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Nitric oxide and ROS mediate autophagy and regulate Alternaria alternata toxin-induced cell death in tobacco BY-2 cells

Sadhu, Abhishek, Moriyasu, Yuji, Acharya, Krishnendu, Bandyopadhyay, Maumita·2019·Scientific Reports
DOI 10.1038/s41598-019-45470-yPMC PMC6586778
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Abstract

Synergistic interaction of nitric oxide (NO) and reactive oxygen species (ROS) is essential to initiate cell death mechanisms in plants. Though autophagy is salient in either restricting or promoting hypersensitivity response (HR)-related cell death, the crosstalk between the reactive intermediates and autophagy during hypersensitivity response is paradoxical. In this investigation, the consequences of Alternaria alternata toxin (AaT) in tobacco BY-2 cells were examined. At 3 h, AaT perturbed intracellular ROS homeostasis, altered antioxidant enzyme activities, triggered mitochondrial depolarization and induced autophagy. Suppression of autophagy by 3-Methyladenine caused a decline in cell viability in AaT treated cells, which indicated the vital role of autophagy in cell survival. After 24 h, AaT facilitated Ca 2+ influx with an accumulation of reactive oxidant intermediates and NO, to manifest necrotic cell death. Inhibition of NO accumulation by 2-(4-Carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide (cPTIO) decreased the level of necrotic cell death, and induced autophagy, which suggests NO accumulation represses autophagy and facilitates necrotic cell death at 24 h. Application of N-acetyl-L-cysteine at 3 h, confirmed ROS to be the key initiator of autophagy, and together with cPTIO for 24 h, revealed the combined effects of NO and ROS is required for necrotic HR cell death.

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Research works printed but not linked: 90

  1. Martin, G. B., Bogdanove, A. J. & Sessa, G. Understanding the functions of plant disease resistance proteins. Annu. Rev. Plant Biol. 54, 23–61 (2003). · DOI
  2. Nimchuk, Z., Eulgem, T., Holt, B. F. III & Dangl, J. L. Recognition and response in the plant immune system. Annu. Rev. Genet. 37, 579–609 (2003). · DOI
  3. Delledonne, M., Zeier, J., Marocco, A. & Lamb, C. Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. P. Natl. Acad. Sci. USA 98, 13454–13459 (2001). · DOI
  4. Zaninotto, F., La Camera, S., Polverari, A. & Delledonne, M. Cross talk between reactive nitrogen and oxygen species during the hypersensitive disease resistance response. Plant Physiol. 141, 379–383 (2006). · DOI
  5. Pietrowska, E., Różalska, S., Kaźmierczak, A., Nawrocka, J. & Małolepsza, U. Reactive oxygen and nitrogen (ROS and RNS) species generation and cell death in tomato suspension cultures—Botrytis cinerea interaction. Protoplasma 252, 307–319 (2015). · DOI
  6. Doke, N. Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of Phytophthora infestans and to the hyphal wall components. Physiol. Plant Pathol. 23, 345–357 (1983). · DOI
  7. Auh, C. K. & Murphy, T. M. Plasma membrane redox enzyme is involved in the synthesis of O2 − and H2O2 by Phytophthora elicitor-stimulated rose cells. Plant Physiol. 107, 1241–1247 (1995). · DOI
  8. Grant, M. et al. The RPM1 plant disease resistance gene facilitates a rapid and sustained increase in cytosolic calcium that is necessary for the oxidative burst and hypersensitive cell death. Plant J. 23, 441–450 (2000). · DOI
  9. McDowell, J. M. & Dangl, J. L. Signal transduction in the plant immune response. Trends Biochem. Sci. 25, 79–82 (2000). · DOI
  10. Liu, Y. Autophagy regulates programmed cell death during the plant innate immune response. Cell 121, 567–577 (2005). · DOI
  11. Wang, J. & Higgins, V. J. Nitric oxide has a regulatory effect in the germination of conidia of Colletotrichum coccodes. Fungal Genet. Biol. 42, 284–292 (2005). · DOI
  12. Moreau, M., Lindermayr, C., Durner, J. & Klessig, D. F. NO synthesis and signaling in plants–where do we stand? Physiol. Plant. 138, 372–383 (2010). · DOI
  13. Gas, E., Flores-Pérez, Ú., Sauret-Güeto, S. & Rodríguez-Concepción, M. Hunting for plant nitric oxide synthase provides new evidence of a central role for plastids in nitric oxide metabolism. Plant Cell 21, 18–23 (2009). · DOI
  14. Jeandroz, S. et al. Occurrence, structure, and evolution of nitric oxide synthase–like proteins in the plant kingdom. Sci. Signal. 9, 1–9 (2016). · DOI
  15. Santolini, J., André, F., Jeandroz, S. & Wendehenne, D. Nitric oxide synthase in plants: Where do we stand? Nitric Oxide 63, 30–38 (2017). · DOI
  16. Chamizo-Ampudia, A. et al. A dual system formed by the ARC and NR molybdoenzymes mediates nitrite‐dependent NO production in Chlamydomonas. Plant Cell Environ. 39, 2097–2107 (2016). · DOI
  17. Corpas, F. J., Palma, J. M., Del Río, L. A. & Barroso, J. B. Evidence supporting the existence of l-arginine-dependent nitric oxide synthase activity in plants. New Phytol. 184, 9–14 (2009). · DOI
  18. Rasul, S. et al. Nitric oxide production mediates oligogalacturonide‐triggered immunity and resistance to Botrytis cinerea in Arabidopsis thaliana. Plant Cell Environ. 35, 1483–1499 (2012). · DOI
  19. Howlett, B. J. Secondary metabolite toxins and nutrition of plant pathogenic fungi. Curr. Opin. Plant Biol. 9, 371–375 (2006). · DOI
  20. Koonin, E. V. & Aravind, L. Origin and evolution of eukaryotic apoptosis: the bacterial connection. Cell Death Differ. 9, 394–404 (2002). · DOI
  21. Van Doorn, W. G. et al. Morphological classification of plant cell deaths. Cell Death Differ. 18, 1241–1246 (2011). · DOI · Paper page
  22. Hofius, D. et al. Autophagic components contribute to hypersensitive cell death in Arabidopsis. Cell 137, 773–783 (2009). · DOI
  23. Komatsu, K. et al. Viral-induced systemic necrosis in plants involves both programmed cell death and the inhibition of viral multiplication, which are regulated by independent pathways. Mol. Plant Microbe In. 23, 283–293 (2010). · DOI
  24. Christofferson, D. E. & Yuan, J. Necroptosis as an alternative form of programmed cell death. Curr. Opin. Cell Biol. 22, 263–268 (2010). · DOI
  25. Patel, S. & Dinesh-Kumar, S. P. Arabidopsis ATG6 is required to limit the pathogen-associated cell death response. Autophagy 4, 20–27 (2008). · DOI
  26. Yoshimoto, K. et al. Autophagy negatively regulates cell death by controlling NPR1-dependent salicylic acid signaling during senescence and the innate immune response in Arabidopsis. Plant Cell 21, 2914–2927 (2009). · DOI
  27. Lai, Z., Wang, F., Zheng, Z., Fan, B. & Chen, Z. A critical role of autophagy in plant resistance to necrotrophic fungal pathogens. Plant J. 66, 953–968 (2011). · DOI
  28. Lenz, H. D. et al. Autophagy differentially controls plant basal immunity to biotrophic and necrotrophic pathogens. Plant J. 66, 818–830 (2011a). · DOI
  29. Lenz, H. D., Vierstra, R. D., Nürnberger, T. & Gust, A. A. ATG7 contributes to plant basal immunity towards fungal infection. Plant Signal Behav. 6, 1040–1042 (2011b). · DOI
  30. Duan, S. et al. Transcriptomic profile of tobacco in response to Alternaria longipes and Alternaria alternata infections. Sci. Rep, https://doi.org/10.1038/srep25635 (2016). · DOI
  31. Wang, H. C. et al. Phenotypic analysis of Alternaria alternata, the causal agent of tobacco brown spot. Plant Pathology J. 14, 79–85 (2015). · DOI
  32. Tsuge, T. et al. Host-selective toxins produced by the plant pathogenic fungus Alternaria alternata. FEMS Microbiol. Rev. 37, 44–66 (2013). · DOI
  33. Takao, K. The global regulator LaeA controls biosynthesis of host-specific toxins, pathogenicity and development of Alternaria alternata pathotypes. J. Gen. Plant Pathol. 82, 121–131 (2016). · DOI
  34. Saha, D. Identification of a polyketide synthase required for alternariol (AOH) and alternariol-9-methyl ether (AME) formation in Alternaria alternata. PLoS One, https://doi.org/10.1371/journal.pone.0040564 (2012). · DOI
  35. Oh, K. B., Tajima, Y., Saito, M., Chang, I. M. & Matsuoka, H. Cytotoxicity of extracts from Alternaria alternata against cultured tobacco BY-2 cells. Biocontrol Sci. 7, 127–130 (2002). · DOI
  36. Slavov, S., Mayama, S. & Atanassov, A. Toxin production of Alternaria alternata tobacco pathotype. Biotechnol. Biotec. Eq. 18, 90–95 (2004). · DOI
  37. Cheng, D. D. Characterization of the programmed cell death induced by metabolic products of Alternaria alternata in tobacco BY‐2 cells. Physiol. Plantarum 1, 117–129 (2011). · DOI
  38. McCabe, P. F. & Leaver, C. J. Programmed cell death in cell cultures in Programmed Cell Death in Higher Plants (eds Lam, E., Fukuda, H., Greenberg, J.) 115–124 (Springer, 2000). · DOI
  39. Gupta, N. S., Banerjee, M., Basu, S. K. & Acharya, K. Involvement of nitric oxide signal in Alternaria alternata toxin induced defense response in Rauvolfia serpentina Benth. ex Kurz calli. Plant Omics 6, 157–164 (2013).
  40. Hayward, A. P., Tsao, J. & Dinesh-Kumar, S. P. Autophagy and plant innate immunity: defense through degradation. Semin. Cell Dev. Biol. 20, 1041–1047 (2009). · DOI
  41. Minina, E. A., Bozhkov, P. V. & Hofius, D. Autophagy as initiator or executioner of cell death. Trends Plant Sci. 19, 692–697 (2014). · DOI
  42. Niu, L. & Liao, W. Hydrogen peroxide signaling in plant development and abiotic responses: crosstalk with nitric oxide and calcium. Front. Plant Sci. 7, 230 (2016).
  43. Hou, Y. et al. Comparative genomics of pathogens causing brown spot disease of tobacco: Alternaria longipes and Alternaria alternata. PloS one, https://doi.org/10.1371/journal.pone.0155258 (2016). · DOI
  44. Langhans, M. & Robinson, D. G. 1-Butanol targets the Golgi apparatus in tobacco BY-2 cells, but in a different way to Brefeldin A. J. Exp. Bot. 58, 3439–3447 (2007). · DOI
  45. Pérez-Pérez, M. E., Lemaire, S. D. & Crespo, J. L. Reactive oxygen species and autophagy in plants and algae. Plant physiol. 160, 156–164 (2012). · DOI
  46. Lamb, C. & Dixon, R. A. The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 251–275 (1997). · DOI
  47. Liu, H. B. et al. NADPH oxidase RBOHD contributes to autophagy and hypersensitive cell death during the plant defense response in Arabidopsis thaliana. Biol. Plantarum 59, 570–580 (2015). · DOI
  48. Jiménez-Quesada, M. J., Traverso, J. Á. & de Dios Alché, J. NADPH Oxidase-Dependent Superoxide Production in Plant Reproductive Tissues. Front. Plant Sci. 7, 1–13 (2016). · DOI
  49. Kadota, Y., Shirasu, K. & Zipfel, C. Regulation of the NADPH oxidase RBOHD during plant immunity. Plant Cell Physiol. 56, 1472–1480 (2015). · DOI
  50. Locato, V., Paradiso, A., Sabetta, W., De Gara, L. & de Pinto, M. C. Nitric oxide and reactive oxygen species in PCD signaling in Advances in Botanical Research: Nitric oxide and signaling in plants (eds Wendehenne, D., Jacquot, J. P., Gadal, P.) 165–192 (Academic Press, 2016). · DOI
  51. Mittler, R. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7, 405–410 (2002). · DOI
  52. Kalogeris, T., Bao, Y. & Korthuis, R. J. Mitochondrial reactive oxygen species: a double edged sword in ischemia/reperfusion vs preconditioning. Redox Biol. 2, 702–714 (2014). · DOI
  53. Zorov, D. B., Juhaszova, M. & Sollott, S. J. Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release. Physiol. Rev. 94, 909–950 (2014). · DOI · Paper page
  54. Michaeli, S. & Galili, G. Degradation of organelles or specific organelle components via selective autophagy in plant cells. Int. J. Mol. Sci. 15, 7624–7638 (2014). · DOI
  55. Begara-Morales, J. C. et al. Differential molecular response of monodehydroascorbate reductase and glutathione reductase by nitration and S-nitrosylation. J. Exp. Bot. 66, 5983–5996 (2015). · DOI
  56. Clark, D., Durner, J., Navarre, D. A. & Klessig, D. F. Nitric oxide inhibition of tobacco catalase and ascorbate peroxidase. Mol. Plant. Microbe. In. 13, 1380–1384 (2000). · DOI
  57. Fares, A., Rossignol, M. & Peltier, J. B. Proteomics investigation of endogenous S-nitrosylation in Arabidopsis. Biochem. Bioph. Res. Co. 416, 331–336 (2011). · DOI
  58. Foyer, C. H. & Noctor, G. Ascorbate and glutathione: the heart of the redox hub. Plant Physiol. 155, 2–18 (2011). · DOI
  59. Keyster, M., Klein, A., Egbich, I., Jacobs, A. & Ludidi, N. Nitric oxide increases the enzymatic activity of three ascorbate peroxidase isoforms in soybean root nodules. Plant Signal Behav. 6, 956–961 (2011). · DOI
  60. Begara-Morales, J. C. et al. Dual regulation of cytosolic ascorbate peroxidase (APX) by tyrosine nitration and S-nitrosylation. J. Exp. Bot. 65, 527–538 (2014). · DOI
  61. Corpas, F. J., Alché, J. D. & Barroso, J. B. Current overview of S-nitrosoglutathione (GSNO) in higher plants. Front. Plant. Sci. 4, 126 (2013).
  62. de Pinto, M. C., Paradiso, A., Leonetti, P. & de Gara, L. Hydrogen peroxide, nitric oxide and cytosolic ascorbate peroxidase at the crossroad between defence and cell death. Plant J. 48, 784–795 (2006). · DOI
  63. Yakimova, E. T., Yordanova, Z., Slavov, S., Kapchina‐Toteva, V. M. & Woltering, E. J. Alternaria alternata AT toxin induces programmed cell death in tobacco. J. Phytopathol. 157, 592–601 (2009). · DOI
  64. Víteček, J. et al. Cell death induced by sodium nitroprusside and hydrogen peroxide in tobacco BY-2 cell suspension. Biol. Plantarum 51, 472–479 (2007). · DOI
  65. Hatsugai, N. et al. A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell death. Science 305, 855–858 (2004). · DOI
  66. Xiong, Y., Contento, A. L., Nguyen, P. Q. & Bassham, D. C. Degradation of oxidized proteins by autophagy during oxidative stress in Arabidopsis. Plant physiol. 143, 291–299 (2007). · DOI
  67. Delledonne, M., Xia, Y., Dixon, R. A. & Lamb, C. Nitric oxide functions as a signal in plant disease resistance. Nature 394, 85–88 (1998). · DOI
  68. Sarkar, S. et al. Complex inhibitory effects of nitric oxide on autophagy. Mol. Cell 43, 19–32 (2011). · DOI
  69. Shen, C., Yan, J., Erkocak, O. F., Zheng, X. F. & Chen, X. D. Nitric oxide inhibits autophagy via suppression of JNK in meniscal cells. Rheumatology 53, 1022–1033 (2014). · DOI
  70. Takatsuka, C. et al. Autophagy in tobacco BY-2 cells cultured under sucrose starvation conditions: isolation of the autolysosome and its characterization. Plant Cell Physiol. 52, 2074–2087 (2011). · DOI
  71. Santos, A. R. The impact of CdSe/ZnS quantum dots in cells of Medicago sativa in suspension culture. J. Nanobiotechnol. 8, 1–14 (2010). · DOI
  72. Huang, W., Xing, W., Li, D. & Liu, Y. Microcystin-RR induced apoptosis in tobacco BY-2 suspension cells is mediated by reactive oxygen species and mitochondrial permeability transition pore status. Toxicol. in vitro 22, 328–337 (2008). · DOI
  73. Morin, L. G. Direct colorimetric determination of serum calcium with o-cresolphthalein complexon. Am. J. Clin. Pathol. 61, 114–117 (1974). · DOI
  74. Sadhu, A., Ghosh, I., Moriyasu, Y., Mukherjee, A. & Bandyopadhyay, M. Role of cerium oxide nanoparticle-induced autophagy as a safeguard to exogenous H2O2-mediated DNA damage in tobacco BY-2 cells. Mutagenesis 33, 161–177 (2018). · DOI
  75. Ghosh, M., Bandyopadhyay, M. & Mukherjee, A. Genotoxicity of titanium dioxide (TiO2) nanoparticles at two trophic levels: plant and human lymphocytes. Chemosphere 81, 1253–1262 (2010). · DOI
  76. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254 (1976). · DOI · Paper page
  77. Beauchamp, C. & Fridovich, I. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal. Biochem. 44, 276–287 (1971). · DOI · Paper page
  78. Achary, V. M. M., Jena, S., Panda, K. K. & Panda, B. B. Aluminium induced oxidative stress and DNA damage in root cells of Allium cepa L. Ecotoxicol. Environ. Saf. 70, 300–310 (2008). · DOI
  79. Aebi, H. Catalase in vitro in Methods in enzymology, vol. 105 (ed. Packer, L.) 121–126 (Academic Press Inc,. 1984). · DOI · Paper page
  80. Chance, B. & Maehly, A. C. Assay of catalases and peroxidases in Methods in enzymology (ed. Glick, D.) 764–775 (Wiley, 1955). · DOI
  81. Gallego, S. M., Benavides, M. P. & Tomaro, M. L. Effect of heavy metal ion excess on sunflower leaves: evidence for involvement of oxidative stress. Plant Sci. 121, 151–159 (1996). · DOI
  82. Smith, I. K., Vierheller, T. L. & Thorne, C. A. Assay of glutathione reductase in crude tissue homogenates using 5, 5′-dithiobis (2-nitrobenzoic acid). Anal. Biochem. 175, 408–413 (1988). · DOI
  83. Anderson, M. E. Determination of glutathione and glutathione disulfide in biological samples in Methods in Enzymology, vol 113 (ed. Meister, A.) 548–555 (Elsevier, 1985). · DOI
  84. Sahoo, S., Awasthi J. P., Sunkar, R., Panda, S. K. Determining Glutathione Levels in Plants in Plant Stress Tolerance. Methods in Molecular Biology, vol 1631 (ed. Sunkar, R.) 273– 277 (Humana Press, 2017). · DOI
  85. Yamada, T., Takatsu, Y., Kasumi, M., Ichimura, K. & van Doorn, W. G. Nuclear fragmentation and DNA degradation during programmed cell death in petals of morning glory (Ipomoea nil). Planta 224, 1279–1290 (2006). · DOI
  86. Riccardi, C. & Nicoletti, I. Analysis of apoptosis by propidium iodide staining and flow cytometry. Nat. Protoc. 1, 1458–1461 (2006). · DOI · Paper page
  87. Chan, F. K. M., Moriwaki, K., De Rosa, M. J. Detection of necrosis by release of lactate dehydrogenase activity in Immune Homeostasis: Methods and Protocols (eds Snow, A. L. & Lenardo, M. J.) 65–70 (Springer, 2013). · DOI
  88. Ohno, R. et al. Cryptogein-Induced cell cycle arrest at G2 phase is associated with inhibition of cyclin-dependent kinases, suppression of expression of cell cycle-related genes and protein degradation in synchronized tobacco BY-2 cells. Plant Cell Physiol. 52, 922–932 (2011). · DOI
  89. Mitou, G., Budak, H. & Gozuacik, D. Techniques to study autophagy in plants. Int. J. Plant Genomics, https://doi.org/10.1155/2009/451357 (2009). · DOI
  90. Yano, K. et al. Dissection of autophagy in tobacco BY-2 cells under sucrose starvation conditions using the vacuolar H+-ATPase inhibitor concanamycin A and the autophagy-related protein Atg8. Plant Signal. Behav, https://doi.org/10.1080/15592324.2015.1082699 (2015). · DOI

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Metadata

Authors
Sadhu, A., Moriyasu, Y., Acharya, K., & Bandyopadhyay, M.
Venue
Scientific Reports
Publisher
Springer Science and Business Media LLC
Published
2019-06-20
Volume
9
Issue
1
ISSN
2045-2322
DOI
10.1038/s41598-019-45470-y
PMC
PMC6586778
Cited by
48
References
0
Language
en
Update notices
correction (2024-03-04)
Licence
Funders
Department of Science and Technology, Ministry of Science and Technology (DST/INT/JSPS/P-261/2017 dt. 16/10/17)

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