006.11.002
35. Overmyer, K., Brosche, M., Pellinen, R., Kuittinen, T., Tuominen, H., Ahlfors, R., et al. (2005). Ozone-induced programmed cell death in the Arabidopsis radical-induced cell death1 mutant. Plant Physiol. 137, 1092-1104. doi: 10.1104/pp.104.055681
36. Overmyer, L., Tuominen, H., Kettunen, R., Betz, C., Langebartels, C., Sandermann, H., et al. (2000). Ozone-sensitive Arabidopsis rcd1 mutant reveals opposite roles for ethylene and jasmonate signaling pathways in regulating superoxide-dependent cell death. Plant Cell 12, 1849-1862. doi: 10.1105/tpc.12.10.1849
37. Pena-Ahumada, A., Kahmann, U., Dietz, K. J., and Baier, M. (2006). Regulation of peroxiredoxin expression versus expression of Halliwell-Asada-Cycle enzymes during early seedling development of Arabidopsis thaliana. Photosynth. Res. 89, 99-112. doi: 10.1007/s11120-006-9087-3
38. Pfannschmidt, T. (2003). Chloroplast redox signals: How photosynthesis controls its own genes. Trends Plant Sci. 8, 33-41. doi: 10.1016/S1360-1385(02)00005-5
39. 2 availability preferentially drives glutathione accumulation in vacuoles and chloroplasts. Plant Cell Environ. 34, 21-32. doi: 10.1111/j.1365-3040.2010.02222.x
40. Rossel, J. B., Wilson, P. B., Hussain, D., Woo, N. S., Gordon, M. J., Mewett, O. P., et al. (2007). Systemic and intracellular responses to photooxidative stress in Arabidopsis. Plant Cell 19, 4091-4110. doi: 10.1105/tpc.106.045898
41. Samuilov, V. D., Lagunova, E. M., Dzyubinskaya, E. V., Izyumov, D. S., Kiselevsky, D. B., and Makarova, Y. V. (2002). Involvement of chloroplasts in the programmed cell death of plant cells. Biochemistry 67, 627-634. doi: 10.1023/A:1016138003183
42. Samuilov, V. D., Lagunova, E. M., Kiselevsky, D. B., Dzyubinskaya, E. V., Makarova, Y. V., and Gusev, M. V. (2003). Participation of chloroplasts in plant apoptosis. Biosci. Rep. 23, 103-117. doi: 10.1023/A:1025576307912
43. Schneider, S., Buchert, M., and Hovens, C. M. (1996). An in vitro assay of beta-galactosidase from yeast. Biotechniques 20, 960-962.
44. Schreiber, U., and Bilger, W. (1993). Progress in chlorophyll fluorescence research: major developments during the past years in retrospect. Prog. Bot. 54, 151-173.
45. Shaikhali, J., and Baier, M. (2010). Ascorbate regulation of 2-Cys peroxiredoxin- A promoter activity is light-dependent. J. Plant Physiol. 167, 461-467. doi: 10.1016/j.jplph.2009.10.021
46. Shaikhali, J., Heiber, I., Seidel, T., Ströher, E., Hiltscher, H., Birkmann, S., et al. (2008). The redox-sensitive transcription factor Rap2.4a controls nuclear expression of 2-Cys peroxiredoxin A and other chloroplast antioxidant enzymes. BMC Plant Biol. 8:48. doi: 10.1186/1471-2229-8-48
47. Sheffield, J. B. (2007). ImageJ, a useful tool for biological image processing and analysis. Microsc. Microanal. 13, 200-201. doi: 10.1017/S1431927607076611
48. Teotia, S., and Lamb, R. S. (2009). The paralogous genes RADICAL-INDUCED CELL DEATH1 and SIMILAR TO RCD ONE1 have partially redundant functions during Arabidopsis development. Plant Physiol. 151, 180-198. doi: 10.1104/pp.109.142786
49. Teotia, S., and Lamb, R. S. (2011). RCD1 and SRO1 are necessary to maintain meristematic fate in Arabidopsis thaliana. J. Exp. Bot. 62, 1271-1284. doi: 10.1093/jxb/erq363
50. Vainonen, J. P., Jaspers, P., Wrzaczek, M., Lamminmaki, A., Reddy, R. A., Vaahtera, L., et al. (2012). RCD1-DREB2A interaction in leaf senescence and stress responses in Arabidopsis thaliana. Biochem. J. 442, 573-581. doi: 10.1042/BJ20111739
51. Vernoux, T., Wilson, R. C., Seeley, K. A., Reichheld, J. P., Muroy, S., Brown, S., et al. (2000). The ROOT MERISTEMLESS1/CADMIUM SENSITIVE2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development. Plant Cell 12, 97-110. doi: 10.1105/tpc.12.1.97
52. Wachter, A., Wolf, S., Steininger, H., Bogs, J., and Rausch, T. (2005). Differential targeting of GSH1 and GSH2 is achieved by multiple transcription initiation: implications for the compartmentation of glutathione biosynthesis in the Brassicaceae. Plant J. 41, 15-30. doi: 10.1111/j.1365-313X.2004.02269.x
53. Wood, Z. A., Poole, L. B., and Karplus, P. A. (2003). Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science 300, 650-653. doi: 10.1126/science.1080405
54. Zapata, J. M., Guera, A., Esteban-Carrasco, A., Martin, M., and Sabater, B. (2005). Chloroplasts regulate leaf senescence: Delayed senescence in transgenic ndhF-defective tobacco. Cell Death Differ. 12, 1277-1284. doi: 10.1038/sj.cdd.4401657
55. Zhu, Y., Du, B., Qian, J., Zou, B., and Hua, J. (2013). Disease resistance gene-induced growth inhibition is enhanced by rcd1 independent of defense activation in Arabidopsis. Plant Physiol. 161, 2005-2013. doi: 10.1104/pp.112.213363