2,4-Dichlorophenoxyacetic acid promotes S-nitrosylation and oxidation of actin affecting cytoskeleton and peroxisomal dynamics

Journal of Experimental Botany

Volumn 65, Issue 17, 2014, Pages 4783-4793

  Rodriguez Serrano M ^a   Pazmino D M ^a   Sparkes, I ^b,c   Rochetti, A ^b   Hawes, C ^b   Romero Puertas, M C ^a   Sandalio, L M ^a  

^a CSIC   (Spain)

^b OXFORD BROOKES UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF EXETER   (United Kingdom)

Author keywords

2, 4 D; Actin; Cytoskeleton; Nitric oxide; Peroxisomes; ROS; S nitrosylation; Xanthine dehydrogenase

Indexed keywords

2,4 DICHLOROPHENOXYACETIC ACID; HYDROGEN PEROXIDE; NITRIC OXIDE; NITROGEN; OXIDIZING AGENT; REACTIVE OXYGEN METABOLITE; SINGLET OXYGEN;

ACTIN FILAMENT; ARABIDOPSIS; CONFOCAL MICROSCOPY; DRUG EFFECTS; METABOLISM; MITOCHONDRION; OXIDATION REDUCTION REACTION; PEROXISOME;

2,4-DICHLOROPHENOXYACETIC ACID; ACTIN CYTOSKELETON; ARABIDOPSIS; HYDROGEN PEROXIDE; MICROSCOPY, CONFOCAL; MITOCHONDRIA; NITRIC OXIDE; NITROGEN; OXIDANTS; OXIDATION-REDUCTION; PEROXISOMES; REACTIVE OXYGEN SPECIES; SINGLET OXYGEN;

EID: 84907398766     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/eru237     Document Type: Article

References (67)

1. Astier J, Rasul S, Koen E, Manzoor H, Besson-Bard A, Lamotte O, Jendroz S, Durner J, Lindernayr C, Wendehenne D. 2011. S-Nitrosylation: an emerging post-translational protein modification in plants. Plant Science 181, 527-533.
2. Baluska F, Jasik J, Edelmann HG, Salajová T, Volkmann D. 2001. Latrunculin B-induced plant dwarfism: plant cell elongation is F-actindependent. Developmental Biology 231, 113-124.
3. Benjamins R, Scheres B. 2008. Auxin: the looping star in plant development. Annual Review of Plant Biology 59, 443-465.
4. Blume YB, Nyporko AY, Yemets AI, Baird WV. 2003. Structural modeling of the interaction of plant alpha-tubulin with dinitroaniline and phosphoroamidate herbicides. Cell Biology International 27, 171-174.
5. Collings DA, Lill AW, Himmelspach R, Wasteneys GO. 2006. Hypersensitivity to cytoskeletal antagonists demonstrates microtubule- microfilament cross-talk in the control of root elongation in Arabidopsis thaliana. New Phytologist 170, 275-290.
6. Dalle-Donne I, Milzani A, Giustarini D, Di Simplicio P, Colombo R, Rossi R. 2000. S-NO-actin: S-nitrosylation kinetics and the effect on isolated vascular smooth muscle. Journal of Muscle Research and Cell Motility 21, 171-181.
7. Dalle-Donne I, Rossi R, Milzani A, Di Simplicio P, Colombo R. 2001. The actin cytoskeleton response to oxidants: from small heat shock protein phosphorylation to changes in the redox state of actin itself. Free Radical Biology and Medicine 31, 1624-1632.
8. Delker C, Raschke A, Quint M. 2008. Auxin dynamics: the dazzling complexity of a small molecule's message. Planta 227, 929-941.
9. Delledonne M. 2005. NO news is good news for plants. Current Opinion in Plant Biology 8, 390-396.
10. del Río LA. 2011. Peroxisomes as a cellular source of reactive nitrogen species signal molecules. Archives of Biochemistry and Biophysics 506, 1-11.
11. Délye C, Menchari Y, Michel S, Darmency H. 2004. Molecular bases for sensitivity to tubulin-binding herbicides in green foxtail. Plant Physiology 136, 3920-3932.
12. Dhonukshe P, Grigoriev I, Fischer R, et al. 2008. Auxin transport inhibitors impair vesicle motility and actin cytoskeleton dynamics in diverse eukaryotes. Proceedings of the National Academy of Sciences, USA 105, 4489-4494.
13. Foissner I, Grolig F, Obermeyer G. 2002. Reversible protein phosphorylation regulates the dynamic organization of the pollen tube cytoskeleton: effects of calyculin A and okadaic acid. Protoplasma 220, 1-5.
14. Grossmann K. 2010. Auxin herbicides: current status of mechanism and mode of action. Pest Managment Science 66, 113-120.
15. Grossmann K, Kwiatkowski J, Tresch S. 2001. Auxin herbicides induce H2O2 overproduction and tissue damage in cleavers (Galiumaparine L.). Journal of Experimental Botany 52, 1811-1816.
16. Halliwell B, Gutteridge J. 2007. Free radicals in biology and medicine , 4th edn. Oxford: Oxford University Press.
17. Hussey PJ, Ketelaar T, Deeks MJ. 2006. Control of the actin cytoskeleton in plant cell growth. Annual Review of Plant Biology 57, 109-125.
18. Jaffrey SR, Erdjument-Bromage H, Ferris CD, Tempst P, Snyder SH. 2001. Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nature Cell Biology 3, 193-197.
19. Kasprowicz A, Szuba A, Volkmann D, Baluska F, Wojtaszek P. 2009. Nitric oxide modulates dynamic actin cytoskeleton and vesicle trafficking in a cell type-specific manner in root apices. Journal of Experimental Botany 60, 1605-1617.
20. Ketelaar T, Allwood EG, Anthony RG, Voigt B, Menzel D, Hussey PJ. 2004. The actin-interacting protein AIP1 is essential for actin organization and plant development. Current Biology 14, 57-62.
21. Koch E, Slusarenko A. 1990. Arabidopsis is susceptible to infection by a downy mildew fungus. The Plant Cell 2, 437-445.
22. Lanza M, Garcia-Ponce B, Castrillo G, et al. 2012. Role of actin cytoskeleton in brassinosteroid signaling and in its integration with the auxin response in plants. Developmental Cell 22, 1275-1285.
23. Liszkay A, van der Zalm E, Schopfer P. 2004. Production of reactive oxygen intermediates (O2-, H2O2, and OH) by maize roots and their role in wall loosening and elongation growth. Plant Physiology 136, 3114-3123.
24. Lounifi, I, Arc E, Molassiotis A, Job D, Rajjou, L, Tanou G. 2013. Interplay between protein carbonylation and nitrosylation in plants. Proteomics 13, 568-578.
25. Malerba M, Contran N, Tonelli M, Crosti P, Cerana R. 2008. Role of nitric oxide in actin depolymerization and programmed cell death induced by fucicoccin in sycamore (Acer pseudoplatanus) culture cells. Physiologia Plantarum 133, 449-467.
26. Mano S, Nakamori C, Hayashi M, Kato A, Kondo M, Nishimura M. 2002. Distribution and characterization of peroxisomes in arabidopsis by visualization with GFP: dynamic morphology and actin-dependent movement. Plant and Cell Physiology 43, 331-341.
27. Mittler R, Vanderauwera S, Suzuki N, Miller GAD, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F. 2011. ROS signaling: the new wave? Trends in Plant Science 16, 300-309.
28. Moreau M, Lindermayr C, Durner J, Klessig DF. 2010. NO synthesis and signaling in plants-where do we stand? Physiologia Plantarum 138, 372-383.
29. Nakatsubo N, Kojima H, Kikuchi K, Nagoshi H, Hirata Y, Maeda D, Imai Y, Irimura T, Nagano T. 1998. Direct evidence of nitric oxide production from bovine aortic endothelial cells using new fluorescence indicators: diaminofluoresceins. FEBS Letters 427, 263-266.
30. Neill S, Barros R, Bright J, Desikan R, Hancock J, Harrison J, Morris P, Ribeiro D, Wilson I. 2008. Nitric oxide, stomatal closure, and abiotic stress. Journal of Experimental Botany 59, 165-176.
31. Nelson BK, Cai X, Nebenführ A. 2007. A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. The Plant Journal 51, 1126-1136.
32. Nick P, Han MJ, An G. 2009. Auxin stimulates its own transport by shaping actin filaments. Plant Physiology 151, 155-167.
33. Ortega-Galisteo A, Rodríguez-Serrano M, Pazmino DM, Gupta D, Sandalio LM, Romero-Puertas MC. 2012. S-nitrosylated proteins in pea (Pisum sativum L.) leaf peroxisomes: changes under abiotic stress. Journal of Experimental Botany 63, 2089-2103.
34. Ovidi E, Gambellini G, Taddei AR, Cai G, Del Casino C, Ceci M, Rondini S, Tiezzi A. 2001. Herbicides and the microtubular apparatus of Nicotiana tabacum pollen tube: immunofluorescence and immunogold labelling studies. Toxicology in vitro 15, 143-151.
35. Pazmiño DM. 2009. Contribución de las especies de oxígeno y nitrógeno reactivo, y de los peroxisomas a la toxicidad del 2,4-D en plantas. PhD Thesis. University of Granada, Spain.
36. Pazmiño DM, Rodríguez-Serrano M, Romero-Puertas MC, Archilla- Ruiz A, Del Río LA, Sandalio LM. 2011. Differential response of young and adult leaves to herbicide 2,4-dichlorophenoxyacetic acid in pea plants: role of reactive oxygen species. Plant, Cell and Environment 34, 1874-1889.
37. Pazmiño DM, Rodríguez-Serrano M, Sanz M, Romero-Puertas MC, Sandalio LM. 2014 Regulation of epinasty induced by 2,4-dichlorophenoxyacetic acid in pea and Arabidopsis plants. Plant Biology (in press). doi:10.1111/plb.12128.
38. Pazmiño DM, Romero-Puertas MC, Sandalio LM. 2012. Insights into the toxicity mechanism of and cell response to the herbicide 2,4-D in plants. Plant Signaling and Behaviour 7, 1-3.
39. Rahman A, Bannigan A, Sulaman W, Pechter P, Blancaflor EB, Baskin TI. 2007. Auxin, actin and growth of the Arabidopsis thaliana primary root. The Plant Journal 50, 514-528.
40. Rasmussen I, Pedersen LH, Byg L, Suzuki K, Sumimoto H, Vilhardt F. 2010. Effects of F/G-actin ratio and actin turn-over rate on NADPH oxidase activity in microglia. BMC Immunology 11, 44.
41. Rodríguez-Serrano M, Romero-Puertas MC, Sparkes I, Hawes C, del Río LA, Sandalio LM. 2009. Peroxisome dynamics in Arabidopsis plants under oxidative stress induced by cadmium. Free Radicals in Biology and Medicine 47, 1632-1639.
42. Romero-Puertas MC, Palma JM, Gómez M, del Río LA, Sandalio LM. 2002. Cadmium causes the oxidative modification of proteins in pea plants. Plant, Cell and Environment 25, 677-686.
43. Romero-Puertas MC, McCarthy I, Gómez M, Sandalio LM, Corpas FJ, del Río LA, Palma JM. 2004a. Reactive oxygen species-mediated enzymatic systems involved in the oxidative action of 2,4-dichlorophenoxyacetic acid. Plant, Cell and Environment 27, 1135-1148.
44. Romero-Puertas MC, Rodríguez-Serrano M, Corpas FJ, Gómez M, del Río LA, Sandalio LM. 2004b. Cadmium-induced subcellular accumulation of O2- and H2O2 in pea leaves. Plant, Cell and Environment 27, 1122-1134.
45. Romero-Puertas MC, Rodríguez-Serrano M, Sandalio LM. 2013. Protein S-nitrosylation in plants under abiotic stress: an overview. Frontiers in Plant Science 4, 373.
46. Sandalio LM, Rodríguez-Serrano M, Gupta DK, Archilla A, Romero- Puertas MC, del Río LA. 2012. Reactive oxygen species and nitric oxide in plants under cadmium stress. In: Amad P, Prassad MNV, eds. Toxicity to signaling. Environmental adaptations and stress tolerance of plants in the era of climate change. Berlin: Springer, 199-215.
47. Sandalio LM, Rodríguez-Serrano M, Romero-Puertas MC, del Río LA. 2008. Imaging of reactive oxygen species and nitric oxide in vivo in plant tissues. Methods in Enzymology 440: 397-409.
48. Sandalio LM, Rodríguez-Serrano M, Romero-Puertas MC, del Río LA. 2013. Role of peroxisomes as a source of reactive oxygen species (ROS) signaling molecules. In: del Río LA, ed. Peroxisomes and their key role in cellular signaling and metabolism. Dordrecht, Springer Science+Business, 231-249.
49. Schopfer P, Liszkay A, Bechtold M, Frahry G, Wagner A. 2002. Evidence that hydroxyl radicals mediate auxin-induced extension growth. Planta 214, 821-828.
50. Sheahan MB, Staiger JC, Rose RJ, McCurdy DW. 2004. A green fluorescent protein fusion to actin-binding domain 2 of Arabidopsis fimbrin highlights new features of a dynamic actin cytoskeleton in live plant cells. Plant Physiology 136, 3968-3978.
51. Sheremet YA, Yemets AI, Blume YB. 2012. Inhibitors of tyrosine kinases and phosphatases as a tool for the investigation of microtubule role in plant cold response. Cytology and Genetics 46, 1-8.
52. Smith LG, Oppenheimer DG. 2005. Spatial control of cell expansion by the plant cytoskeleton. Annual Review of Cell and Developmental Biology 21, 271-294.
53. Song X, Ma Q, Hao X, Li H. 2012. Roles of the actin cytoskeleton and an actin-binding protein in wheat resistance against Puccinic striiformis f. sp. tritici. Protoplasma 249, 99-106.
54. Staiger CJ, Blanchoin L. 2006. Actin dynamics: old friends with new stories. Current Opinion in Plant Biology 19, 554-562.
55. Staiger CJ, Sheahan MB, Khurana P, Wang X, McCurdy DW, Blanchoin L. 2009. Actin filament dynamics are dominated by rapid growth and severing activity in the Arabidopsis cortical array. Journal of Cell Biology 184, 269-280.
56. Stamler JS, Lamas S, Fang FC. 2001. Nitrosylation, the prototypic redox-based signaling mechanism. Cell 106, 675-683.
57. Sun J, Steenbergen C, Murphy E. 2006. S-nitrosylation: NO-related redox signaling to protect against oxidative stress. Antioxidants and Redox Signaling 8, 1693-1705.
58. Suzuki N, Koussevitzky S, Mittler R, Miller G. 2011. ROS and redox signalling in the response of plants to abiotic stress. Plant, Cell and Environment 35, 259-270.
59. Teixeira MC, Duque P, Sá-Correia I. 2007. Environmental genomics: mechanistic insights into toxicity of and resistance to the herbicide 2,4-D. Trends in Biotechnology 25, 363-370.
60. Terman JR, Kashina A. 2013. Post-translational modification and regulation of actin. Current Opinion in Cell Biology 25, 30-38.
61. Vandenabeele S, Vanderauwera S, Vuylsteke M, Rombauts S, Langebartels C, Seidlitz HK, Zabeau M, Van Montagu M, Inzé D, Van Breusegem F. 2004. Catalase deficiency drastically affects gene expression induced by high light in Arabidopsis thaliana. The Plant Journal 39, 45-58.
62. Vandelle E, Delledonne M. 2011. Peroxinitrite formation and function in plants. Plant Science 181, 534-539.
63. Van Gestel K, Kohler RH, Verbelen JP. 2002. Plant mitochondria move on F-actin, but their positioning in the cortical cytoplasm depends on both F-actin and microtubules. Journal of Experimental Botany 53, 659-667.
64. Wasteneys GO, Yang Z. 2004. New views on the plant cytoskeleton. Plant Physiology 136, 3884-3891.
65. Wilkins KA, Bancroft J, Bosch M, Ings J, Smirnoff N, Franklin- Tong VE. 2011. Reactive oxygen species and nitric oxide mediate actin reorganization and programmed cell death in the self-incompatibility response of Papaver. Plant Physiology 156, 404-416.
66. Yemets AI, Kraslylenko YA, Lytryn DI, Sheremet YA, Blume YB. 2011. Nitric oxide signalling via cytoskeleton in plants. Plant Science 181, 545-554.
67. Zaninotto F, Camera SL, Polverari A, Delledonne M. 2006. Cross talk between reactive nitrogen and oxygen species during the hypersensitive disease resistance response. Plant Physiology 141, 379-383.