Systemic Potato virus X infection induces defence gene expression and accumulation of β-phenylethylamine-alkaloids in potato
Annette Niehl A C , Christophe Lacomme B , Alexander Erban A , Joachim Kopka A , Ute Krämer A and Joachim Fisahn AA Max-Planck Institute of Molecular Plant Physiology, Campus Golm, Am Mühlenberg 1, D-14476 Potsdam, Germany.
B Scottish Crop Research Institute, Invergowrie, Dundee DD2 5DA, Scotland, UK.
C Corresponding author. Email: niehl@mpimp-golm.mpg.de
Functional Plant Biology 33(6) 593-604 https://doi.org/10.1071/FP06049
Submitted: 7 March 2006 Accepted: 11 April 2006 Published: 1 June 2006
Abstract
A better understanding of defence responses elicited during compatible plant–virus interactions is a current goal in plant pathology. We analysed defence responses during infection of Solanum tuberosum L. cv. Desiree with Potato virus X (PVX) at the transcript and metabolite level. A mostly unchanged primary metabolism reflects the compatible nature of this plant–virus interaction. Salicylic acid biosynthesis and expression of several defence genes including PR-1 and glutathione-S-transferase, which are involved in ethylene and reactive oxygen species dependent signalling, were highly up-regulated in upper-uninoculated (systemic) leaves of PVX-infected potato plants compared with mock-inoculated controls. Moreover, the β-phenylethylamine-alkaloids tyramine, octopamine, dopamine and norepinephrine were highly induced upon infection. β-phenylethylamine-alkaloids can contribute to active plant defence responses by forming hydroxycinnamic acid amides (HCAA), which are thought to increase cell wall stability by extracellular peroxidative polymerisation. Expression of tyramine-hydroxycinnamoyl transferase (THT) and apoplastic peroxidase (POD) was highly induced upon PVX infection in systemic leaves, which suggests synthesis and extracellular polymerisation of HCAA. Since cell-wall-bound ion concentrations could contribute to this process, we measured cell-wall-bound and total ion concentrations in PVX-infected and mock-inoculated leaves. The observed metabolic and transcriptional changes might represent a systemic acquired resistance response against subsequent pathogen challenge.
Keywords: dopamine, hydroxycinnamic acid amides, PR-genes, PVX infection, salicylic acid, tyramine.
Acknowledgments
We thank Jonathan Negrel for providing p-coumaroyltyramine, feruloyltyramine and p-coumaroyldopamine standards and Leonard Krall for critical reading of the manuscript. We are grateful to Markus Pauly and Nicolai Obel for help with cell wall sugar analysis. Further, we thank Astrid Schroeder for carrying out ICP analysis. AN was supported by a Marie Curie Training PhD Fellowship in Plant Virology (QLK3-CT-2001-60032). Part of this work was supported by the German Federal Ministry of Education and Research Biofuture grant 0311877 (UK).
Becher M,
Talke IN,
Krall L, Krämer U
(2004) Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. The Plant Journal 37, 251–268.
| PubMed |
Bernards MA,
Fleming WD,
Llewellyn DB,
Priefer R,
Yang XL,
Sabatino A, Plourde GL
(1999) Biochemical characterization of the suberization-associated anionic peroxidase of potato. Plant Physiology 121, 135–145.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Cao H,
Glazebrook J,
Clarke JD,
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 | GoogleScholarGoogle Scholar | PubMed |
Christou P, Barton KA
(1989) Cytokinin antagonist activity of substituted phenethylamines in plant cell culture. Plant Physiology 89, 564–568.
| PubMed |
Czechowski T,
Bari RP,
Stitt M,
Scheible W-R, Udvardi MK
(2004) Real-time RT-PCR profiling of over 1400 Arabidopsis transcription factors: unprecedented sensitivity reveals novel root- and shoot-specific genes. The Plant Journal 38, 366–379.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Dardick CD,
Golem S, Culver JN
(2000) Susceptibility and symptom development in Arabidopsis thaliana to tobacco mosaic virus is influenced by virus cell-to-cell movement. Molecular Plant–Microbe Interactions 13, 1139–1144.
| PubMed |
Dempsey DA,
Shah J, Klessig DF
(1999) Salicylic acid and disease resistance in plants. Critical Reviews in Plant Sciences 18, 547–575.
| Crossref | GoogleScholarGoogle Scholar |
Ducic T, Polle A
(2005) Transport and detoxification of manganese and copper in plants. Brazilian Journal of Plant Physiology 17, 103–112.
Dunand C,
Tognolli M,
Overney S,
von Tobel L,
Meyer M,
Simon P, Penel C
(2002) Identification and characterisation of Ca2+-pectate binding peroxidases in Arabidopsis thaliana. Journal of Plant Physiology 159, 1165–1171.
| Crossref | GoogleScholarGoogle Scholar |
Facchini PJ
(1998) Temporal correlation of tyramine metabolism with alkaloid and amide biosynthesis in elicited opium poppy cell cultures. Phytochemistry 49, 481–490.
| Crossref | GoogleScholarGoogle Scholar |
Facchini PJ,
Hagel J, Zulak KG
(2002) Hydroxycinnamic acid amide metabolism: physiology and biochemistry. Canadian Journal of Botany 80, 577–589.
| Crossref | GoogleScholarGoogle Scholar |
Faivre-Rampant O,
Gilroy EM,
Hrubikova K,
Hein I,
Millam S,
Loake GJ,
Birch P,
Taylor M, Lacomme C
(2004) Potato virus X-induced gene silencing in leaves and tubers of potato. Plant Physiology 134, 1308–1316.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Fecht-Christoffers MM,
Maier P, Horst WJ
(2003) Apoplastic peroxidases and ascorbate are involved in manganese toxicity and tolerance of Vigna unguiculata. Physiologia Plantarum 117, 237–244.
| Crossref | GoogleScholarGoogle Scholar |
Fiehn O,
Kopka J,
Trethewey RN, Willmitzer L
(2000) Identification of uncommon plant metabolites based on calculation of elemental compositions using gas chromatography and quadrupole mass spectrometry. Analytical Chemistry 72, 3573–3580.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Fritzemeier KH,
Cretin C,
Kombrink E,
Rohwer F,
Taylor J,
Scheel D, Hahlbrock K
(1987) Transient induction of phenylalanine ammonia-lyase and 4-coumarate : CoA ligase mRNAs in potato leaves infected with virulent or avirulent races of Phytophthora infestans. Plant Physiology 85, 34–41.
| PubMed |
Grandmaison J,
Olah GM,
Vancalsteren MR, Furlan V
(1993) Characterization and localization of plant phenolics likely involved in the pathogen resistance expressed by endomycorrhizal roots. Mycorrhiza 3, 155–164.
| Crossref | GoogleScholarGoogle Scholar |
Hagel JM, Facchini PJ
(2005) Elevated tyrosine decarboxylase and tyramine hydroxycinnamoyltransferase levels increase wound-induced tyramine-derived hydroxycinnamic acid amide accumulation in transgenic tobacco leaves. Planta 221, 904–914.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Harikrishna K,
Jampatesbeale R,
Milligan SB, Gasser CS
(1996) An endochitinase gene expressed at high levels in the stylar transmitting tissue of tomatoes. Plant Molecular Biology 30, 899–911.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hoegen E,
Stromberg A,
Pihlgren U, Kombrink E
(2002) Primary structure and tissue-specific expression of the pathogenesis-related protein PR-1b in potato. Molecular Plant Pathology 3, 329–345.
| Crossref | GoogleScholarGoogle Scholar |
Huang ZL,
Yeakley JM,
Garcia EW,
Holdridge JD,
Fan JB, Whitham SA
(2005) Salicylic acid-dependent expression of host genes in compatible Arabidopsis–virus interactions. Plant Physiology 137, 1147–1159.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Joos HJ, Hahlbrock K
(1992) Phenylalanine ammonia-lyase in potato (Solanum tuberosum L.). Genomic complexity, structural comparison of two selected genes and modes of expression. European Journal of Biochemistry 204, 621–629.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kawalleck P,
Keller H,
Hahlbrock K,
Scheel D, Somssich I
(1993) A pathogen-responsive gene of parsley encodes tyrosine decarboxylase. Journal of Biological Chemistry 268, 2189–2194.
| PubMed |
Kombrink E,
Schröder M, Hahlbrock K
(1988) Several ‘pathogenesis-related’ proteins in potato are 1,3-β-glucanases and chitinases. Proceedings of the National Academy of Sciences USA 85, 782–786.
Kopka J,
Schauer N,
Krueger S,
Birkemeyer C, Usadel B , et al.
(2005) GMD@CSB.DB: the Golm metabolome database. Bioinformatics 21, 1635–1638.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Love AJ,
Yun BW,
Laval V,
Loake GJ, Milner JJ
(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 Physiology 139, 935–948.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Martin-Tanguy J,
Martin C,
Gallet M, Vernoy R
(1976) Natural potent inhibitors of tobacco mosaic-virus multiplication. Comptes Rendus Hebdomadaires des Seances de l’Academie des Sciences Serie D 282, 2231–2234.
Matsuda F,
Morino K,
Ano R,
Kuzawa M,
Wakasa K, Miyagawa H
(2005) Metabolic flux analysis of the phenylpropanoid pathway in elicitor-treated potato tuber tissue. Plant & Cell Physiology 46, 454–466.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
McLusky SR,
Bennett MH,
Beale MH,
Lewis MJ,
Gaskin P, Mansfield JW
(1999) Cell wall alterations and localized accumulation of feruloyl-3′-methoxytyramine in onion epidermis at sites of attempted penetration by Botrytis allii are associated with actin polarisation, peroxidase activity and suppression of flavonoid biosynthesis. The Plant Journal 17, 523–534.
| Crossref | GoogleScholarGoogle Scholar |
Nakane E,
Kawakita K,
Doke N, Yoshioka H
(2003) Elicitation of primary and secondary metabolism during defense in the potato. Journal of General Plant Pathology 69, 378–384.
| Crossref | GoogleScholarGoogle Scholar |
Negrel J, Javelle F
(1997) Purification, characterization and partial amino acid sequencing of hydroxycinnamoyl-CoA-tyramine N-(hydroxycinnamoyl)transferase from tobacco cell-suspension cultures. European Journal of Biochemistry 247, 1127–1135.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Negrel J, Jeandet P
(1987) Metabolism of tyramine and feruloyltyramine in TMV inoculated leaves of Nicotiana tabacum. Phytochemistry 26, 2185–2190.
| Crossref | GoogleScholarGoogle Scholar |
Negrel J, Martin C
(1984) The biosynthesis of feruloyltyramine in Nicotiana tabacum. Phytochemistry 23, 2797–2801.
| Crossref | GoogleScholarGoogle Scholar |
Newman MA,
von Roepenack-Lahaye E,
Parr A,
Daniels MJ, Dow JM
(2001) Induction of hydroxycinnamoyl-tyramine conjugates in pepper by Xanthomonas campestris, a plant defense response activated by hrp gene-dependent and hrp gene-independent mechanisms. Molecular Plant–Microbe Interactions 14, 785–792.
| PubMed |
Niggeweg R,
Michael AJ, Martin C
(2004) Engineering plants with increased levels of the antioxidant chlorogenic acid. Nature Biotechnology 22, 746–754.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Park JB, Schoene N
(2002) Synthesis and characterization of N-coumaroyltyramine as a potent phytochemical which arrests human transformed cells via inhibiting protein tyrosine kinases. Biochemical and Biophysical Research Communications 292, 1104–1110.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Passardi F,
Penel C, Dunand C
(2004) Performing the paradoxical: how plant peroxidases modify the cell wall. Trends in Plant Science 9, 534–540.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pilling J,
Willmitzer L,
Bücking H, Fisahn J
(2004) Inhibition of a ubiquitously expressed pectin methyl esterase in Solanum tuberosum L. affects plant growth, leaf growth polarity, and ion partitioning. Planta 219, 32–40.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ramakers C,
Ruijter JM,
Deprez RHL, Moorman AFM
(2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neuroscience Letters 339, 62–66.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Roberts E,
Kutchan T, Kolattukudy PE
(1988) Cloning and sequencing of cDNA for a highly anionic peroxidase from potato and the induction of its mRNA in suberizing potato tubers and tomato fruits. Plant Molecular Biology 11, 15–26.
| Crossref | GoogleScholarGoogle Scholar |
Ryals J,
Weymann K,
Lawton K,
Friedrich L, Ellis D , et al.
(1997) The Arabidopsis NIM1 protein shows homology to the mammalian transcription factor inhibitor IκB. The Plant Cell 9, 425–439.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Schauer N,
Steinhauser D,
Strelkov S,
Schomburg D,
Allison G,
Moritz T,
Lundgren K,
Roessner-Tunali U,
Forbes M, Willmitzer L
(2005) GC–MS libraries for the rapid identification of metabolites in complex biological samples. FEBS Letters 579, 1332–1337.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Schmidt A,
Grimm R,
Schmidt J,
Scheel D,
Strack D, Rosahl S
(1999) Cloning and expression of a potato cDNA encoding hydroxycinnamoyl-CoA: tyramine N-(hydroxycinnamoyl)transferase. Journal of Biological Chemistry 274, 4273–4280.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Shadle GL,
Wesley SV,
Korth KL,
Chen F,
Lamb C, Dixon RA
(2003) Phenylpropanoid compounds and disease resistance in transgenic tobacco with altered expression of l-phenylalanine ammonia-lyase. Phytochemistry 64, 153–161.
| Crossref | l-phenylalanine ammonia-lyase.&journal=Phytochemistry&volume=64&pages=153-161&publication_year=2003&author=RA%20Dixon&hl=en&doi=10.1016/S0031-9422(03)00151-1" target="_blank" rel="nofollow noopener noreferrer" class="reftools">GoogleScholarGoogle Scholar | PubMed |
Shah K,
Penel C,
Gagnon J, Dunand C
(2004) Purification and identification of a Ca2+-pectate binding peroxidase from Arabidopsis leaves. Phytochemistry 65, 307–312.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sinclair SJ,
Johnson R, Hamill JD
(2004) Analysis of wound-induced gene expression in Nicotiana species with contrasting alkaloid profiles. Functional Plant Biology 31, 721–729.
| Crossref | GoogleScholarGoogle Scholar |
Spoel SH,
Koornneef A,
Claessens SMC,
Korzelius JP, Van Pelt JA , et al.
(2003) NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. The Plant Cell 15, 760–770.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Swiedrych A,
Lorenc-Kukula K,
Skirycz A, Szopa J
(2004) The catecholamine biosynthesis route in potato is affected by stress. Plant Physiology and Biochemistry 42, 593–600.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Taylor JL,
Fritzemeier KH,
Hauser I,
Kombrink E,
Rohwer F,
Schröder M,
Strittmatter G, Hahlbrock K
(1990) Structural analysis and activation by fungal infection of a gene encoding a pathogenesis-related protein in potato. Molecular Plant–Microbe Interactions 3, 72–77.
| PubMed |
Torrance L,
Larkins AP, Butcher GW
(1986) Characterization of monoclonal antibodies against potato virus X and comparison of serotypes with resistance groups. The Journal of General Virology 67, 57–67.
Trezzini G,
Horrichs A, Somssich I
(1993) Isolation of putative defense-related genes from Arabidopsis thaliana and expression in fungal elicitor-treated cells. Plant Molecular Biology 21, 385–389.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tuchinda P,
Pohmakotr M,
Reutrakul V,
Thanyachareon W,
Sophasan S,
Yoosook C,
Santisuk T, Pezzuto J
(2001) 2-Substituted furans from Polyalthia suberosa. Planta Medica 67, 572–575.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
von Roepenack-Lahaye E,
Newman MA,
Schornack S,
Hammond-Kosack KE,
Lahaye T,
Jones JDG,
Daniels MJ, Dow JM
(2003) p-Coumaroylnoradrenaline, a novel plant metabolite implicated in tomato defense against pathogens. Journal of Biological Chemistry 278, 43373–43383.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wagner C,
Sefkow M, Kopka J
(2003) Construction and application of a mass spectral and retention time index database generated from plant GC / EI-TOF-MS metabolite profiles. Phytochemistry 62, 887–900.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Whitham SA,
Quan S,
Chang HS,
Cooper B,
Estes B,
Zhu T,
Wang X, Hou YM
(2003) Diverse RNA viruses elicit the expression of common sets of genes in susceptible Arabidopsis thaliana plants. The Plant Journal 33, 271–283.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wildermuth MC,
Dewdney J,
Wu G, Ausubel FM
(2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414, 562–565.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Yalpani N,
Leon J,
Lawton MA, Raskin I
(1993) Pathway of salicylic acid biosynthesis in healthy and virus-inoculated tobacco. Plant Physiology 103, 315–321.
| PubMed |
Yu M, Facchini PJ
(1999) Purification, characterization, and immunolocalization of hydroxycinnamoyl-CoA: tyramine N-(hydroxycinnamoyl)transferase from opium poppy. Planta 209, 33–44.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Yu M, Facchini PJ
(2000) Molecular cloning and characterization of a type III glutathione S-transferase from cell suspension cultures of opium poppy treated with a fungal elicitor. Physiologia Plantarum 108, 101–109.
| Crossref | GoogleScholarGoogle Scholar |
