Skip to main content
Log in

Accumulation of hydroxycinnamic acid amides induced by pathogen infection and identification of agmatine coumaroyltransferase in Arabidopsis thaliana

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Hydroxycinnamic acid amides (HCAAs) are secondary metabolites involved in the defense of plants against pathogens. Here, we report the first identification of HCAAs, p-coumaroylagmatine, feruloylagmatine, p-coumaroylputrescine and feruloylputrescine, in Arabidopsis thaliana rosette leaves infected with Alternaria brassicicola and the assignment of At5g61160 as the agmatine coumaroyltransferase (AtACT) that catalyzes the last reaction in the biosynthesis of the HCAAs. Feeding experiments with putative labeled precursors revealed that the four HCAAs were synthesized from hydroxycinnamic acids and agmatine or putrescine. AtACT gene function was identified from an analysis of a mutant that did not accumulate HCAAs. In wild-type Arabidopsis, AtACT transcripts markedly increased in response to A. brassicicola infection. Enzymatic activity that catalyzes the synthesis of the HCAAs was confirmed in vitro by using a recombinant AtACT expressed in Escherichia coli. The Atact mutant was susceptible to infection by A. brassicicola, indicating that HCAAs are responsible for defense against pathogens in A. thaliana.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

HCAA:

Hydroxycinnamic acid amide

CouAgm:

p-Coumaroylagmatine

FerAgm:

Feruloylagmatine

CouPtr:

p-Coumaroylputrescine

FerPtr:

Feruloylputrescine

ACT:

Agmatine coumaroyltransferase

AtACT:

Arabidopsis thaliana agmatine coumaroyltransferase

References

  • Alcázar R, García-Martínez JL, Cuevas JC, Tiburcio AF, Altabella T (2005) Overexpression of ADC2 in Arabidopsis induces dwarfism and late-flowering through GA deficiency. Plant J 45:425–436

    Article  CAS  Google Scholar 

  • Bernards M, Lopez ML, Zajicek J, Lewis NG (1995) Hydroxycinnamic acid-derived polymers constitute the polyaromatic domain of suberin. J Biol Chem 270:7382–7386

    Article  PubMed  CAS  Google Scholar 

  • Burhenne K, Kristensen BK, Rasmussen SK (2003) A new class of N-hydroxycinnamoyltransferase. J Biol Chem 278:13919–13927

    Article  PubMed  CAS  Google Scholar 

  • D’Auria JC (2006) Acyltransferases in plants: a good time to be BAHD. Curr Opin Plant Biol 9:331–340

    Article  PubMed  CAS  Google Scholar 

  • Fellenberg C, Milkowski C, Hause B, Lange PR, Böttcher C, Schmidt J, Vogt T (2008) Tapetum-specific location of a cation-dependent O-methyltransferase in Arabidopsis thaliana. Plant J 56:132–145

    Article  PubMed  CAS  Google Scholar 

  • Fester T, Maier W, Strack D (1999) Accumulation of secondary compounds in barley and wheat roots in response to inoculation with an arbuscular mycorrhizal fungus and co-inoculation with rhizosphere bacteria. Mycorrhiza 8:241–246

    Article  CAS  Google Scholar 

  • Fujiwara H, Tanaka Y, Yonekura-Sakakibara K, Fukuchi-Mizutani M, Nakao M, Fukui Y, Yamaguchi M, Ashikari T, Kusumi T (1998) cDNA cloning, gene expression and subcellular localization of anthocyanin 5-aromatic acyltransferase from Gentiana triflora. Plant J 16:421–431

    Article  PubMed  CAS  Google Scholar 

  • Grienenberger E, Besseau S, Geoffroy P, Debayle D, Heintz D, Lapierre C, Pollet B, Heitz T, Legrand M (2009) A BAHD acyltransferase is expressed in the tapetum of Arabidopsis anthers and is involved in the synthesis of hydroxycinnamoyl spermidines. Plant J doi:10.1111/j.1365-313X.2008.03773.x

  • Ishihara A, Hashimoto Y, Tanaka C, Dubouzet JG, Nakao T, Matsuda F, Nishioka T, Miyagawa H, Wakasa K (2008) The tryptophan pathway is involved in the defense responses of rice against pathogenic infection via serotonin production. Plant J 54:481–495

    Article  PubMed  CAS  Google Scholar 

  • Jin S, Yoshida M, Nakajima T, Murai A (2003) Accumulation of hydroxycinnamic acid amides in winter wheat under snow. Biosci Biotechnol Biochem 67:1245–1249

    Article  PubMed  CAS  Google Scholar 

  • Keller H, Hohlfeld H, Wray V, Hahlbrock K, Scheel D, Strack D (1996) Changes in the accumulation of soluble and cell wall-bound phenolics in elicitor-treated cell suspension cultures and fungus-infected leaves of Solanum tuberosum. Phytochemistry 42:389–396

    Article  CAS  Google Scholar 

  • Martin-Tanguy J, Martin C, Gallet M, Vernoy R (1976) Potent natural inhibitors of tobacco mosaic virus multiplication. C R Acad Sci Hebd Seances Acad Sci D 282:2231–2234

    PubMed  CAS  Google Scholar 

  • Martin-Tanguy J, Deshayes A, Perdrizet E, Martin C (1979) Hydroxycinnamic acid amides (HCA) in Zea mays. FEBS Lett 108:176–178

    Article  CAS  Google Scholar 

  • 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 Physiol 46:454–466

    Article  PubMed  CAS  Google Scholar 

  • Mayama S, Tani T, Matauura Y, Ueno T, Fukami H (1981) The production of phytoalexins by oat in response to crown rust, Puccinia coronata f. sp. avenae. Physiol Plant Pathol 19:217–226

    CAS  Google Scholar 

  • Mayama S, Matsuura Y, Iida H, Tani T (1982) The role of avenalumin in the resistance of oat to crown rust, Puccinia coronata f. sp. avenae. Physiol Plant Pathol 20:189–199

    Article  CAS  Google Scholar 

  • Miyagawa H, Ishihara A, Nishimoto T, Ueno T, Mayama S (1995) Induction of avenanthramides in oat leaves inoculated with crown rust fungus, Puccinia coronata f. sp. avenae. Biosci Biotechnol Biochem 59:2305–2306

    Article  CAS  Google Scholar 

  • Negrel J, Jeandet P (1987) Metabolism of tyramine and feruloyltyramine in TMV inoculated leaves of Nicotiana tabacum. Phytochemistry 26:2185–2190

    Article  CAS  Google Scholar 

  • Negrel J, Paynot M, Javelle F (1992) Purification and properties of putrescine hydroxycinnamoyl transferase from tobacco (Nicotiana tabacum) cell suspensions. Plant Physiol 98:1264–1269

    Article  PubMed  CAS  Google Scholar 

  • Nomura T, Ishizuka A, Kishida K, Islam AKMR, Endo TR, Iwamura H, Ishihara A (2007) Chromosome arm location of the genes for the biosynthesis of hordatines in barley. Genes Genet Syst 82:455–464

    Article  PubMed  CAS  Google Scholar 

  • Ogura Y, Ishihara A, Iwamura H (2001) Induction of hydroxycinnamic acid amides and tryptophan by jasmonic acid, abscisic acid and osmotic stress in barley leaves. Z Naturforsch 56c:193–202

    Google Scholar 

  • Okazaki Y, Isobe T, Iwata Y, Matsukawa T, Matsuda F, Miyagawa H, Ishihara A, Nishioka T, Iwamura H (2004) Metabolism of avenanthramide phytoalexins in oats. Plant J 39:560–572

    Article  PubMed  CAS  Google Scholar 

  • Rowe HC, Kliebenstein DJ (2008) Complex genetics control natural variation in Arabidopsis thaliana resistance to Botrytis cinerea. Genetics 180:2237–2250

    Article  PubMed  Google Scholar 

  • Schmidt A, Scheel D, Strack D (1998) Elicitor-stimulated biosynthesis of hydroxycinnamoyltyramines in cell suspension cultures of Solanum tuberosum. Planta 205:51–55

    Article  CAS  Google Scholar 

  • 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. J Biol Chem 274:4273–4280

    Article  PubMed  CAS  Google Scholar 

  • Soylu S (2006) Accumulation of cell-wall bound phenolic compounds and phytoalexin in Arabidopsis thaliana leaves following inoculation with pathovars of Pseudomonas syringae. Plant Sci 170:942–952

    Article  CAS  Google Scholar 

  • Stoessl A (1967) The antifungal factors in barley. IV. Isolation, structure, and synthesis of the hordatines. Can J Chem 45:1745–1760

    Article  CAS  Google Scholar 

  • Suzuki H, Nishino T, Nakayama T (2007) cDNA cloning of a BAHD acyltransferase from soybean (Glycine max): isoflavone 7-O-glucoside-6″-O-malonyltransferase. Phytochemistry 68:2035–2042

    Article  PubMed  CAS  Google Scholar 

  • Thomma BPHJ, Nelissen I, Eggermont K, Broekaert WF (1999) Deficiency in phytoalexin production causes enhanced susceptibility of Arabidopsis thaliana to the fungus Alternaria brassicicola. Plant J 19:163–171

    Article  PubMed  CAS  Google Scholar 

  • Tsuji J, Jackson EP, Gage DA, Hammerschmidt R, Somerville SC (1992) Phytoalexin accumulation in Arabidopsis thaliana during the hypersensitive reaction to Pseudomonas syringae pv syringae. Plant Physiol 98:1304–1309

    Article  PubMed  CAS  Google Scholar 

  • Ueda M, Tashiro C, Yamamura S (1997) cis-p-Coumaroylagmatine, the genuine leaf-opening substance of nyctinastic plant, Albizzia julibrissin Durazz. Tetrahedron Lett 38:3253–3256

    Article  CAS  Google Scholar 

  • Urano K, Hobo T, Shinozaki K (2005) Arabidopsis ADC genes involved in polyamine biosynthesis are essential for seed development. FEBS Lett 579:1557–1564

    Article  PubMed  CAS  Google Scholar 

  • von Röpenack E, Parr A, Schulze-Lefert P (1998) Structural analyses and dynamics of soluble and cell wall-bound phenolics in a broad spectrum resistance to the powdery mildew fungus in barley. J Biol Chem 273:9013–9022

    Article  Google Scholar 

  • Yang Q, Reinhard K, Schilz E, Matern U (1997) Characterization and heterologous expression of hydroxycinamoyl/benzoyl-CoA:anthranilate N-hydroxycinnamoyl/benzoyltransferase from elicited cell cultures of carnation, Dianthus caryophyllus L. Plant Mol Biol 35:777–789

    Article  PubMed  CAS  Google Scholar 

  • Yang Q, Trinh HX, Imai S, Ishihara A, Zhang L, Nakayashiki H, Tosa Y, Mayama S (2004) Analysis of the involvement of hydroxyanthranilate hydroxycinnamoyltransferase and caffeoyl-CoA 3-O-methyltransferase in phytoalexin biosynthesis in oat. Mol Plant Microbe Interact 17:81–89

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors are grateful to the Radioisotope Research Center, Kyoto University, for instrumental support with the radioisotope experiments. This work was partly supported by Grants-in-aid for Scientific Research (No. 18380066 to T.N. and No. 21580126 to A.I.) from the Japan Society for the Promotion of Science.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Atsushi Ishihara.

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Muroi, A., Ishihara, A., Tanaka, C. et al. Accumulation of hydroxycinnamic acid amides induced by pathogen infection and identification of agmatine coumaroyltransferase in Arabidopsis thaliana . Planta 230, 517–527 (2009). https://doi.org/10.1007/s00425-009-0960-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-009-0960-0

Keywords

Navigation