High-level expression of alternative oxidase protein sequences enhances the spread of viral vectors in resistant and susceptible plants.

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 NN-genotype tobacco than those produced by vectors bearing sequences of comparable length [the green fluorescent protein (gfp) gene sequence or antisense aox] or the 'empty' viral vector. Also, in the highly susceptible host Nicotiana benthamiana, systemic movement of TMV vectors expressing AOX or AOX-E was faster than that of TMV constructs bearing gfp or antisense aox sequences. Notably, in N. benthamiana, 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 aox 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.

[1]  Richard S Nelson,et al.  A natural variant of a host RNA-dependent RNA polymerase is associated with increased susceptibility to viruses by Nicotiana benthamiana. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[2]  M. C. Heath.  Hypersensitive response-related death , 2000, Plant Molecular Biology.

[3]  J. Carr,et al.  Activation of multiple antiviral defence mechanisms by salicylic acid. , 2004, Molecular plant pathology.

[4]  O. Voinnet,et al.  Viral suppression of RNA silencing in plants. , 2004, Molecular plant pathology.

[5]  Darrell Desveaux,et al.  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 Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.012849. , 2003, The Plant Cell Online.

[6]  J. Carr,et al.  Genetic Modification of Alternative Respiration Has Differential Effects on Antimycin A-Induced versus Salicylic Acid-Induced Resistance to Tobacco mosaic virus1 , 2003, Plant Physiology.

[7]  Xinnian Dong,et al.  Inducers of Plant Systemic Acquired Resistance Regulate NPR1 Function through Redox Changes , 2003, Cell.

[8]  C. Foyer,et al.  Leaf Mitochondria Modulate Whole Cell Redox Homeostasis, Set Antioxidant Capacity, and Determine Stress Resistance through Altered Signaling and Diurnal Regulation Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.009464. , 2003, The Plant Cell Online.

[9]  Diqiu Yu,et al.  Analysis of the involvement of an inducible Arabidopsis RNA-dependent RNA polymerase in antiviral defense. , 2003, Molecular plant-microbe interactions : MPMI.

[10]  V. Higgins,et al.  Mitochondrial Alternative Oxidase Is Not a Critical Component of Plant Viral Resistance But May Play a Role in the Hypersensitive Response1 , 2002, Plant Physiology.

[11]  D. Baulcombe,et al.  Silencing of a gene encoding a protein component of the oxygen-evolving complex of photosystem II enhances virus replication in plants. , 2002, Virology.

[12]  J. Carr,et al.  Salicylic Acid Has Cell-Specific Effects on Tobacco mosaic virus Replication and Cell-to-Cell Movement1 , 2002, Plant Physiology.

[13]  Paul G Crichton,et al.  Exploring the molecular nature of alternative oxidase regulation and catalysis , 2002, FEBS letters.

[14]  J. Carr,et al.  Chemically induced virus resistance in Arabidopsis thaliana is independent of pathogenesis-related protein expression and the NPR1 gene. , 2002, Molecular plant-microbe interactions : MPMI.

[15]  G. Vanlerberghe,et al.  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. , 2001, Physiologia plantarum.

[16]  W. Dawson,et al.  Assessment of recombinants that arise from the use of a TMV-based transient expression vector. , 2001, Virology.

[17]  B. Fan,et al.  An important role of an inducible RNA-dependent RNA polymerase in plant antiviral defense , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[18]  K. Krab,et al.  Control of plant mitochondrial respiration. , 2001, Biochimica et biophysica acta.

[19]  D. Baulcombe.  RNA silencing: Diced defence , 2001, Nature.

[20]  G. Hansen.  Evidence for Agrobacterium-induced apoptosis in maize cells. , 2000, Molecular plant-microbe interactions : MPMI.

[21]  D. Klessig,et al.  Resistance to Turnip Crinkle Virus in Arabidopsis Is Regulated by Two Host Genes and Is Salicylic Acid Dependent but NPR1, Ethylene, and Jasmonate Independent , 2000, Plant Cell.

[22]  J. Balk,et al.  Translocation of cytochrome c from the mitochondria to the cytosol occurs during heat‐induced programmed cell death in cucumber plants , 1999, FEBS letters.

[23]  L. C. Loon,et al.  The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins , 1999 .

[24]  L. Mcintosh,et al.  The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[25]  S. Santa Cruz,et al.  Bax-induced cell death in tobacco is similar to the hypersensitive response. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[26]  Jyoti Shah,et al.  Salicylic acid and disease resistance in plants. , 1999 .

[27]  A. Wellburn,et al.  Elevated Glutathione Biosynthetic Capacity in the Chloroplasts of Transgenic Tobacco Plants Paradoxically Causes Increased Oxidative Stress , 1999, Plant Cell.

[28]  Singh,et al.  Salicylic acid-induced resistance to viruses and other pathogens: a parting of the ways? , 1999, Trends in plant science.

[29]  D. J. Lewandowski,et al.  Heterologous sequences greatly affect foreign gene expression in tobacco mosaic virus-based vectors. , 1999, Virology.

[30]  S. Grant,et al.  Dissecting the Mechanisms of Posttranscriptional Gene Silencing Divide and Conquer , 1999, Cell.

[31]  A. Moore,et al.  A Highly Conserved Glutamate Residue (Glu-270) Is Essential for Plant Alternative Oxidase Activity* , 1998, The Journal of Biological Chemistry.

[32]  J. O. Berry,et al.  Salicylic Acid Can Induce Resistance to Plant Virus Movement , 1998 .

[33]  J. Carr,et al.  Cyanide Restores N Gene–Mediated Resistance to Tobacco Mosaic Virus in Transgenic Tobacco Expressing Salicylic Acid Hydroxylase , 1998, Plant Cell.

[34]  C. Foyer,et al.  ASCORBATE AND GLUTATHIONE: Keeping Active Oxygen Under Control. , 1998, Annual review of plant physiology and plant molecular biology.

[35]  David B. Collinge,et al.  Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley—powdery mildew interaction , 1997 .

[36]  M. Ribas-Carbó,et al.  The Effects of Salicylic Acid and Tobacco Mosaic Virus Infection on the Alternative Oxidase of Tobacco , 1997, Plant physiology.

[37]  L. Mcintosh,et al.  ALTERNATIVE OXIDASE: From Gene to Function. , 1997, Annual review of plant physiology and plant molecular biology.

[38]  J. Carr,et al.  Salicylic Acid Interferes with Tobacco Mosaic Virus Replication via a Novel Salicylhydroxamic Acid-Sensitive Mechanism. , 1997, The Plant cell.

[39]  Jane Glazebrook,et al.  The Arabidopsis NPR1 Gene That Controls Systemic Acquired Resistance Encodes a Novel Protein Containing Ankyrin Repeats , 1997, Cell.

[40]  J. Siedow,et al.  Covalent and Noncovalent Dimers of the Cyanide-Resistant Alternative Oxidase Protein in Higher Plant Mitochondria and Their Relationship to Enzyme Activity , 1993, Plant physiology.

[41]  E. Ward,et al.  Increased tolerance to two oomycete pathogens in transgenic tobacco expressing pathogenesis-related protein 1a. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[42]  L. Mcintosh,et al.  Salicylic Acid Regulation of Respiration in Higher Plants: Alternative Oxidase Expression. , 1992, The Plant cell.

[43]  L. C. van Loon,et al.  Analysis of acidic and basic chitinases from tobacco and petunia and their constitutive expression in transgenic tobacco. , 1990, Molecular plant-microbe interactions : MPMI.

[44]  D F Klessig,et al.  Disease response to tobacco mosaic virus in transgenic tobacco plants that constitutively express the pathogenesis-related PR1b gene. , 1989, Virology.

[45]  T. Boller,et al.  Antifungal Hydrolases in Pea Tissue : II. Inhibition of Fungal Growth by Combinations of Chitinase and beta-1,3-Glucanase. , 1988, Plant physiology.

[46]  T. Boller,et al.  Antifungal Hydrolases in Pea Tissue : I. Purification and Characterization of Two Chitinases and Two beta-1,3-Glucanases Differentially Regulated during Development and in Response to Fungal Infection. , 1988, Plant physiology.

[47]  I. Raskin,et al.  Salicylic Acid: A Natural Inducer of Heat Production in Arum Lilies , 1987, Science.

[48]  T. Boller,et al.  Plant chitinases are potent inhibitors of fungal growth , 1986, Nature.