Skip to main content
Log in

Structurally unrelated algal oligosaccharides differentially stimulate growth and defense against tobacco mosaic virus in tobacco plants

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

Tobacco plants were treated with structurally unrelated oligosaccharides obtained from Chilean marine macroalgae. These oligosaccharides were prepared by chemical depolymerization of native polysaccharides extracted from brown and red algae and correspond to pure polymers of around 20 units of guluronic acid (Poly-Gu), mannuronic acid (Poly-Ma) and sulphated galactan (Poly-Ga). These oligosaccharides were solubilized in water, at a final concentration of 500 μg mL−1, and sprayed on tobacco leaves, once a week for a month. Their effects on the stimulation of growth and defense against tobacco mosaic virus (TMV) were determined 7 and 15 days after the final spraying, respectively. The activities of several defense and antioxidant enzymes and the levels of water-soluble antioxidant compounds were determined. Plants treated with Poly-Ga and Poly-Ma showed an increase in height of 23% and 49%, respectively, whereas Poly-Gu did not stimulate growth. Plants treated with Poly-Gu, Poly-Ma and Poly-Ga showed an increase in defense against TMV corresponding to decreases in the number of necrotic lesions of 9%, 22% and 74%, respectively. The stimulation of plant growth correlates with activation of the antioxidant enzyme ascorbate peroxidase (AP) and with a decrease in ascorbate level. On the other hand, the stimulation of defense against TMV is correlated with the activation of the defense enzyme phenylalanine ammonia-lyase (PAL). These results indicate that algal oligosaccharides differentially stimulate growth and defense against TMV in tobacco plants and that these processes involve the activation of the enzymes AP and PAL, respectively.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Ahl-Goy PA, Signer H, Reist R, Aichholz R, Blum W, Schmidt E, Kessmann H (1993) Accumulation of scopoletin is associated with the high disease resistance of hybrid Nicotiana glutinosa x Nicotiana debney. Planta 191:200–206

    CAS  Google Scholar 

  • Alvarez M, Pennell R, Meijer P, Ishikawa A, Dixon RA, Lamb C (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92:773–784

    Article  PubMed  CAS  Google Scholar 

  • Aziz A, Poinssot B, Daire X, Adrian M, Bézier A, Lambert B, Joubert JM, Pugin A (2003) Laminarin elicits defense responses in grapevine and induces protection against Botrytis cinerea and Plasmopara viticola. Mol Plant-Microbe Interact 16:1118–1128

    PubMed  CAS  Google Scholar 

  • Blée E (2004) Impact of phyto-oxylipins in plant defense. Trends Plant Sci 7:315–321

    Article  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Cáceres PJ, Carlucci MJ, Damonte EB, Matsuhiro B, Zúñiga EA (2000) Carrageenans from chilean samples of Stenogramme interrupta (Phyllophoraceae): structural analysis and biological activity. Phytochemistry 53:81–86

    Article  PubMed  Google Scholar 

  • Chandía NP, Matsuhiro B, Mejías E, Moenne A (2004) Alginic acids in Lessonia vadosa: partial hydrolysis and elicitor properties of the polymannuronic acid fraction. J Appl Phycol 16:127–133

    Article  Google Scholar 

  • Chandía NP, Matsuhiro B, Vásquez AE (2001) Alginic acids in Lessonia trabeculata: characterization by formic acid hydrolysis and FT-IR spectroscopy. Carbohydr Res 46:81–87

    Article  Google Scholar 

  • Chong J, Baltz R, Schmitt C, Beffa R, Fitig B, Saindrenan P (2002) Downregulation of a pathogen-responsive tobacco UDP-Glc: phenylpropanoid glucosyltransferase reduces scopoletin glucoside accumulation, enhance oxidative stress, and weakens virus resistance. Plant Cell 14:1093–1107

    Article  PubMed  CAS  Google Scholar 

  • Côté F, Roberts K, Hahn M (2000) Identification of high affinity binding sites for the hepta-β-glucoside elicitor in membranes of the model legumes Medicago trunculata and Lotus japonicus. Planta 211:596–605

    Article  PubMed  Google Scholar 

  • Creelman RA, Mullet JE (1997) Oligosaccharins, brassinolides, and jasmonates: nontraditional regulators of plant growth, development, and gene expression. Plant Cell 9:1211–1223

    Article  PubMed  CAS  Google Scholar 

  • Dixon RA (2001) Natural products and plant disease resistance. Nature 411:843–847

    Article  PubMed  CAS  Google Scholar 

  • Eberhard S, Doubrava N, Marfà V, Mohnen D, Southwick A, Darvill A, Albersheim P (1989) Pectic cell wall fragments regulate tobacco thin-layer explant morphogenesis. Plant Cell 1:747–755

    Article  PubMed  CAS  Google Scholar 

  • Foreman J, Demidchik V, Bothwell JHF, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JDG, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446

    Article  PubMed  CAS  Google Scholar 

  • Göbel C, Feussner I, Schmidt A, Scheel D, Sánchez-Serrano J, Hamberg M, Roshal S (2001) Oxylipin profiling reveal the preferential stimulation of the 9–lipoxygenase pathway in elicitor-treated potato cells. J Biol Chem 276:6267–6273

    Article  PubMed  Google Scholar 

  • Hammond-Kosack KE, Jones JDG (1996) Resistance gene-dependent plant defense responses. Plant Cell 8:1773–1791

    Article  PubMed  CAS  Google Scholar 

  • Horemans N, Asard H, Caubergs RJ (1997) The ascorbate carrier of higher plant plasma membranes preferentially translocate the fully oxidized (dehydroascorbate) molecule. Plant Physiol 114:1247–1253

    PubMed  CAS  Google Scholar 

  • Horemans N, Foyer CH, Asard H (2000) Transport and action of ascorbate at the plant plasma membrane. Trends Plant Sci 5:263–267

    Article  PubMed  CAS  Google Scholar 

  • Howe GA, Schilmiller AL (2002) Oxylipin metabolism in response to stress Curr Opin Plant Biol 5:230–236

    Article  PubMed  CAS  Google Scholar 

  • Howles PA, Paiva NL, Sewalt VJH, Elkind NL, Bate Y, Lamb CJ, Dixon RA (1996) Overexpression of l-penylalanine ammonia-lyase in transgenic tobacco plants reveals control points for flux into phenylpropanoid biosynthesis. Plant Physiol 112:1617–1624

    PubMed  CAS  Google Scholar 

  • Itoh Y, Kaku H, Shibuya N (1997) Identification of high-affinity binding protein for N-acetylchitooligosaccharide elicitor in the plasma membrane of suspension-cultured rice cells by affinity labeling. Plant J 12:347–356

    Article  Google Scholar 

  • Kato N, Esaka M (1999) Changes in ascorbate oxidase gene expression and ascorbate levels in cell division and cell elongation in tobacco cells. Physiol Plant 105:321–329

    Article  CAS  Google Scholar 

  • Kawano T (2003) Roles of the reactive oxygen species-generating peroxidase reactions in plant defense and growth induction. Plant Cell Rep 21:829–837

    PubMed  CAS  Google Scholar 

  • Klarzynski O, Descamps V, Plesse B, Yvin JC, Kloareg B, Fritig B (2003) Sulfated fucan oligosaccharides elicit defense responses in tobacco and local and systemic resistance against tobacco mosaic virus. Mol Plant-Microbe Interact 16:115–122

    PubMed  CAS  Google Scholar 

  • Klarzynski O, Plesse B, Joubert JM, Yvin JC, Kopp M, Kloareg B, Fritig B (2000) Linear β–1,3 glucans are elicitors of defense responses in tobacco. Plant Physiol 124:1027–1037

    Article  PubMed  CAS  Google Scholar 

  • La Caméra S, Gouzhert G, Dohndt S, Hoffmann L, Fritig B, Legrand M, Heitz T (2004) Metabolic reprogramming in plant innate immunity: the contributions of phenylpropanoid and oxylipin pathways. Immunol Rev 198:267–284

    Article  PubMed  Google Scholar 

  • Lawton MA, Lamb CJ (1987) Transcriptional activation of plant defense genes by fungal elicitor, wounding and infection. Mol Cell Biol 7:335–341

    PubMed  CAS  Google Scholar 

  • Matsuhiro B, Conte AF, Damonte EB, Kolender AA, Matulewicz MC, Mejías EG, Pujol CA, Zuniga EA (2005) Structural analysis and antiviral activity of a sulphated galactan from the red seaweed Schizymenia binderi (Gigartinales, Rodophyta). Carbohydr Res 340:2392–2402

    Article  PubMed  CAS  Google Scholar 

  • Mauch-Mani B, Slusarenko AJ (1996) Production of salicylic acid precursors is a major function of phenylalanine ammonia-lyase in the resistance of Arabidopsis to Peronospora parasitica. Plant Cell 8:203–212

    Article  PubMed  CAS  Google Scholar 

  • McDougall GJ, Fry SC (1990) Xyloglucan oligosaccharides promote growth and activate cellulase: evidence for cellulase in cell expansion. Plant Physiol 93:1042–1048

    Article  PubMed  CAS  Google Scholar 

  • McDowell JM, Woffenden BJ (2003) Plant disease resistance genes: recent insights and potential applications. Trends Biotechnol 21:178–183

    Article  PubMed  CAS  Google Scholar 

  • Ménard R, Alban S, De Ruffray P, Jamois F, Franz G, Fritig B, Yvin JC, Kauffmann S (2004) β–1,3 glucan sulfate, but not β–1,3 glucan, induces salicylic acid signaling pathway in tobacco and Arabidopsis. Plant Cell 16:3020–3032

    Article  PubMed  CAS  Google Scholar 

  • Mercier L, Lafitte C, Borderies G, Briand X, Esquerré-Tugayé MT, Fournier J (2001) The algal polysaccharide carrageenans can act as an elicitor of plant defence. New Phytol 149:43–51

    Article  CAS  Google Scholar 

  • Nita-Lazar M, Chevolot M, Iwahara S, Takegawa K, Furmanek A, Lienart Y (2002) High performance liquid chromatography and photodiode array detection of ferulic acid in Rubus protoplasts elicited by O-glycans from Fusarium sp. M7–1. Acta Biochim Pol 49:1019–1027

    PubMed  CAS  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279

    Article  PubMed  CAS  Google Scholar 

  • Orr JD, Edwards R, Dixon RA (1993) Stress responses in alfalfa (Medicago sativa L.). Changes in the level of phenylpropanoid pathway intermediates in relation to regulation of phenylalanine ammonia-lyase in elicitor-treated cell-suspension cultures. Plant Physiol 101:847–856

    PubMed  CAS  Google Scholar 

  • Pallas JA, Paiva NL, Lam CJ, Dixon RA (1996) Tobacco plants epigenetically supressed in phenylalanine ammonia-lyase expression do not develop systemic acquired resistance in response to infection by tobacco mosaic virus. Plant J 10:281–293

    Article  CAS  Google Scholar 

  • Patier P, Potin P, Rochas C, Kloareg B, Yvin JC, Liénart Y (1995) Free or silica-bound oligokappa-carrageenans elicit laminarase activity in Rubus cells and protoplasts. Plant Sci 110:27–35

    Article  CAS  Google Scholar 

  • Pignocchi C, Fletcher JM, Wilkinson JE, Barnes JD, Foyer CH (2003) The function of ascorbate oxidase in tobacco. Plant Physiol 132:1631–1641

    Article  PubMed  CAS  Google Scholar 

  • Pignocchi C, Foyer C (2003) Apoplastic ascorbate metabolism and its role in the regulation of cell signaling. Curr Opin Plant Biol 6:379–389

    Article  PubMed  CAS  Google Scholar 

  • Pnueli L, Liang H, Rozenberg M, Mittler R (2003) Growth suppression, altered stomatal responses, and augmented induction of heat shock proteins in cytosolic ascorbate peroxidase (Apx1)-deficient Arabidopsis plants. Plant J 34:187–203

    Article  PubMed  CAS  Google Scholar 

  • Ratkevicius N, Correa JA, Moenne A (2003) Copper accumulation, synthesis of ascorbate and activation of ascorbate peroxidase in Enteromorpha compressa (L.) Grev. (Chlorophyta) from heavy metal-enriched environments in northern Chile. Plant Cell Environ 26:1599–1608

    Article  CAS  Google Scholar 

  • Rodríguez AA, Grunberg KA, Taleisnik EL (2002) Reactive oxygen species in the elongation zone of maize leaves are necessary for leaf extension. Plant Physiol 129:1627–1632

    Article  PubMed  CAS  Google Scholar 

  • Schopfer P, Liskay A, Bechtold M, Fahry G, Wagner A (2002) Evidence that hydroxyl radicals mediate auxin-induced extension growth. Planta 21:821–828

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Sokal RR, Rolph JF (1981) Biometry, 2nd edn. Freeman, New York, p 859

    Google Scholar 

  • Tran Thanh Van K, Toubart P, Cousson A (1985) Manipulation of the morphogenetic pathways of tobacco by oligosaccharins. Nature 314:615–617

    Article  Google Scholar 

  • Whitham S, Dinesh-Kumar SP, Choi D, Hell R, Corr C (1994) The product of the tobacco mosaic virus resistance gene N: similarity to Toll and Interleukin-1 receptors. Cell 78:1101–1115

    Article  PubMed  CAS  Google Scholar 

  • Zhang S, Du H, Klessig DF (1998) Activation of the tobacco SIP kinase by both a cell wall-derived carbohydrate elicitor and purified proteinaceous elicitins from Phytophthora spp. Plant Cell 10:435–449

    Article  PubMed  CAS  Google Scholar 

  • Zúñiga EA, Matsuhiro B, Mejías E (2006) Preparation of a low molecular weight fraction by free radical depolimerization of the sulphated galactan from Schizymenia binderi (Gigartinales, Rodophyta) and its anticoagulant activity. Carbohydr Polym (in press)

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alejandra Moenne.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Laporte, D., Vera, J., Chandía, N.P. et al. Structurally unrelated algal oligosaccharides differentially stimulate growth and defense against tobacco mosaic virus in tobacco plants. J Appl Phycol 19, 79–88 (2007). https://doi.org/10.1007/s10811-006-9114-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-006-9114-y

Key words

Navigation