Double mutants deficient in cytosolic and thylakoid ascorbate peroxidase reveal a complex mode of interaction between reactive oxygen species, plant development, and response to abiotic stresses

Plant Physiology

Volumn 144, Issue 4, 2007, Pages 1777-1785

  Miller, Gad ^a   Suzuki, Nobuhiro ^a   Rizhsky, Ludmila ^b   Hegie, Alicia ^a   Koussevitzky, Shai ^a   Mittler, Ron ^a,c  

^a UNIVERSITY OF NEVADA   (United States)

^b IOWA STATE UNIVERSITY   (United States)

^c HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CHLOROPHYLL; ENZYME ACTIVITY; METABOLISM; MUTAGENS;

REACTIVE OXYGEN SPECIES; THERMOTOLERANCE; THYLAKOID ASCORBATE PEROXIDASE;

PLANTS (BOTANY);

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 34547925626     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.107.101436     Document Type: Article

References (35)

1. Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141: 391-396
2. Bailey-Serres J, Mittler R (2006) The roles of reactive oxygen species in plant cells. Plant Physiol 141: 311
3. Bariola PA, MacIntosh GC, Green PJ (1999) Regulation of S-like ribonuclease levels in Arabidopsis: antisense inhibition of RNS1 or RNS2 elevates anthocyanin accumulation. Plant Physiol 119: 331-342
4. Bienert GP, Moller AL, Kristiansen KA, Schulz A, Moller IM, Schjoerring JK, Jahn TP (2007) Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J Biol Chem 282: 1183-1192
5. Ciftci-Yilmaz S, Morsy MR, Song L, Coutu A, Krizek BA, Lewis MW, Warren D, Cushman J, Connolly EL, Mittler R (2007) The ear-motif of the C2H2 zinc-finger protein ZAT7 plays a key role in the defense response of Arabidopsis to salinity stress. J Biol Chem 282: 9260-9268
6. Danna CH, Bartoli CG, Sacco F, Ingala LR, Santa-Maria GE, Guiamet JJ, Ugalde RA (2003) Thylakoid-bound ascorbate peroxidase mutant exhibits impaired electron transport and photosynthetic activity. Plant Physiol 132: 2116-2125
7. Davletova S, Rizhsky L, Liang H, Shengqiang Z, Oliver DJ, Coutu J, Shulaev V, Schlauch K, Mittler R (2005a) Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 17: 268-281
8. Davletova S, Schlauch K, Coutu J, Mittler R (2005b) The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiol 139: 847-856
9. Gapper C, Dolan L (2006) Control of plant development by reactive oxygen species. Plant Physiol 141: 341-345
10. Halliwell B (2006) Reactive species and antioxidants: redox biology is a fundamental theme of aerobic life. Plant Physiol 141: 312-322
11. Henzler T, Steudle E (2000) Transport and metabolic degradation of hydrogen peroxide in Chara corallina: model calculations and measurements with the pressure probe suggest transport of H(2)O(2) across water channels. J Exp Bot 51: 2053-2066
12. Johansson E, Olsson O, Nystrom T (2004) Progression and specificity of protein oxidation in the life cycle of Arabidopsis thaliana. J Biol Chem 279: 22204-22208
13. Karpinski S, Escobar C, Karpinska B, Creissen G, Mullineaux PM (1997) Photosynthetic electron transport regulates the expression of cytosolic ascorbate peroxidase genes in Arabidopsis during excess light stress. Plant Cell 9: 627-640
14. Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen G, Mullineaux P (1999) Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284: 654-657
15. Koussevitzky S, Nott A, Mockler TC, Hong F, Sachetto-Martins G, Surpin M, Lim J, Mittler R, Chory J (2007) Multiple signals from damaged chloroplasts converge on a common pathway to regulate nuclear gene expression. Science 316: 715-719
16. Kwak JM, Nguyen V, Schroeder JI (2006) The role of reactive oxygen species in hormonal responses. Plant Physiol 141: 323-329
17. Laloi C, Stachowiak M, Pers-Kamczyc E, Warzych E, Murgia I, Apel K (2007) Cross-talk between singlet oxygen- and hydrogen peroxide-dependent signaling of stress responses in Arabidopsis thaliana. Proc Natl Acad Sci USA 104: 672-677
18. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7: 405-410
19. Mittler R, Kim Y, Song L, Coutu J, Coutu A, Ciftci-Yilmaz S, Lee H, Stevenson B, Zhu JK (2007) Gain- and loss-of-function mutations in Zat10 enhance the tolerance of plants to abiotic stress. FEBS Lett 580: 6537-6542
20. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9: 490-498
21. Mullineaux PM, Karpinski S, Baker NR (2006) Spatial dependence for hydrogen peroxide-directed signaling in light-stressed plants. Plant Physiol 141: 346-350
22. Murgia I, Tarantino D, Vannini C, Bracale M, Carravieri S, Soave C (2004) Arabidopsis thaliana plants overexpressing thylakoidal ascorbate peroxidase show increased resistance to Paraquat-induced photooxidative stress and to nitric oxide-induced cell death. Plant J 38: 940-953
23. Nott A, Jung HS, Koussevitzky S, Chory J (2006) Plastid-to-nucleus retrograde signaling. Annu Rev Plant Biol 57: 739-759
24. Pitzschke A, Hirt H (2006) Mitogen-activated protein kinases and reactive oxygen species signaling in plants. Plant Physiol 141: 351-356
25. Pnueli L, Liang H, Rozenberg M, Mittler R (2003) Growth suppression, altered stomatal responses, and augmented induction of heat shock proteins in cytosolic ascorbate peroxidase (Apx1)-deficient Arabidopsis plants. Plant J 34: 187-203
26. Rizhsky L, Davletova S, Liang H, Mittler R (2004) The zinc finger protein Zat12 is required for cytosolic ascorbate peroxidase 1 expression during oxidative stress in Arabidopsis. J Biol Chem 279: 11736-11743
27. Rizhsky L, Hallak-Herr E, Van Breusegem F, Rachmilevitch S, Barr JE, Rodermel S, Inze D, Mittler R (2002) Double antisense plants lacking ascorbate peroxidase and catalase are less sensitive to oxidative stress than single antisense plants lacking ascorbate peroxidase or catalase. Plant J 32: 329-342
28. Suzuki N, Rizhsky L, Liang H, Shuman J, Shulaev V, Mittler R (2005) Enhanced tolerance to environmental stress in transgenic plants expressing the transcriptional coactivator multiprotein bridging factor 1c. Plant Physiol 139: 1313-1322
29. Tarantino D, Vannini C, Bracale M, Campa M, Soave C, Murgia I (2005) Antisense reduction of thylakoidal ascorbate peroxidase in Arabidopsis enhances paraquat-induced photooxidative stress and nitric oxide-induced cell death. Planta 221: 757-765
30. Torres MA, Dangl JL (2005) Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr Opin Plant Biol 8: 397-403
31. Torres MA, Jones JD, Dangl JL (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiol 141: 373-378
32. Van Breusegem F, Dat JF (2006) Reactive oxygen species in plant cell death. Plant Physiol 141: 384-390
33. Vanderauwera S, Zimmermann P, Rombauts S, Vandenabeele S, Langebartels C, Gruissem W, Inze D, Van Breusegem F (2005) Genome-wide analysis of hydrogen peroxide-regulated gene expression in Arabidopsis reveals a high light-induced transcriptional cluster involved in anthocyanin biosynthesis. Plant Physiol 139: 806-821
34. Yabuta Y, Motoki T, Yoshimura K, Takeda T, Ishikawa T, Shigeoka S (2002) Thylakoid membrane-bound ascorbate peroxidase is a limiting factor of antioxidative systems under photo-oxidative stress. Plant J 32: 915-925
35. Zaninotto F, La Camera S, Polverari A, Delledonne M (2006) Cross talk between reactive nitrogen and oxygen species during the hypersensitive disease resistance response. Plant Physiol 141: 379-383