Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

The involvement of two epoxide hydrolase genes, NbEH1.1 and NbEH1.2, of Nicotiana benthamiana in the interaction with Colletotrichum destructivum, Colletotrichum orbiculare or Pseudomonas syringae pv. tabaci

C. P. Wijekoon A , P. H. Goodwin A B and T. Hsiang A
+ Author Affiliations
- Author Affiliations

A Department of Environmental Biology, University of Guelph, Guelph, Ontario N1G 2W1, Canada.

B Corresponding author. Email: pgoodwin@uoguelph.ca

Functional Plant Biology 35(11) 1112-1122 https://doi.org/10.1071/FP08160
Submitted: 4 June 2008  Accepted: 5 August 2008   Published: 28 November 2008

Abstract

Epoxide hydrolase hydrates epoxides to vicinal diols in the phyto-oxylipin peroxygenase pathway resulting in the production of epoxy alcohols, dihydrodiols, triols and epoxides, including many lipid epoxides associated with resistance. Two epoxide hydrolase genes from Nicotiana benthamiana L., NbEH1.1 and NbEH1.2, were amplified from coding DNA of leaves during a susceptible response to the hemibiotrophic pathogens, Colletotrichum destructivum O’Gara, Colletotrichum orbiculare Berk. and Mont. von Arx. or Pseudomonas syringae pv. tabaci Wolf and Foster, or the hypersensitive resistance response to P. syringae pv. tabaci expressing avrPto. Increases in expression of NbEH1.1 generally occurred during the late biotrophic and necrotrophic stages in the susceptible responses and before the hypersensitive response. NbEH1.2 expression was not significantly induced by C. orbiculare but was induced by C. destructivum, P. syringae pv. tabaci and P. syringae pv. tabaci expressing avrPto, although to a lesser degree than NbEH1.1. Virus-induced gene silencing of NbEH1.1 delayed the appearance of lesions for C. destructivum, reduced populations of P. syringae pv. tabaci and increased populations of P. syringae pv. tabaci expressing avrPto. The importance of epoxide hydrolase during pathogen attack may be related to its roles in detoxification, signalling, or metabolism of antimicrobial compounds.

Additional keywords: hemibiotrophy, hypersensitive response, oxylipin, virus-induced gene silencing.


Acknowledgements

Funding for this study was provided by the Natural Science and Engineering Research Council of Canada. Nicotiana benthamiana containing Pto was kindly provided by Dr R. Michelmore University of California, Davis, CA. Pseudomonas syringae pv. tabaci 11528R and P. syringae pv. tabaci 11528R containing avrPto were kindly provided by Dr Bridget Randall, Boyce Thompson Institute, Ithaca, NY.


References


Arahira M, Nong Udaka VHK, Fukazawa C (2000) Purification, molecular cloning and ethylene-inducible expression of a soluble-type epoxide hydrolase from soybean (Glycine max [L.] Merr.). European Journal of Biochemistry 267, 2649–2657.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Baulcombe D (1999) Fast forward genetics based on virus-induced gene silencing. Current Opinion in Plant Biology 2, 109–113.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Baulcombe D (2004) RNA silencing in plants. Nature 431, 356–363.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Beetham JK, Grant D, Arand M, Garbarino J, Kiyosue T, Pinot F (1995) Gene evolution of epoxide hydrolases and recommended nomenclature. DNA and Cell Biology 14, 61–71.
CAS | PubMed |
open url image1

Blee E (1998) Phyto-oxylipins and plant defense reactions. Progress in Lipid Research 37, 33–72.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Blee E (2002) Impact of phyto-oxylipins in plant defense. Trends in Plant Science 7, 315–322.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Chen N, Hsiang T, Goodwin PH (2003) Use of green fluorescent protein to quantify the growth of Colletotrichum during infection of tobacco. Journal of Microbiological Methods 53, 113–122.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, Thompson JD (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Research 31, 3497–3500.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Da Cunha L, Sreerekha MV, Mackey D (2007) Defense suppression by virulence effectors of bacterial phytopathogens. Current Opinion in Plant Biology 10, 349–357.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Dean JD, Goodwin PH, Hsiang T (2002) Comparison of relative RT-PCR and northern blot analyses to measure expression of β-1,3-glucanase in Nicotiana benthamiana infected with Colletotrichum destructivum. Plant Molecular Biology Reporter 20, 347–356.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Dinesh-Kumar SP , Anandalakshmi R , Marathe R , Schiff M , Liu Y (2003) Virus-induced gene silencing. In ‘Methods in molecular biology plant functional genomics’. (Ed. E Grotewold) pp. 286–293. (Humana Press: Totowa, NJ)

Edqvist J, Farbos I (2000) Characterization of an Euphorbia lagascae epoxide hydrolase gene which is induced early during germination. Biochemical Society Transactions 28, 855–857.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Gobel C, Feussner I, Rosahl S (2003) Lipid peroxidation during the hypersensitive response in potato in the absence of 9-lipoxygenases. Journal of Biological Chemistry 278, 52834–52840.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gomi K, Yamamoto H, Akimitsu K (2003) Epoxide hydrolase: a mRNA induced by the fungal pathogen Alternaria alternata on rough lemon (Citrus jambhiri Lush). Plant Molecular Biology 53, 189–199.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Guo A, Durner J, Klessig DF (1998) Characterization of a tobacco epoxide hydrolase gene induced during the resistance response to TMV. The Plant Journal 15, 647–656.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Hamberg M, Hamberg G (1996) Peroxygenase-catalyzed fatty acid epoxidation in cereal seeds: Sequential oxidation of linoleic acid into 9(S),12(S),13(S)-trihydroxy-10(E)-octadecenoic acid. Plant Physiology 110, 807–815.
CAS | PubMed |
open url image1

Hammerschmidt R (1999) Phytoalexins: What have we learned after 60 years? Annual Review of Phytopathology 37, 285–306.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Hao L, Hsiang T, Goodwin PH (2006) Role of two cysteine proteinases in the susceptible response of Nicotiana benthamiana to Colletotrichum destructivum and hypersensitive response to Pseudomonas syringae pv. tomato. Plant Science 170, 1001–1009.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Kato T, Yamaguchi Y, Uyehara T, Yokkoyama T, Namai T, Yamanaka S (1983) Self-defensive substances in rice plant against rice plant disease. Tetrahedron Letters 24, 4715–4718.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

King EO, Ward MK, Raney DE (1954) Two simple media for the demonstration of pyocyanin and fluorescin. Journal of Laboratory and Clinical Medicine 44, 301–307.
CAS | PubMed |
open url image1

Kolattukudy PE (1981) Structure, biosynthesis, and biodegradation of cutin and suberin. Annual Review of Plant Physiology 32, 539–567.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Liu Y, Schiff M, Marathe R, Dinesh-Kumar SP (2002) Tobacco Rar1, EDS1 and NPR1/NIM1 like genes are required for N-mediated resistance to tobacco mosaic virus. The Plant Journal 30, 415–429.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Lucas GB (1965) ‘Diseases of tobacco.’ (Scarecrow Press: New York, NY).

Malamy J, Hennig J, Klessig DJ (1992) Temperature-dependent induction of salicylic acid and its conjugate during the resistance response to tobacco mosaic virus infection. The Plant Cell 4, 359–366.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Manandhar J, Hartman G, Sinclair J (1986) Colletotrichum destructivum, the anamorph of Glomerella glycines. Phytopathology 76, 282–285.
Crossref |
open url image1

Matsuoka K, Demura T, Galis I, Horiguchi T, Sasaki M, Tashiro G, Fukuda H (2004) A comprehensive gene expression analysis toward the understanding of growth and differentiation of tobacco BY-2 cells. Plant & Cell Physiology 45, 1280–1289.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mudgett MB (2005) New insights to the function of phytopathogenic bacterial type III effectors in plants. Annual Review of Plant Biology 56, 509–531.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Murray GI, Paterson PJ, Weaver RJ, Ewen SW, Melvin WT, Burke MD (1993) The expression of cytochrome P-450, epoxide hydrolase, and glutathione S-transferase in hepatocellular carcinoma. Cancer 71, 36–43.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Newman JW, Morisseau C, Hammock BD (2005) Epoxide hydrolases: their roles and interactions with lipid metabolism. Progress in Lipid Research 44, 1–51.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Nicot N, Hausman JF, Hoffmann L, Evers D (2005) Housekeeping gene selection for real-time RT-PCR normalization in potato during biotic and abiotic stress. Journal of Experimental Botany 56, 2907–2914.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Ohta H, Shida K, Peng YL, Furusawa I, Shishiyama J, Aibara S, Morita Y (1991) A lipoxygenase pathway is activated in rice after infection with the rice blast fungus Magnaporthe grisea. Plant Physiology 97, 94–98.
CAS | PubMed |
open url image1

Prost I, Dhondt S, Rothe G, Vicente J, Rodriguez MJ , et al. (2005) Evaluation of the antimicrobial activities of plant oxylipins supports their involvement in defense against pathogens. Plant Physiology 139, 1902–1913.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Robertson D (2004) VIGS vectors for gene silencing: many targets, many tools. Annual Review of Plant Biology 55, 495–519.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Rommens CMT, Salmeron JM, Oldroyd GED, Staskawicz BJ (1995) Intergeneric transfer and functional expression of the tomato disease resistance gene Pto. The Plant Cell 7, 1537–1544.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Ronald PC (1992) The cloned avirulence gene avrPto induces disease resistance in tomato cultivars containing the Pto resistance gene. Journal of Bacteriology 174, 1604–1611.
CAS | PubMed |
open url image1

Shen S, Goodwin PH, Hsiang T (2001a) Hemibiotrophic infection and identity of the fungus, Colletotrichum destructivum, causing anthracnose of tobacco. Mycological Research 105, 1340–1347.
Crossref | GoogleScholarGoogle Scholar | open url image1

Shen S, Goodwin PH, Hsiang T (2001b) Infection of Nicotiana spp by the anthracnose fungus, Colletotrichum orbiculare. European Journal of Plant Pathology 107, 767–773.
Crossref | GoogleScholarGoogle Scholar | open url image1

Solis C, Becerra J, Flores C, Robledo J, Silva M (2004) Antibacterial and antifungal terpenes from Pilgerodendron uviferum (D. Don) Florin. Journal of the Chilean Chemical Society 49, 157–162.
CAS |
open url image1

Stapleton A, Beetham JK, Pinot F, Garbarino JE, Rockhold DR, Friedman M, Hammock BD, Belknap WR (1994) Cloning and expression of soluble epoxide hydrolase from potato. The Plant Journal 6, 251–258.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Szatmari A, Ott PG, Varga GJ, Besenyei E, Czelleng A, Klement Z, Bozsó Z (2006) Characterisation of basal resistance (BR) by expression patterns of newly isolated representative genes in tobacco. Plant Cell Reports 25, 728–740.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Vidhyasekaran P (2008) ‘Fungal pathogenesis in plants and crops.’ (CRC Press: Boca Raton, FL)

Vranová VC, Atichartpongkul S, Villarroel R, Montagu MV, Inzé D, Wim Camp WV (2002) Comprehensive analysis of gene expression in Nicotiana tabacum leaves acclimated to oxidative stress. Proceedings of the National Academy of Sciences of the United States of America 99, 10870–10875.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Xiao F, Goodwin SM, Xiao Y, Sun Z, Baker D, Tang X, Jenks MA, Zhou JM (2004) Arabidopsis CYP86A2 represses Pseudomonas syringae type III genes and is required for cuticle development. The EMBO Journal 23, 2903–2913.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Yoshimoto K, Hanaoka H, Sato S, Kato T, Tabata S, Noda TD, Ohsumi Y (2004) Processing of ATG8s, ubiquitin-like proteins, and their deconjugation by ATG4s are essential for plant autophagy. The Plant Cell 16, 2967–2983.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1