1887

Abstract

Nitric oxide (NO) is an important defensive signal in plants but its effects on virus infection are not well understood. Administration of NO-releasing compounds immediately before inoculation of tobacco leaves with potato virus X and tobacco mosaic virus decreased the accumulation of virus, indicating that NO can induce resistance rapidly. Resistance induction was inhibited by co-administration with an NO-scavenging compound or when experiments were done in transgenic tobacco plants expressing increased alternative respiratory pathway capacity due to constitutive expression of the plant mitochondrial enzyme, alternative oxidase (AOX). These results indicate that NO, which inhibits electron transport chain activity, is triggering defensive signalling by inducing changes in mitochondrial reactive oxygen species levels that are in turn regulated by AOX. Experiments using -transgenic plants, which cannot accumulate the defensive plant hormone salicylic acid (SA) showed that NO rapidly induces resistance to virus infection independently of SA. However, this initial state of resistance may be transient. Subsequently, by 5 days post-treatment, NO had caused an increase in pathogenesis-related protein 1 (PR1) expression (a proxy for increased SA biosynthesis), which correlated with a longer-term state of resistance to virus infection. The induction by NO of PR1 accumulation was modified in -transgenic plants. This indicates that the influence of NO on defensive gene expression is in part mediated through its effects on mitochondria.

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2014-09-01
2020-01-24
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References

  1. Affourtit C., Krab K., Moore A. L.. ( 2001;). Control of plant mitochondrial respiration. . Biochim Biophys Acta 1504:, 58–69. [CrossRef][PubMed]
    [Google Scholar]
  2. Carr J. P., Lewsey M. G., Palukaitis P.. ( 2010;). Signaling in induced resistance. . Adv Virus Res 76:, 57–121. [CrossRef][PubMed]
    [Google Scholar]
  3. Chivasa S., Carr J. P.. ( 1998;). Cyanide restores N gene-mediated resistance to tobacco mosaic virus in transgenic tobacco expressing salicylic acid hydroxylase. . Plant Cell 10:, 1489–1498.[PubMed]
    [Google Scholar]
  4. Delledonne M., Xia Y., Dixon R. A., Lamb C.. ( 1998;). Nitric oxide functions as a signal in plant disease resistance. . Nature 394:, 585–588. [CrossRef][PubMed]
    [Google Scholar]
  5. Durner J., Wendehenne D., Klessig D. F.. ( 1998;). Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. . Proc Natl Acad Sci U S A 95:, 10328–10333. [CrossRef][PubMed]
    [Google Scholar]
  6. Dutilleul C., Garmier M., Noctor G., Mathieu C., Chétrit P., Foyer C. H., de Paepe R.. ( 2003;). Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation. . Plant Cell 15:, 1212–1226. [CrossRef][PubMed]
    [Google Scholar]
  7. Ederli L., Morettini R., Borgogni A., Wasternack C., Miersch O., Reale L., Ferranti F., Tosti N., Pasqualini S.. ( 2006;). Interaction between nitric oxide and ethylene in the induction of alternative oxidase in ozone-treated tobacco plants. . Plant Physiol 142:, 595–608. [CrossRef][PubMed]
    [Google Scholar]
  8. Feechan A., Kwon E., Yun B. W., Wang Y., Pallas J. A., Loake G. J.. ( 2005;). A central role for S-nitrosothiols in plant disease resistance. . Proc Natl Acad Sci U S A 102:, 8054–8059. [CrossRef][PubMed]
    [Google Scholar]
  9. Fu L. J., Shi K., Gu M., Zhou Y. H., Dong D. K., Liang W. S., Song F. M., Yu J. Q.. ( 2010;). Systemic induction and role of mitochondrial alternative oxidase and nitric oxide in a compatible tomato–Tobacco mosaic virus interaction. . Mol Plant Microbe Interact 23:, 39–48. [CrossRef][PubMed]
    [Google Scholar]
  10. Gaffney T., Friedrich L., Vernooij B., Negrotto D., Nye G., Uknes S., Ward E., Kessmann H., Ryals J.. ( 1993;). Requirement of salicylic acid for the induction of systemic acquired resistance. . Science 261:, 754–756. [CrossRef][PubMed]
    [Google Scholar]
  11. Gilliland A., Singh D. P., Hayward J. M., Moore C. A., Murphy A. M., York C. J., Slator J., Carr J. P.. ( 2003;). Genetic modification of alternative respiration has differential effects on antimycin A-induced versus salicylic acid-induced resistance to Tobacco mosaic virus. . Plant Physiol 132:, 1518–1528. [CrossRef][PubMed]
    [Google Scholar]
  12. Gupta K. J., Fernie A. R., Kaiser W. M., van Dongen J. T.. ( 2011;). On the origins of nitric oxide. . Trends Plant Sci 16:, 160–168. [CrossRef][PubMed]
    [Google Scholar]
  13. Gupta K. J., Igamberdiev A. U., Mur L. A. J.. ( 2012;). NO and ROS homeostasis in mitochondria: a central role for alternative oxidase. . New Phytol 195:, 1–3. [CrossRef][PubMed]
    [Google Scholar]
  14. Huang X., von Rad U., Durner J.. ( 2002;). Nitric oxide induces transcriptional activation of the nitric oxide-tolerant alternative oxidase in Arabidopsis suspension cells. . Planta 215:, 914–923. [CrossRef][PubMed]
    [Google Scholar]
  15. Hunter L. J. R., Westwood J. H., Heath G., Macaulay K., Smith A. G., Macfarlane S. A., Palukaitis P., Carr J. P.. ( 2013;). Regulation of RNA-dependent RNA polymerase 1 and isochorismate synthase gene expression in Arabidopsis. . PLoS ONE 8:, e66530. [CrossRef][PubMed]
    [Google Scholar]
  16. Kachroo P., Yoshioka K., Shah J., Dooner H. K., Klessig D. F.. ( 2000;). Resistance to turnip crinkle virus in Arabidopsis is regulated by two host genes and is salicylic acid dependent but NPR1, ethylene, and jasmonate independent. . Plant Cell 12:, 677–690. [CrossRef][PubMed]
    [Google Scholar]
  17. Köhm B. A., Goulden M. G., Gilbert J. E., Kavanagh T. A., Baulcombe D. C.. ( 1993;). A potato virus X resistance gene mediates an induced, non-specific resistance in protoplasts. . Plant Cell 5:, 913–920. [CrossRef][PubMed]
    [Google Scholar]
  18. Lee W. S., Fu S. F., Verchot-Lubicz J., Carr J. P.. ( 2011;). Genetic modification of alternative respiration in Nicotiana benthamiana affects basal and salicylic acid-induced resistance to potato virus X. . BMC Plant Biol 11:, 41. [CrossRef][PubMed]
    [Google Scholar]
  19. Liao Y. W. K., Sun Z. H., Zhou Y. H., Shi K., Li X., Zhang G. Q., Xia X. J., Chen Z. X., Yu J. Q.. ( 2013;). The role of hydrogen peroxide and nitric oxide in the induction of plant-encoded RNA-dependent RNA polymerase 1 in the basal defense against Tobacco mosaic virus. . PLoS ONE 8:, e76090. [CrossRef][PubMed]
    [Google Scholar]
  20. Love A. J., Yun B. W., Laval V., Loake G. J., Milner J. J.. ( 2005;). Cauliflower mosaic virus, a compatible pathogen of Arabidopsis, engages three distinct defense-signaling pathways and activates rapid systemic generation of reactive oxygen species. . Plant Physiol 139:, 935–948. [CrossRef][PubMed]
    [Google Scholar]
  21. Love A. J., Laval V., Geri C., Laird J., Tomos A. D., Hooks M. A., Milner J. J.. ( 2007;). Components of Arabidopsis defense- and ethylene-signaling pathways regulate susceptibility to Cauliflower mosaic virus by restricting long-distance movement. . Mol Plant Microbe Interact 20:, 659–670. [CrossRef][PubMed]
    [Google Scholar]
  22. Ma H., Song C., Borth W., Sether D., Melzer M., Hu J.. ( 2011;). Modified expression of alternative oxidase in transgenic tomato and petunia affects the level of tomato spotted wilt virus resistance. . BMC Biotechnol 11:, 96. [CrossRef][PubMed]
    [Google Scholar]
  23. Mailloux R. J., McBride S. L., Harper M. E.. ( 2013;). Unearthing the secrets of mitochondrial ROS and glutathione in bioenergetics. . Trends Biochem Sci 38:, 592–602. [CrossRef][PubMed]
    [Google Scholar]
  24. Moffett P.. ( 2009;). Mechanisms of recognition in dominant R gene mediated resistance. . Adv Virus Res 75:, 1–33, 228–229. [CrossRef][PubMed]
    [Google Scholar]
  25. Moreau M., Lindermayr C., Durner J., Klessig D. F.. ( 2010;). NO synthesis and signaling in plants – where do we stand?. Physiol Plant 138:, 372–383. [CrossRef][PubMed]
    [Google Scholar]
  26. Mur L. A. J., Prats E., Pierre S., Hall M. A., Hebelstrup K. H.. ( 2013;). Integrating nitric oxide into salicylic acid and jasmonic acid/ethylene plant defense pathways. . Front Plant Sci 4:, 215. [CrossRef][PubMed]
    [Google Scholar]
  27. Murphy A. M., Gilliland A., York C. J., Hyman B., Carr J. P.. ( 2004;). High-level expression of alternative oxidase protein sequences enhances the spread of viral vectors in resistant and susceptible plants. . J Gen Virol 85:, 3777–3786. [CrossRef][PubMed]
    [Google Scholar]
  28. Norman C., Howell K. A., Millar A. H., Whelan J. M., Day D. A.. ( 2004;). Salicylic acid is an uncoupler and inhibitor of mitochondrial electron transport. . Plant Physiol 134:, 492–501. [CrossRef][PubMed]
    [Google Scholar]
  29. Palukaitis P., Groen S. C., Carr J. P.. ( 2013;). The Rumsfeld paradox: some of the things we know that we don’t know about plant virus infection. . Curr Opin Plant Biol 16:, 513–519. [CrossRef][PubMed]
    [Google Scholar]
  30. Pandey S. P., Baldwin I. T.. ( 2007;). RNA-directed RNA polymerase 1 (RdR1) mediates the resistance of Nicotiana attenuata to herbivore attack in nature. . Plant J 50:, 40–53. [CrossRef][PubMed]
    [Google Scholar]
  31. Scheler C., Durner J., Astier J.. ( 2013;). Nitric oxide and reactive oxygen species in plant biotic interactions. . Curr Opin Plant Biol 16:, 534–539. [CrossRef][PubMed]
    [Google Scholar]
  32. Singh D. P., Moore C. A., Gilliland A., Carr J. P.. ( 2004;). Activation of multiple antiviral defence mechanisms by salicylic acid. . Mol Plant Pathol 5:, 57–63. [CrossRef][PubMed]
    [Google Scholar]
  33. Song F. M., Goodman R. M.. ( 2001;). Activity of nitric oxide is dependent on, but is partially required for function of, salicylic acid in the signaling pathway in tobacco systemic acquired resistance. . Mol Plant Microbe Interact 14:, 1458–1462. [CrossRef][PubMed]
    [Google Scholar]
  34. Tada Y., Spoel S. H., Pajerowska-Mukhtar K., Mou Z. L., Song J. Q., Wang C., Zuo J. R., Dong X. N.. ( 2008;). Plant immunity requires conformational charges of NPR1 via S-nitrosylation and thioredoxins. . Science 321:, 952–956. [CrossRef][PubMed]
    [Google Scholar]
  35. Vernooij B., Friedrich L., Ahl Goy P., Staub T., Kessmann H., Ryals J. A.. ( 1995;). 2,6-Dichloroisonicotinic acid-induced resistance to pathogens without the accumulation of salicylic acid. . Mol Plant Microbe Interact 8:, 228–234. [CrossRef]
    [Google Scholar]
  36. Wong C. E., Carson R. A., Carr J. P.. ( 2002;). Chemically induced virus resistance in Arabidopsis thaliana is independent of pathogenesis-related protein expression and the NPR1 gene. . Mol Plant Microbe Interact 15:, 75–81. [CrossRef][PubMed]
    [Google Scholar]
  37. Wulff A., Oliveira H. C., Saviani E. E., Salgado I.. ( 2009;). Nitrite reduction and superoxide-dependent nitric oxide degradation by Arabidopsis mitochondria: influence of external NAD(P)H dehydrogenases and alternative oxidase in the control of nitric oxide levels. . Nitric Oxide 21:, 132–139. [CrossRef][PubMed]
    [Google Scholar]
  38. Xu T., Zhang L., Zhen J., Fan Y., Zhang C., Wang L.. ( 2013;). Expressional and regulatory characterization of Arabidopsis RNA-dependent RNA polymerase 1. . Planta 237:, 1561–1569. [CrossRef][PubMed]
    [Google Scholar]
  39. Yun B. W., Feechan A., Yin M., Saidi N. B. B., Le Bihan T., Yu M., Moore J. W., Kang J. G., Kwon E.. & other authors ( 2011;). S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. . Nature 478:, 264–268. [CrossRef][PubMed]
    [Google Scholar]
  40. Zhang L., Oh Y., Li H. Y., Baldwin I. T., Galis I.. ( 2012;). Alternative oxidase in resistance to biotic stresses: Nicotiana attenuata AOX contributes to resistance to a pathogen and a piercing–sucking insect but not Manduca sexta larvae. . Plant Physiol 160:, 1453–1467. [CrossRef][PubMed]
    [Google Scholar]
  41. Zhou T., Murphy A. M., Lewsey M. G., Westwood J. H., Zhang H. M., González I., Canto T., Carr J. P.. ( 2014;). Domains of the cucumber mosaic virus 2b silencing suppressor protein affecting inhibition of salicylic acid-induced resistance and priming of salicylic acid accumulation during infection. . J Gen Virol 95:, 1408–1413. [CrossRef][PubMed]
    [Google Scholar]
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