Home LiteratureArticle Details
PMID: 22286136 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Glycolate oxidase modulates reactive oxygen species-mediated signal transduction during nonhost resistance in Nicotiana benthamiana and Arabidopsis.

The Plant cell ·Vol. 24 ·No. 1 ·2012-01-00 ·Pages 336-52

Rojas CM, Senthil-Kumar M, Wang K, Ryu CM, Kaundal A, Mysore KS

Abstract

In contrast to gene-for-gene disease resistance, nonhost resistance governs defense responses to a broad range of potential pathogen species. To identify specific genes involved in the signal transduction cascade associated with nonhost disease resistance, we used a virus-induced gene-silencing screen in Nicotiana benthamiana, and identified the peroxisomal enzyme glycolate oxidase (GOX) as an essential component of nonhost resistance. GOX-silenced N. benthamiana and Arabidopsis thaliana GOX T-DNA insertion mutants are compromised for nonhost resistance. Moreover, Arabidopsis gox mutants have lower H(2)O(2) accumulation, reduced callose deposition, and reduced electrolyte leakage upon inoculation with hypersensitive response-causing nonhost pathogens. Arabidopsis gox mutants were not affected in NADPH oxidase activity, and silencing of a gene encoding NADPH oxidase (Respiratory burst oxidase homolog) in the gox mutants did not further increase susceptibility to nonhost pathogens, suggesting that GOX functions independently from NADPH oxidase. In the two gox mutants examined (haox2 and gox3), the expression of several defense-related genes upon nonhost pathogen inoculation was decreased compared with wild-type plants. Here we show that GOX is an alternative source for the production of H(2)O(2) during both gene-for-gene and nonhost resistance responses.

MeSH Terms
Alcohol Oxidoreductases/genetics,metabolism Arabidopsis/enzymology,genetics,immunology,microbiology Gene Expression Regulation, Plant/genetics,physiology Molecular Sequence Data Plant Diseases/genetics,immunology,microbiology Plant Immunity/genetics,physiology Plants, Genetically Modified/enzymology,genetics,immunology,microbiology Pseudomonas syringae/pathogenicity Reactive Oxygen Species/metabolism Signal Transduction/genetics,physiology Tobacco/enzymology,genetics,immunology,microbiology
Chemicals
Reactive Oxygen Species Alcohol Oxidoreductases glycollate oxidase
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Rojas Clemencia M
Plant Biology Division, Samuel Roberts Noble Foundation, Ardmore, Oklahoma 73402, USA.
Senthil-Kumar Muthappa
Wang Keri
Ryu Choong-Min
Kaundal Amita
Mysore Kirankumar S
References (80)
80 references, click to expand
  1. Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response.
    Proc Natl Acad Sci U S A. 2002 Jan 8;99(1):517-22 PMID: 11756663
  2. COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility.
    Science. 1998 May 15;280(5366):1091-4 PMID: 9582125
  3. Initiation of Plant Disease Resistance by Physical Interaction of AvrPto and Pto Kinase
    Science. 1996 Dec 20;274(5295):2060-3 PMID: 8953033
  4. Ethylene-insensitive tobacco lacks nonhost resistance against soil-borne fungi.
    Proc Natl Acad Sci U S A. 1998 Feb 17;95(4):1933-7 PMID: 9465120
  5. Plant eR genes that encode photorespiratory enzymes confer resistance against disease.
    Plant Cell. 2004 Jan;16(1):172-84 PMID: 14688292
  6. The white barley mutant albostrians shows a supersusceptible but symptomless interaction phenotype with the hemibiotrophic fungus Bipolaris sorokiniana.
    Mol Plant Microbe Interact. 2004 Apr;17(4):366-73 PMID: 15077669
  7. Identification of a new Arabidopsis disease resistance locus, RPs4, and cloning of the corresponding avirulence gene, avrRps4, from Pseudomonas syringae pv. pisi.
    Mol Plant Microbe Interact. 1996 Jan;9(1):55-61 PMID: 8589423
  8. Arabidopsis seedling flood-inoculation technique: a rapid and reliable assay for studying plant-bacterial interactions.
    Plant Methods. 2011 Oct 06;7:32 PMID: 21978451
  9. Identification of a disease resistance locus in Arabidopsis that is functionally homologous to the RPG1 locus of soybean.
    Plant J. 1993 Nov;4(5):813-20 PMID: 8275100
  10. Virus-induced silencing of WIPK and SIPK genes reduces resistance to a bacterial pathogen, but has no effect on the INF1-induced hypersensitive response (HR) in Nicotiana benthamiana.
    Mol Genet Genomics. 2003 Aug;269(5):583-91 PMID: 12838412
  11. Arabidopsis SENESCENCE-ASSOCIATED GENE101 stabilizes and signals within an ENHANCED DISEASE SUSCEPTIBILITY1 complex in plant innate immunity.
    Plant Cell. 2005 Sep;17(9):2601-13 PMID: 16040633
  12. Arabidopsis RAR1 exerts rate-limiting control of R gene-mediated defenses against multiple pathogens.
    Plant Cell. 2002 May;14(5):979-92 PMID: 12034891
  13. HopPtoN is a Pseudomonas syringae Hrp (type III secretion system) cysteine protease effector that suppresses pathogen-induced necrosis associated with both compatible and incompatible plant interactions.
    Mol Microbiol. 2004 Oct;54(2):353-65 PMID: 15469508
  14. Reactive oxygen species in plant cell death.
    Plant Physiol. 2006 Jun;141(2):384-90 PMID: 16760492
  15. Fast forward genetics based on virus-induced gene silencing.
    Curr Opin Plant Biol. 1999 Apr;2(2):109-13 PMID: 10322199
  16. An Arabidopsis thaliana T-DNA mutagenized population (GABI-Kat) for flanking sequence tag-based reverse genetics.
    Plant Mol Biol. 2003 Sep;53(1-2):247-59 PMID: 14756321
  17. Disease resistance conferred by expression of a gene encoding H2O2-generating glucose oxidase in transgenic potato plants.
    Plant Cell. 1995 Sep;7(9):1357-68 PMID: 8589621
  18. Nonhost resistance and nonspecific plant defenses.
    Curr Opin Plant Biol. 2000 Aug;3(4):315-9 PMID: 10873843
  19. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response.
    Cell. 1994 Nov 18;79(4):583-93 PMID: 7954825
  20. Peroxisomal hydrogen peroxide is coupled to biotic defense responses by ISOCHORISMATE SYNTHASE1 in a daylength-related manner.
    Plant Physiol. 2010 Aug;153(4):1692-705 PMID: 20543092
  21. AraPerox. A database of putative Arabidopsis proteins from plant peroxisomes.
    Plant Physiol. 2004 Sep;136(1):2587-608 PMID: 15333753
  22. Reactive oxygen species signaling in response to pathogens.
    Plant Physiol. 2006 Jun;141(2):373-8 PMID: 16760490
  23. PAD4 functions upstream from salicylic acid to control defense responses in Arabidopsis.
    Plant Cell. 1998 Jun;10(6):1021-30 PMID: 9634589
  24. A novel class of elicitin-like genes from Phytophthora infestans.
    Mol Plant Microbe Interact. 1997 Nov;10(8):1028-30 PMID: 9353948
  25. A bacterial virulence protein suppresses host innate immunity to cause plant disease.
    Science. 2006 Jul 14;313(5784):220-3 PMID: 16840699
  26. Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants.
    J Exp Bot. 2006;57(3):449-59 PMID: 16397003
  27. The receptor for the fungal elicitor ethylene-inducing xylanase is a member of a resistance-like gene family in tomato.
    Plant Cell. 2004 Jun;16(6):1604-15 PMID: 15155877
  28. Arabidopsis non-host resistance to powdery mildews.
    Curr Opin Plant Biol. 2008 Aug;11(4):404-11 PMID: 18499508
  29. Arabidopsis thaliana-derived resistance against Leptosphaeria maculans in a Brassica napus genomic background.
    Theor Appl Genet. 2002 Sep;105(4):498-504 PMID: 12582497
  30. Dual roles of reactive oxygen species and NADPH oxidase RBOHD in an Arabidopsis-Alternaria pathosystem.
    Plant Physiol. 2009 Nov;151(3):1459-75 PMID: 19726575
  31. NPR1, all things considered.
    Curr Opin Plant Biol. 2004 Oct;7(5):547-52 PMID: 15337097
  32. Insights into nonhost disease resistance: can they assist disease control in agriculture?
    Plant Cell. 2006 Mar;18(3):523-8 PMID: 16513603
  33. Ethylene-insensitive tobacco shows differentially altered susceptibility to different pathogens.
    Phytopathology. 2003 Jul;93(7):813-21 PMID: 18943162
  34. Virus-induced gene silencing in plants.
    Methods. 2003 Aug;30(4):296-303 PMID: 12828943
  35. The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli.
    Sci Signal. 2009 Aug 18;2(84):ra45 PMID: 19690331
  36. Identification and characterization of plant genes involved in Agrobacterium-mediated plant transformation by virus-induced gene silencing.
    Mol Plant Microbe Interact. 2007 Jan;20(1):41-52 PMID: 17249421
  37. Involvement of plasma-membrane NADPH oxidase in abscisic acid- and water stress-induced antioxidant defense in leaves of maize seedlings.
    Planta. 2002 Oct;215(6):1022-30 PMID: 12355163
  38. Nicotiana benthamiana gp91phox homologs NbrbohA and NbrbohB participate in H2O2 accumulation and resistance to Phytophthora infestans.
    Plant Cell. 2003 Mar;15(3):706-18 PMID: 12615943
  39. Deletions in the repertoire of Pseudomonas syringae pv. tomato DC3000 type III secretion effector genes reveal functional overlap among effectors.
    PLoS Pathog. 2009 Apr;5(4):e1000388 PMID: 19381254
  40. Roles of Arabidopsis WRKY3 and WRKY4 transcription factors in plant responses to pathogens.
    BMC Plant Biol. 2008 Jun 20;8:68 PMID: 18570649
  41. Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana.
    Nat Genet. 2005 Oct;37(10):1130-4 PMID: 16170317
  42. Monitoring in planta bacterial infection at both cellular and whole-plant levels using the green fluorescent protein variant GFPuv.
    New Phytol. 2007;174(1):212-223 PMID: 17335510
  43. Resistance of nicotiana benthamiana to phytophthora infestans is mediated by the recognition of the elicitor protein INF1
    Plant Cell. 1998 Sep;10(9):1413-26 PMID: 9724689
  44. T-DNA mutagenesis in Arabidopsis.
    Methods Mol Biol. 2003;236:177-88 PMID: 14501065
  45. GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox.
    Plant Physiol. 2004 Sep;136(1):2621-32 PMID: 15375207
  46. High-throughput in planta expression screening identifies a class II ethylene-responsive element binding factor-like protein that regulates plant cell death and non-host resistance.
    Plant J. 2005 Aug;43(4):491-505 PMID: 16098104
  47. Agroinfiltration is a versatile tool that facilitates comparative analyses of Avr9/Cf-9-induced and Avr4/Cf-4-induced necrosis.
    Mol Plant Microbe Interact. 2000 Apr;13(4):439-46 PMID: 10755307
  48. Arabidopsis PAD3, a gene required for camalexin biosynthesis, encodes a putative cytochrome P450 monooxygenase.
    Plant Cell. 1999 Dec;11(12):2419-28 PMID: 10590168
  49. Use of Arabidopsis for genetic dissection of plant defense responses.
    Annu Rev Genet. 1997;31:547-69 PMID: 9442907
  50. An investigation into the involvement of defense signaling pathways in components of the nonhost resistance of Arabidopsis thaliana to rust fungi also reveals a model system for studying rust fungal compatibility.
    Mol Plant Microbe Interact. 2003 May;16(5):398-404 PMID: 12744510
  51. Host and non-host pathogens elicit different jasmonate/ethylene responses in Arabidopsis.
    Plant J. 2004 Dec;40(5):633-46 PMID: 15546348
  52. Photorespiratory metabolism: genes, mutants, energetics, and redox signaling.
    Annu Rev Plant Biol. 2009;60:455-84 PMID: 19575589
  53. The AtrbohD-mediated oxidative burst elicited by oligogalacturonides in Arabidopsis is dispensable for the activation of defense responses effective against Botrytis cinerea.
    Plant Physiol. 2008 Nov;148(3):1695-706 PMID: 18790995
  54. Genetic analysis of ethylene signal transduction in Arabidopsis thaliana: five novel mutant loci integrated into a stress response pathway.
    Genetics. 1995 Mar;139(3):1393-409 PMID: 7768447
  55. Nonhost resistance: how much do we know?
    Trends Plant Sci. 2004 Feb;9(2):97-104 PMID: 15102376
  56. A comprehensive analysis of hydrogen peroxide-induced gene expression in tobacco.
    Proc Natl Acad Sci U S A. 2003 Dec 23;100(26):16113-8 PMID: 14671332
  57. Tobacco Rar1, EDS1 and NPR1/NIM1 like genes are required for N-mediated resistance to tobacco mosaic virus.
    Plant J. 2002 May;30(4):415-29 PMID: 12028572
  58. Virus-induced gene silencing in tomato.
    Plant J. 2002 Sep;31(6):777-86 PMID: 12220268
  59. Recognition specificity for the bacterial avirulence protein AvrPto is determined by Thr-204 in the activation loop of the tomato Pto kinase.
    Mol Cell. 1998 Aug;2(2):241-5 PMID: 9734361
  60. Hydrogen peroxide and nitric oxide as signalling molecules in plants.
    J Exp Bot. 2002 May;53(372):1237-47 PMID: 11997372
  61. Expression of spinach glycolate oxidase in Saccharomyces cerevisiae: purification and characterization.
    Biochemistry. 1991 May 7;30(18):4612-9 PMID: 1850628
  62. Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis.
    Science. 2005 Nov 18;310(5751):1180-3 PMID: 16293760
  63. A virus-induced gene silencing screen identifies a role for Thylakoid Formation1 in Pseudomonas syringae pv tomato symptom development in tomato and Arabidopsis.
    Plant Physiol. 2010 Jan;152(1):281-92 PMID: 19915014
  64. Deficiency in phytoalexin production causes enhanced susceptibility of Arabidopsis thaliana to the fungus Alternaria brassicicola.
    Plant J. 1999 Jul;19(2):163-71 PMID: 10476063
  65. Acquired Resistance Signal Transduction in Arabidopsis Is Ethylene Independent.
    Plant Cell. 1994 May;6(5):581-588 PMID: 12244251
  66. Isolation of Arabidopsis mutants with enhanced disease susceptibility by direct screening.
    Genetics. 1996 Jun;143(2):973-82 PMID: 8725243
  67. Characterization of nonhost resistance of Arabidopsis to the Asian soybean rust.
    Mol Plant Microbe Interact. 2008 Nov;21(11):1421-30 PMID: 18842092
  68. The plant immune system.
    Nature. 2006 Nov 16;444(7117):323-9 PMID: 17108957
  69. AtRbohF is a crucial modulator of defence-associated metabolism and a key actor in the interplay between intracellular oxidative stress and pathogenesis responses in Arabidopsis.
    Plant J. 2012 Feb;69(4):613-27 PMID: 21985584
  70. Pathogenicity of Pseudomonas syringae pv. tomato on tomato seedlings: phenotypic and gene expression analyses of the virulence function of coronatine.
    Mol Plant Microbe Interact. 2008 Apr;21(4):383-95 PMID: 18321184
  71. Superoxide production by plant homologues of the gp91(phox) NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection.
    Plant Physiol. 2001 Jul;126(3):1281-90 PMID: 11457979
  72. The disease resistance signaling components EDS1 and PAD4 are essential regulators of the cell death pathway controlled by LSD1 in Arabidopsis.
    Plant Cell. 2001 Oct;13(10):2211-24 PMID: 11595797
  73. Coordinated plant defense responses in Arabidopsis revealed by microarray analysis.
    Proc Natl Acad Sci U S A. 2000 Oct 10;97(21):11655-60 PMID: 11027363
  74. Why are literature data for H2O2 contents so variable? A discussion of potential difficulties in the quantitative assay of leaf extracts.
    J Exp Bot. 2008;59(2):135-46 PMID: 18332224
  75. Interplay of the Arabidopsis nonhost resistance gene NHO1 with bacterial virulence.
    Proc Natl Acad Sci U S A. 2003 Mar 18;100(6):3519-24 PMID: 12626746
  76. Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins.
    Cell. 1997 Jun 27;89(7):1133-44 PMID: 9215635
  77. MAPKKKalpha is a positive regulator of cell death associated with both plant immunity and disease.
    EMBO J. 2004 Aug 4;23(15):3072-82 PMID: 15272302
  78. THE OXIDATIVE BURST IN PLANT DISEASE RESISTANCE.
    Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48:251-275 PMID: 15012264
  79. PLANT DISEASE RESISTANCE GENES.
    Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48:575-607 PMID: 15012275
  80. Arabidopsis NHO1 is required for general resistance against Pseudomonas bacteria.
    Plant Cell. 2001 Feb;13(2):437-47 PMID: 11226196
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1532-298X
DOI
10.1105/tpc.111.093245
Published
2012-01-00
Epub
2012-00-27
Pages
336-52
Language
English
Region
England
NLM ID
9208688
PMCID
PMC3289552
Subset
IM
Databases
GENBANK
HQ110098, JN688262, JN688263, JN688264
External Links
PubMed source DOI: 10.1105/tpc.111.093245 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2