1887

Abstract

The alternative oxidase (AOX) is the terminal oxidase of the cyanide-resistant alternative respiratory pathway in plants and has been implicated in resistance to viruses. When tobacco mosaic virus (TMV) vectors were used to drive very high levels of expression of either AOX or AOX mutated in its active site (AOX-E), virus spread was enhanced. This was visualized as the induction of larger hypersensitive-response lesions after inoculation onto -genotype tobacco than those produced by vectors bearing sequences of comparable length [the green fluorescent protein () gene sequence or antisense ] or the ‘empty’ viral vector. Also, in the highly susceptible host , systemic movement of TMV vectors expressing AOX or AOX-E was faster than that of TMV constructs bearing or antisense sequences. Notably, in , TMV.AOX and TMV.AOX-E induced symptoms that were severe and ultimately included cell death, whereas the empty vector, TMV.GFP and the TMV vector expressing antisense sequences never induced necrosis. The results show that, if expressed at sufficiently high levels, active and inactive AOX proteins can affect virus spread and symptomology in plants.

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2004-12-01
2024-03-29
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References

  1. Abbink T. E. M., Peart J. R., Mos T. N. M., Baulcombe D. C., Bol J. F., Linthorst H. J. M. 2002; Silencing of a gene encoding a protein component of the oxygen-evolving complex of photosystem II enhances virus replication in plants. Virology 295:307–319 [CrossRef]
    [Google Scholar]
  2. Affourtit C., Krab K., Moore A. L. 2001; Control of plant mitochondrial respiration. BBA-Bioenergetics 1504:58–69 [CrossRef]
    [Google Scholar]
  3. Affourtit C., Albury M. S., Crichton P. G., Moore A. L. 2002; Exploring the molecular nature of alternative oxidase regulation and catalysis. FEBS Lett 510:121–126 [CrossRef]
    [Google Scholar]
  4. Albury M. S., Affourtit C., Moore A. L. 1998; A highly conserved glutamate residue (Glu-270) is essential for plant alternative oxidase activity. J Biol Chem 273:30301–30305 [CrossRef]
    [Google Scholar]
  5. Alexander D., Goodman R. M., Gut-Rella M. 8 other authors 1993; Increased tolerance to two oomycete pathogens in transgenic tobacco expressing pathogenesis-related protein 1a. Proc Natl Acad Sci U S A 90:7327–7331 [CrossRef]
    [Google Scholar]
  6. Balk J., Leaver C. J., McCabe P. F. 1999; Translocation of cytochrome c from the mitochondria to the cytosol occurs during heat-induced programmed cell death in cucumber plants. FEBS Lett 463:151–154 [CrossRef]
    [Google Scholar]
  7. Baulcombe D. 2001; RNA silencing: diced defence. Nature 409:295–296 [CrossRef]
    [Google Scholar]
  8. Birch P. R. J., Avrova A. O., Dellagi A., Lacomme C., Santa Cruz S., Lyon G. D. 2000; Programmed cell death in plants in response to pathogen attack. In Molecular Plant Pathology pp  175–197 Edited by Dickinson M., Beynon J. Sheffield, UK: Sheffield Academic Press;
    [Google Scholar]
  9. Cao H., Glazebrook J., Clarke J. D., Volko S., Dong X. 1997; The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88:57–63 [CrossRef]
    [Google Scholar]
  10. 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
    [Google Scholar]
  11. Chivasa S., Murphy A. M., Naylor M., Carr J. P. 1997; Salicylic acid interferes with tobacco mosaic virus replication via a novel salicylhydroxamic acid-sensitive mechanism. Plant Cell 9:547–557 [CrossRef]
    [Google Scholar]
  12. Creissen G., Firmin J., Fryer M. 8 other authors 1999; Elevated glutathione biosynthetic capacity in the chloroplasts of transgenic tobacco plants paradoxically causes increased oxidative stress. Plant Cell 11:1277–1291 [CrossRef]
    [Google Scholar]
  13. Cutt J. R., Harpster M. H., Dixon D. C., Carr J. P., Dunsmuir P., Klessig D. F. 1989; Disease response to tobacco mosaic virus in transgenic tobacco plants that constitutively express the pathogenesis-related PR1b gene. Virology 173:89–97 [CrossRef]
    [Google Scholar]
  14. Dempsey D. A., Shah J., Klessig D. F. 1999; Salicylic acid and disease resistance in plants. Crit Rev Plant Sci 18:547–575 [CrossRef]
    [Google Scholar]
  15. Després C., Chubak C., Rochon A., Clark R., Bethune T., Desveaux D., Fobert P. R. 2003; The Arabidopsis NPR1 disease resistance protein is a novel cofactor that confers redox regulation of DNA binding activity to the basic domain/leucine zipper transcription factor TGA1. Plant Cell 15:2181–2191 [CrossRef]
    [Google Scholar]
  16. 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]
    [Google Scholar]
  17. 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]
    [Google Scholar]
  18. Grant S. R. 1999; Dissecting the mechanisms of posttranscriptional gene silencing: divide and conquer. Cell 96:303–306 [CrossRef]
    [Google Scholar]
  19. Hansen G. 2000; Evidence for Agrobacterium -induced apoptosis in maize cells. Mol Plant-Microbe Interact 13:649–657 [CrossRef]
    [Google Scholar]
  20. Heath M. C. 2000; Hypersensitive response-related death. Plant Mol Biol 44:321–334 [CrossRef]
    [Google Scholar]
  21. 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]
    [Google Scholar]
  22. Lacomme C., Santa Cruz S. 1999; Bax-induced cell death in tobacco is similar to the hypersensitive response. Proc Natl Acad Sci U S A 96:7956–7961 [CrossRef]
    [Google Scholar]
  23. Lennon A. M., Neuenschwander U. H., Ribas-Carbo M., Giles L., Ryals J. A., Siedow J. N. 1997; The effects of salicylic acid and tobacco mosaic virus infection on the alternative oxidase of tobacco. Plant Physiol 115:783–791
    [Google Scholar]
  24. Linthorst H. J. M., van Loon L. C., van Rossum C. M. A., Mayer A., Bol J. F., van Roekel J. S. C., Meulenhoff E. J. S., Cornelissen B. J. C. 1990; Analysis of acidic and basic chitinases from tobacco and petunia and their constitutive expression in transgenic tobacco. Mol Plant-Microbe Interact 3:252–258 [CrossRef]
    [Google Scholar]
  25. Mauch F., Hadwiger L. A., Boller T. 1988; Antifungal hydrolases in pea tissue. I. Purification and characterization of two chitinases and two β -1,3-glucanases differentially regulated during development and in response to fungal infection. Plant Physiol 87:325–333 [CrossRef]
    [Google Scholar]
  26. Maxwell D. P., Wang Y., McIntosh L. 1999; The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc Natl Acad Sci U S A 96:8271–8276 [CrossRef]
    [Google Scholar]
  27. Moissiard G., Voinnet O. 2004; Viral suppression of RNA silencing in plants. Mol Plant Pathol 5:71–82 [CrossRef]
    [Google Scholar]
  28. Mou Z., Fan W., Dong X. 2003; Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113:935–944 [CrossRef]
    [Google Scholar]
  29. Murphy A. M., Carr J. P. 2002; Salicylic acid has cell-specific effects on Tobacco mosaic virus replication and cell-to-cell movement. Plant Physiol 128:552–563 [CrossRef]
    [Google Scholar]
  30. Murphy A. M., Chivasa S., Singh D. P., Carr J. P. 1999; Salicylic acid-induced resistance to viruses and other pathogens: a parting of the ways?. Trends Plant Sci 4:155–160 [CrossRef]
    [Google Scholar]
  31. Naylor M., Murphy A. M., Berry J. O., Carr J. P. 1998; Salicylic acid can induce resistance to plant virus movement. Mol Plant-Microbe Interact 11:860–868 [CrossRef]
    [Google Scholar]
  32. Noctor G., Foyer C. H. 1998; Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279 [CrossRef]
    [Google Scholar]
  33. Ordog S. H., Higgins V. J., Vanlerberghe G. C. 2002; Mitochondrial alternative oxidase is not a critical component of plant viral resistance but may play a role in the hypersensitive response. Plant Physiol 129:1858–1865 [CrossRef]
    [Google Scholar]
  34. Rabindran S., Dawson W. O. 2001; Assessment of recombinants that arise from the use of a TMV-based transient expression vector. Virology 284:182–189 [CrossRef]
    [Google Scholar]
  35. Raskin I., Ehmann A., Melander W. R., Meeuse B. J. D. 1987; Salicylic acid: a natural inducer of heat production in Arum lilies. Science 237:1601–1602 [CrossRef]
    [Google Scholar]
  36. Rhoads D. M., McIntosh L. 1992; Salicylic acid regulation of respiration in higher plants: alternative oxidase expression. Plant Cell 4:1131–1139 [CrossRef]
    [Google Scholar]
  37. Schlumbaum A., Mauch F., Vögeli U., Boller T. 1986; Plant chitinases are potent inhibitors of fungal growth. Nature 324:365–367 [CrossRef]
    [Google Scholar]
  38. Shivprasad S., Pogue G. P., Lewandowski D. J., Hidalgo J., Donson J., Grill L. K., Dawson W. O. 1999; Heterologous sequences greatly affect foreign gene expression in tobacco mosaic virus-based vectors. Virology 255:312–323 [CrossRef]
    [Google Scholar]
  39. 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]
    [Google Scholar]
  40. Thordal-Christensen H., Zhang Z., Wei Y., Collinge D. B. 1997; Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley–powdery mildew interaction. Plant J 11:1187–1194 [CrossRef]
    [Google Scholar]
  41. Umbach A. L., Siedow J. N. 1993; Covalent and noncovalent dimers of the cyanide-resistant alternative oxidase protein in higher plant mitochondria and their relationship to enzyme activity. Plant Physiol 103:845–854
    [Google Scholar]
  42. Vanlerberghe G. C., McIntosh L. 1997; Alternative oxidase: from gene to function. Annu Rev Plant Physiol Plant Mol Biol 48:703–734 [CrossRef]
    [Google Scholar]
  43. van Loon L. C., van Strien E. A. 1999; The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol Mol Plant Pathol 55:85–97 [CrossRef]
    [Google Scholar]
  44. Wong C. E., Carson R. A. J., 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]
    [Google Scholar]
  45. Xie Z., Fan B., Chen C., Chen Z. 2001; An important role of an inducible RNA-dependent RNA polymerase in plant antiviral defense. Proc Natl Acad Sci U S A 98:6516–6521 [CrossRef]
    [Google Scholar]
  46. Yang S.-J., Carter S. A., Cole A. B., Cheng N.-H., Nelson R. S. 2004; A natural variant of a host RNA-dependent RNA polymerase is associated with increased susceptibility to viruses by Nicotiana benthamiana . Proc Natl Acad Sci U S A 101:6297–6302 [CrossRef]
    [Google Scholar]
  47. Yip J. Y. H., Vanlerberghe G. C. 2001; Mitochondrial alternative oxidase acts to dampen the generation of active oxygen species during a period of rapid respiration induced to support a high rate of nutrient uptake. Physiol Plant 112:327–333 [CrossRef]
    [Google Scholar]
  48. Yu D., Fan B., MacFarlane S. A., Chen Z. 2003; Analysis of the involvement of an inducible Arabidopsis RNA-dependent RNA polymerase in antiviral defense. Mol Plant-Microbe Interact 16:206–216 [CrossRef]
    [Google Scholar]
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