Plant Biol (Stuttg) 2005; 7(6): 581-591
DOI: 10.1055/s-2005-873009
Review Article

Georg Thieme Verlag Stuttgart KG · New York

Significance of Flavonoids in Plant Resistance and Enhancement of Their Biosynthesis

D. Treutter1
  • 1Unit of Fruit Science, Center of Life Sciences Weihenstephan, Technical University of Munich, Alte Akademie 16, 85350 Freising, Germany
Further Information

Publication History

Received: April 28, 2005

Accepted: October 28, 2005

Publication Date:
02 January 2006 (online)

Abstract

The roles of flavonoids in plant defence against pathogens, herbivores, and environmental stress are reviewed and their significant contribution to plant resistance is discussed. The induction of flavonoids is of particular interest for gathering evidence of their roles. Tools are mentioned which may enhance flavonoid biosynthesis and accumulation. These include metabolic engineering and UV light. The induction of defence-related flavonoids is modified by other determining factors and competition between growth and secondary metabolism may exist. In an evolutionary context, stress-related oxidative pressure may have been a major trigger for the distribution and abundance of flavonoids. UV protection is one of their most significant, or even the most significant, functional role for flavonoids. The multi-functionality of these compounds, however, often complicates the interpretation of experimental results but, overall, it supports the importance of flavonoids.

References

  • 1 Agrawal G. K., Rakwal R., Tamogami S., Yonekura M., Kubo A., Saji H.. Chitosan activates defense/stress response(s) in the leaves of Oryza sativa seedlings.  Plant Physiology and Biochemistry. (2002);  40 1061-1069
  • 2 Aguero M. E., Gevens A., Nicholson R. L.. Interaction of Cochliobolus heterostrophus with phytoalexin inclusions in Sorghum bicolor.  Physiological and Molecular Plant Pathology. (2002);  61 267-271
  • 3 Alcerito T., Barbo F. E., Negri G., Santos D. Y. A. C., Meda C. I., Young M. C. M., Chávez D., Blatt C. T. T.. Foliar epicuticular wax of Arrabidea brachypoda: flavonoids and antifungal activity.  Biochemical Systematics and Ecology. (2002);  30 677-683
  • 4 Arcas M. C., Botía J. M., Ortuño A. M., Del Rio J. A.. UV irradiation alters the levels of flavonoids involved in the defence mechanism of Citrus aurantium fruits against Peniillium digitatum.  European Journal of Plant Pathology. (2000);  106 617-622
  • 5 Awad M., DeJager A.. Relationships between fruit nutrients and concentrations of flavonoids and chlorogenic acid in “Elstar” apple skin.  Scientia Horticulturae. (2002);  92 265-276
  • 6 Bais H. P., Vepachedu R., Gilroy S., Callaway R. M., Vivanco J. M.. Allelopathy and exotic plant invasion: from molecules and genes to species interaction.  Science. (2003);  301 1377-1380
  • 7 Barceló J., Poschenrieder C.. Fast root growth responses, root exudates, and internal detoxification as clues to the mechanism of aluminium toxicity and resistance: a review.  Environmental and Experimental Botany. (2002);  48 75-92
  • 8 Barry K. M., Davies N. W., Mohammed C. L.. Effect of season and different fungi on phenolics in response to xylem wounding and inoculation in Eucalyptus nitens.  Forest Pathology. (2002);  32 163-178
  • 9 Baur R., Haribal M., Renwick A. A., Städler E.. Contact chemoreception related to host selection and oviposition behaviour in the monarch butterfly, Danaus plexippus.  Physiological Entomology. (1998);  23 7-19
  • 10 Bazzaz F. A.. Allocation of resources in plants: state of the science and critical questions. Bazzaz, F. A. and Grace, J., eds. Plant Resource Allocation. San Diego; Academic Press (1987): 1-38
  • 11 Bazzi C., Messina C., Tortoreto L., Stefani E., Bini F., Brunelli A., Andreotti C., Sabatini E., Spinelli F., Costa G., Hauptmann S., Stammler G., Doerr S., Marr J., Rademacher W.. Control of pathogen incidence in pome fruits and other horticultural crop plants with prohexadione-Ca.  European Journal of Horticultural Science. (2003);  68 108-114
  • 12 Beckman C. H.. Phenolic-storing cells: keys to programmed cell death and periderm formation in wilt disease resistance and in general defence responses in plants?.  Physiological and Molecular Plant Pathology. (2000);  57 101-110
  • 13 Benoit L. F., Berry A. M.. Flavonoid-like compounds from seeds of red alder (Alnus rubra) influence host nodulation by Frankia (Actinomycetales).  Physiologia Plantarum. (1997);  99 588-593
  • 14 Berhow M. A., Vaughn S. F.. Higher plant flavonoids: biosynthesis and chemical ecology. Inderjit, S., Dakshini, K. M. M., and Foy, C. L., eds. Principles and Practices in Plant Ecology. Boca Raton; CRC Press (1999): 423-438
  • 15 Brignolas F., Lieutier F., Sauvard D., Christiansen E., Berryman A. A.. Phenolic predictors for Norway spruce resistance to the bark beetle Ips typographus (Coleoptera: Scolytidae) and an associated fungus, Ceratocystis polonica.  Canadian Journal of Forest Research. (1998);  28 720-728
  • 16 Broughton W. J., Zhang F., Perret X., Staehelin C.. Signals exchanged between legumes and Rhizobium: agricultural uses and perspectives.  Plant and Soil. (2003);  252 129-137
  • 17 Bryant J., Chapin I.F., Klein D.. Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory.  Oikos. (1983);  40 357-368
  • 18 Chalker-Scott L., Krahmer R. L.. Microscopic studies of tannin formation and distribution in plant tissues. Hemingway, R. W. and Karchesy, J. J., eds. Chemistry and Significance of Condensed Tannins. New York; Plenum Press (1989): 345-368
  • 19 Chaves N., Escudero J. C.. Variation of flavonoid synthesis induced by ecological factors. Inderjit, S., Dakshini, K. M. M., and Foy, C. L., eds. Principles and Practices in Plant Ecology. Boca Raton; CRC Press (1999): 267-285
  • 20 Chen K., Ohmura W., Doi S., Aoyama M.. Termite feeding deterrent from Japanese larch wood.  Bioresource Technology. (2004);  95 129-134
  • 21 Chou C.-H.. Roles of allelopathy in plant biodiversity and sustainable agriculture.  Critical Reviews in Plant Sciences. (1999);  18 609-636
  • 22 Close D. C., McArthur C.. Rethinking the role of many plant phenolics - protection from photodamage not herbivores?.  Oikos. (2002);  99 166-172
  • 23 Cohen M. F., Yamaseki H.. Flavonoid-induced expression of a symbiosis-related gene in the cyanobacterium Nostoc punctiforme.  Journal of Bacteriology. (2000);  182 4644-4646
  • 24 Coley P. D., Bryant J. P., Chapin F. S.. Resource availability and plant antiherbivore defense.  Science. (1985);  230 895-899
  • 25 Collingborn F. M. B., Gowen S. R., Mueller-Harvey I.. Investigations into the biochemical basis of nematode resistance in roots of three Musa cultivars in response to Radopholus similis infection.  Journal of Agricultural and Food Chemistry. (2000);  48 5297-5301
  • 26 Cooper J. E.. Multiple responses of Rhizobia to flavonoids during legume root infection.  Advances in Botanical Research. (2004);  41 1-62
  • 27 Cuadra P., Harborne J. B., Waterman P. G.. Increases in surface flavonols and photosynthetic pigments in Gnaphalium luteo-album in response to UV‐B radiation.  Phytochemistry. (1997);  45 1377-1383
  • 28 Davies K. M., Schwinn K. E., Deroles S. C., Manson D. G., Lewis D. H., Bloor S. J., Bradley J. M.. Enhancing anthocyanin production by altering competition for substrate between flavonol synthase and dihydroflavonol 4-reductase.  Euphytica. (2003);  131 259-268
  • 29 Del Rio J. A., Arcas M. C., Botía J. M., Baídez A. G., Fuster M. D., Ortuño A.. Involvement of phenolic compounds in the antifungal defense mechanisms of Olea europaea L. and Citrus sp. Recent Res. Devel.  Journal of Agricultural and Food Chemistry. (2000);  4 331-341
  • 30 Del Rio J. A., Gonzalez A., Fuster M. D., Botia J. M., Gomez P., Frias V., Ortuño A.. Tylose formation and changes in phenolic compounds of grape roots infected with Phaeomoniella chlamydospora and Phaeoacremonium species.  Phytopathology Mediterranean. (2001);  40 (Suppl.) S394-S399
  • 31 Del Rio J. A., Báidez A. G., Botía J. M., Ortuño A.. Enhancement of phenolic compounds in olive plants (Olea europaea L.) and their influence on resistance against Phytophthora sp.  Food Chemistry. (2003);  83 75-78
  • 32 Deng F., Aoki M., Yogo Y.. Effect of naringenin on the growth and lignin biosynthesis of gramoineous plants.  Weed Biology and Management. (2004);  4 49-55
  • 33 Dixon R. A., Steel C. L.. Flavonoids and isoflavonoids - a gold mine for metabolic engineering.  Trends in Plant Science. (1999);  4 394-400
  • 34 Estiarte M., Peñuelas J., Kimball B. A., Hendrix D. L., Pinter  Jr. P. J., Wall G. W., LaMorte R. L., Hunsaker D.. Free-air CO2 enrichment of wheat: leaf flavonoid concentration throughout the growth cycle.  Physiologia Plantarum. (1999);  105 423-433
  • 35 Eyles A., Davies N. W., Yuan Z. Q., Mohammed C.. Host response to natural infection by Cytonaema sp. in the aerial bark of Eucalyptus globulus.  Forest Pathology. (2003);  33 317-331
  • 36 Farooq A., Tahara S.. Fungal metabolism of flavonoids and related phytoalexins.  Current Topics in Phytochemistry. (1999);  2 1-33
  • 37 Feeny P. P.. Plant apparancy and chemical defense.  Recent Advances in Phytochemistry. (1976);  10 1-40
  • 38 Feild T. S., Lee D. W., Holbrook N. M.. Why leaves turn red in autumn. The role of anthocyanins in senescing leaves of Red-Osier Dogwood.  Plant Physiology. (2001);  127 566-574
  • 39 Feucht W., Treutter D.. The role of flavan-3-ols and proanthocyanidins in plant defence. Inderjit, S., Dakshini, K., M., M., and Foy, C. L., eds. Principles and Practices in Plant Ecology. Boca Raton; CRC Press (1999): 307-338
  • 40 Feucht W., Treutter D., Polster J.. Flavanol binding of nuclei from tree species.  Plant Cell Reports. (2004);  22 430-436
  • 41 Feucht W., Treutter D., Dithmar H., Polster J.. Flavanols in somatic cell division and male meiosis of tea (Camellia sinensis) anthers.  Plant Biology. (2005);  7 168-175
  • 42 Fischbach R. J., Kossmann B., Panten H., Steinbrecher R., Heller W., Seidlitz H. K., Sandermann H., Hertkorn N., Schnitzler J.-P.. Seasonal accumulation of ultraviolet-B screening pigments in needles of Norway spruce (Picea abies [L.] Karst.).  Plant, Cell and Environment. (1999);  22 27-37
  • 43 Fofana B., McNally D. J., Labbé C., Boulanger R., Benhamou N., Séguin A., Bélanger R. R.. Milsana-induced resistance in powdery mildew-infected cucumber plants correlates with the induction of chalcone synthase and chalcone isomerase.  Physiological and Molecular Plant Pathology. (2002);  61 121-132
  • 44 Forkner R. E., Marquis R. J., Lill J. T.. Feeny revisited: condensed tannins as anti-herbivore defences in leaf-chewing herbivore communities of Quercus.  Ecological Entomology. (2004);  29 174-187
  • 45 Gallet C., Després L., Tollenaere C.. Phenolic response of Trollius europaeus to Chiastocheta invasion.  Polyphenols Communications. (2004);  2004 759-760
  • 46 Gandikota M., DeKochko A., Chen L., Ithal N., Fauquet C., Reddy A. R.. Development of transgenic rice plants expressing maize anthocyanin genes and increased blast resistance.  Molecular Breeding. (2001);  7 73-83
  • 47 Gayler S., Leser C., Priesack E., Treutter D.. Modelling the effect of environmental factors on the “trade-off” between growth and defensive compounds in young apple trees.  Trees. (2004);  18 363-371
  • 48 Gould K. S., Mickelvie J., Markham K. R.. Do anthocyanins function as antioxidants in leaves? Imaging of H2O2 in red and green leaves after mechanical injury.  Plant, Cell and Environment. (2002);  25 2161-1269
  • 49 Grayer R. J., Harborne J. B.. A survey of antifungal compounds from higher plants, 1982 - 1993.  Phytochemistry. (1994);  37 19-42
  • 50 Hada H., Hidema J., Maekawa M., Kumagai T.. Higher amounts of anthocyanins and UV-absorbing compounds effectively lowered CPD photorepair in purple rice (Oryza sativa L.).  Plant, Cell and Environment. (2003);  26 1691-1701
  • 51 Halbwirth H., Fischer T. C., Roemmelt S., Spinelli F., Schlangen K., Peterek S., Sabatini E., Messina C., Speakman J.-B., Andreotti C., Rademacher W., Bazzi C., Costa G., Treutter D., Forkmann G., Stich K.. Induction of antimicrobial 3-deoxyflavonoids in pome fruit trees controls fire blight.  Zeitschrift für Naturforschung. (2003);  58c 765-770
  • 52 Hammerschmidt R.. Phytoalexins: what have we learned after 60 years?.  Annual Reviews in Phytopathology. (1999);  37 285-306
  • 53 Harborne J. B.. Plant polyphenols and their role in plant defence mechanisms. Brouillard, R., Jay, M., and Scalbert, A., eds. Polyphenols 1994. Versailles; INRA Editions (1994): 19-26
  • 54 Haribal M., Feeny P.. Combined roles of contact stimulant and deterrents in assessment of host-plant quality by ovipositing zebra swallowtail butterflies.  Journal of Chemical Ecology. (2003);  29 653-670
  • 55 Harrison M. J., Dixon R. A.. Spatial pattern of expression of flavonoid/isoflavonoid pathway genes during interactions between roots of Medicago trunculata and the mycorrhizal fungus Glomus versiforme.  The Plant Journal. (1994);  6 9-20
  • 56 Heil M., Delsinne T., Hilpert A., Schürkens S., Andary C., Linsenmair K. E., Sousa M., McKey D.. Reduced chemical defence in ant-plants? A critical re-evaluation of a widely accepted hypothesis.  Oikos. (2002);  99 457-468
  • 57 Herms D. A., Mattson W. J.. The dilemma of plants: to grow or defend.  The Quarterly Review of Biology. (1992);  67 283-335
  • 58 Hoffmann-Campo C. B., Harborne J. B., McCaffery A. R.. Pre-ingestive and post-ingestive effects of soya bean extracts and rutin on Trichoplusia ni growth.  Entomologia Experimentalis et Applicata. (2001);  98 181-194
  • 59 Hungria M., Stacey G.. Molecular signals exchanged between host plants and rhizobia: basic aspects and potential application in agriculture.  Soil Biology and Biochemistry. (1997);  29 819-830
  • 60 Inderjit S., Gross E.. Plant phenolics: potential role in aquatic and terrestrial ecosystems. Martens, S., Treutter, D., and Forkmann, G., eds. Polyphenols 2000. Freising; (2000): 206-234
  • 61 Jansen M. A. K.. Ultraviolet-B radiation effects on plants: induction of morphogenic responses.  Physiologia Plantarum. (2002);  116 423-429
  • 62 Ju Z., Bramlage W. J.. Phenolics and lipid-soluble antioxidants in fruit cuticle of apples and their antioxidant activities in model systems.  Postharvest Biology and Technology. (1999);  16 107-118
  • 63 Kangatharalingam N., Pierce M. L., Bayles M. B., Essenberg M.. Epidermal anthocyanin production as an indicator of bacterial blight resistance in cotton.  Physiological and Molecular Plant Pathology. (2002);  61 189-195
  • 64 Keller M., Rogiers S. Y., Schultz H. R.. Nitrogen and ultraviolett radiation modify grapevines' susceptibility to powdery mildew.  Vitis. (2003 a);  42 87-94
  • 65 Keller M., Viret O., Cole F. M.. Botrytis cinerea infection in grape flowers: defense reaction, latency, and disease expression.  Phytopathology. (2003 b);  93 316-322
  • 66 Kobayashi H., Naciri-Graven Y., Broughton W. J., Perret X.. Flavonoids induce temporal shifts in gene-expression of nod-box controlled loci in Rhizobium sp. NGR234.  Molecular Microbiology. (2004);  51 335-347
  • 67 Kolb C. A., Käser M. A., Kopecký J., Zotz G., Riederer M., Pfündel E. E.. Effects of natural intensities of visible and ultraviolet radiation on epidermal ultraviolet screening and photosynthesis in grape leaves.  Plant Physiology. (2001);  127 863-875
  • 68 Kuc J.. Relevance of phytoalexins - a critical review. Geibel, M., Treutter, D., and Feucht, W., eds. Natural Phenols in Plant Resistance. Freising; Acta Horticulturae (1994): 526-539
  • 69 Lagrange H., Jay-Allemand C., Lapeyrie F.. Rutin, the phenolglycoside from eucalyptus root exudates, stimulates Pisolithus hyphal growth at picomolar concentrations.  New Phytologist. (2001);  149 349-355
  • 70 Lattanzio V., Cardinali A., Palmieri S.. The role of phenolics in the postharvest physiology of fruits and vegetables: browning reactions and fungal diseases.  Italian Journal of Food Science. (1994);  1 3-22
  • 71 Lattanzio V.. Bioactive polyphenols: Their role in quality and storability of fruit and vegetables.  Journal of Applied Botany. (2003);  77 128-146
  • 72 Lavola A., Julkunen-Tiitto R., Roininen H., Aphalo P.. Host-plant preference of an insect herbivore mediated by UV‐B and CO2 in relation to plant secondary metabolites.  Biochemical Systematics and Ecology. (1998);  26 1-12
  • 73 Leser C., Treutter D.. Effects of nitrogen supply on growth, contents of phenolic compounds and pathogen (scab) resistance of apple trees.  Physiologia Plantarum. (2005);  123 49-56
  • 74 Lo S.-C. C., DeVerdier K., Nicholson R. L.. Accumulation of 3-deoxyanthocyanidin phytoalexins and resistance to Colletotichum sublineolum in sorghum.  Physiological and Molecular Plant Pathology. (1999);  55 263-273
  • 75 Loomis W. E.. Growth and differentiation. Loomis, W. E., ed. Growth and Differentiation in Plants. Ames; Iowa State College Press (1953): 1-17
  • 76 Mallikarjuna N., Kranthi K. R., Jadhav D. R., Kranthi S., Chandra S.. Influence of foliar chemical compounds on the development of Spodoptera litura (Fab.) in interspecific derivatives of groundnut.  Journal of Applied Entomology. (2004);  128 321-328
  • 77 Manthey J. A., Grohmann K., Berhow M. A., Tisserat B.. Changes in citrus leaf flavonoid concentrations resulting from blight-induced zinc-deficiency.  Plant Physiology and Biochemistry. (2000);  38 333-343
  • 78 Mathesius U.. Conservation and divergence of signalling pathways between roots and soil microbes - the Rhizobium-legume symbiosis compared to the development of lateral roots, mycorrhizal interactions and nematode-induced galls.  Plant and Soil. (2003);  255 105-119
  • 79 Mathesius U., Schlamann H. R. M., Spaink H. P., Sautter C., Rolfe B. C., Djordjevic M. A.. Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides.  The Plant Journal. (1998);  14 23-24
  • 80 Mattson W. J., Kuokkanen K., Niemelä P., Julkunen-Tiitto R., Kellomäki S., Tahvanainen J.. Elevated CO2 alters birch resistance to Lagomorpha herbivores.  Global Change Biology. (2004);  10 1402-1413
  • 81 Matyssek R., Schnyder H., Elstner E. F., Munch J. C., Pretzsch H., Sandermann H.. Growth and parasite defence in plants: the balance between resource sequestration and retention: in lieu of a guest editorial.  Plant Biology. (2002);  4 133-136
  • 82 Mayr U., Michalek S., Treutter D., Feucht W.. Phenolic compounds of apple and their relationship to scab resistance.  Journal of Phytopathology. (1997);  145 69-75
  • 83 Mayr U., Treutter D.. Flavanols as defence barriers in apple leaves against the apple scab fungus (Venturia inaequalis). .  Acta Horticulturae. (1998);  456 79-82
  • 84 McNally D. J., Wurms K. V., Labbé C., Bélanger R. R.. Synthesis of C-glycosyl flavonoid phytoalexins as a site-specific response to fungal penetration in cucumber.  Physiological and Molecular Plant Pathology. (2003);  63 293-303
  • 85 Merzylak M. N., Solovchenko A. E., Chivkunova O. B.. Patterns of pigment changes in apple fruits during adaptation to high sunlight and sunscald development.  Plant Physiology and Biochemistry. (2002);  40 679-684
  • 86 Mo Y. Y., Geibel M., Bonsall R. F., Gross D. C.. Analysis of sweet cherry (Prunus avium L.) leaves for plant signal molecules that activate the syrB gene required for synthesis of the phytotoxin, syringomycin, by Pseudomonas syringae pv. syringae. .  Plant Physiology. (1995);  107 603-612
  • 87 Moore J. P., Westall K. L., Ravenscroft N., Farrant J. M., Lindsey G. G., Brandt W. F.. The predominant polyphenol in the leaves of the ressurrection plant Myrothamnus flabellifolius, 3,4,5-tri-O-galloylquinic acid, protects membranes against desiccation and free radical induced oxidation.  Polyphenols Communications Helsinki. (2004);  2004 79
  • 88 Murphy A., Peer W. A., Taiz L.. Regulation of auxin transport by aminopeptidases and endogenous flavonoids.  Planta. (2000);  211 315-324
  • 89 Nicholson R. L., Hammerschmidt R.. Phenolic compounds and their role in disease resistance.  Annual Reviews in Phytopathology. (1992);  30 369-389
  • 90 Nicholson R. L., Wood K. V.. Phytoalexins and secondary products, where are they and how can we measure them?.  Physiological and Molecular Plant Pathology. (2001);  59 63-69
  • 91 Nielsen K., Deroles S. C., Markham K. R., Bradley M. J., Podivinsky E., Manson D.. Antisense flavonol synthase alters copigmentation and flower color in lisianthus.  Molecular Breeding. (2002);  9 217-229
  • 92 Nikiforova V., Freitag J., Kempa S., Adamik M., Hesse H., Hoefgen R.. Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity.  The Plant Journal. (2003);  33 633-650
  • 93 Nykänen H., Koricheva J.. Damage-induced changes in woody plants and their effects on insect herbivore performance: a meta-analysis.  Oikos. (2004);  104 247-268
  • 94 Padmavati M., Sakthivel N., Thara K. V., Reddy A. R.. Differential sensitivity of rice pathogens to growth inhibition by flavonoids.  Phytochemistry. (1997);  46 499-502
  • 95 Parvez M. M., Tomita-Yokotani K., Fujii Y., Konishi T., Iwashina T.. Effects of quercetin and its seven derivatives on the growth of Arabidopsis thaliana and Neurospora crassa.  Biochemical Systematics and Ecology. (2004);  32 631-635
  • 96 Picinelli A., Dapena E., Mangas J. J.. Polyphenolic pattern in apple tree leaves in relation to scab resistance. A preliminary study.  Journal of Agricultural and Food Chemistry. (1995);  43 2273-2278
  • 97 Pietrini F., Iannelli M. A., Massacci A.. Anthocyanin accumulation in the illuminated surface of maize leaves enhances protection from photo-inhibitory risks at low temperature, without further limitation to photosynthesis.  Plant, Cell and Environment. (2002);  25 1251-1259
  • 98 Pizzi A., Cameron F. A.. Flavonoid tannins - structural wood components for drought-resistant mechanisms of plants.  Wood Science and Technology. (1986);  20 119
  • 99 Ponce M. A., Scervino J. M., Erra-Balsells R., Ocampo J. A., Godeas A. M.. Flavonoids from shoots and roots of Trifolium repens (white clover) grown in presence or absence of the arbuscular mycorrhizal fungus Glomus intraradices.  Phytochemistry. (2004);  65 1925-1930
  • 100 Reuber S., Bornman J. F., Weissenböck G.. Phenylpropanoid compounds in primary leaf tissues of rye (Secale cereale). Light response of their metabolism and the possible role in UV‐B protection.  Physiologia Plantarum. (1996);  97 160-168
  • 101 Riipi M., Ossipov V., Lempa K., Haukioja E., Koricheva J., Ossipova S., Pihlaja K.. Seasonal changes in birch leaf chemistry: are there trade-offs between leaf growth and accumulation of phenolics?.  Oecologia. (2001);  130 380-390
  • 102 Römmelt S., Treutter D., Speakman J.B., Rademacher W.. Effects of prohexadione-Ca on the flavonoid metabolism of apple with respect to plant resistance against fire blight.  Acta Horticulturae. (1999);  489 359-363
  • 103 Roemmelt S., Zimmermann N., Rademacher W., Treutter D.. Formation of novel flavonoids in apple (Malus × domestica) treated with the 2-oxoglutarate-dependent dioxygenase inhibitor prohexadione-Ca.  Phytochemistry. (2003);  64 709-716
  • 104 Rosati C., Simoneau P., Treutter D., Poupard P., Cadot Y., Cadic A., Duron M.. Engineering of flower color in forsythia by expression of two indepentenly-transformed dihydroflavonol 4-reductase and anthocyanidin synthase genes of flavonoid pathway.  Molecular Breeding. (2003);  12 197-208
  • 105 Rozema J., VanDeStaaij J., Björn L. O., Caldwell M.. UV‐B as an environmental factor in plant life: stress and regulation.  Tree. (1997);  12 22-28
  • 106 Rozema J., Björn L. O., Bornman J. F., Gaberščik A., Häder D.-P., Trošt T., Germ M., Klisch M., Gröniger A., Sinha R. P., Lebert M., He Y.-Y., Buffoni-Hall R., DeBakker N. V. J., VanDeStaaij J., Meijkamp B. B.. The role of UV‐B radiation in aquatic and terrestrial ecosystems - an experimental and functional analysis of the evolution of UV-absorbing compounds.  Journal of Photochemistry and Photobiology. (2002);  B 66 2-12
  • 107 Rühmann S., Leser C., Bannert M., Treutter D.. Relationship betwen growth, secondary metabolism, and resistance of apple.  Plant Biology. (2002);  4 137-193
  • 108 Rühmann S., Treutter D.. Effect of N-nutrition in apple on the response of its secondary metabolism to prohexadione-Ca treatment.  European Journal of Horticultural Science. (2003);  68 152-159
  • 109 Ryan K. G., Swinny E. E., Markham K. R., Winefield C.. Flavonoid gene expression and UV photoprotection in transgenic and mutant Petunia leaves.  Phytochemistry. (2002);  59 23-32
  • 110 Sandermann H., Ernst D., Heller W., Langebartels C.. Ozone: an abiotic elicitor of plant defence reactions.  Trends in Plant Science. (1998);  3 47-50
  • 111 Schlösser E.. Preformed phenols as resistance factors. Geibel, M., Treutter, D., and Feucht, W., eds. Natural Phenols in Plant Resistance. Freising; Acta Horticulturae (1994): 615-630
  • 112 Schijlen E. G. W. M., Ric de Vos C. H., VanTunen A. J., Bovy A.G.. Modification of flavonoid biosynthesis in crop plants.  Phytochemistry. (2004);  65 2631-2648
  • 113 Shiozaki N., Hattori I., Gojo R., Tezuka T.. Activation of growth and nodulation in a symbiotic system between pea plants and legumious bacteria by near-UV radiation.  Journal of Photochemistry and Photobiology. (1999);  B50 33-37
  • 114 Shirley B. W.. Flavonoid biosynthesis: “new” functions for an “old” pathway.  Trends in Plant Science. (1996);  1 377-382
  • 115 Simmonds M. S. J.. Flavonoid-insect interactions: recent advances in our knowledge.  Phytochemistry. (2003);  64 21-30
  • 116 Skadhauge B., Thomsen K., von Wettstein D.. The role of barley testa layer and its flavonoid content in resistance to Fusarium infections.  Hereditas. (1997);  126 147-160
  • 117 Snyder B. A., Leite B., Hipskind J., Butler L. G., Nicholson R. L.. Accumulation of sorghum phytoalexins induced by Colletotrichum graminicola at the infection site.  Physiological and Molecular Plant Pathology. (1991);  39 463-470
  • 118 Snyder B. A., Nicholson R.L.. Synthesis of phytoalexins in sorghum as a site specific response to fungal ingress.  Science. (1990);  248 1637-1639
  • 119 Sosa T., Chaves N., Alias J. C., Escudero J. C., Henao F., Gutiérrez-Merino C.. Inhibition of mouth skeletal muscle relaxation by flavonoids of Cistus ladanifer L.: a plant defense mechanism against herbivores.  Journal of Chemical Ecology. (2004);  30 1087-1101
  • 120 Stewart A. J., Chapman W., Jenkins G. I., Graham I., Martin T., Crozier A.. The effect of nitrogen and phosphorus deficiency on flavonol accumulation in plant tissues.  Plant, Cell and Environment. (2001);  24 1189-1197
  • 121 Tattini M., Galardi C., Pinelli P., Massai R., Remorini D., Agati G.. Differential accumulation of flavonoids and hydroxycinnamates in leaves of Ligustrum vulgare under excess light and drought stress.  New Phytologist. (2004);  163 547-561
  • 122 Tegelberg R., Julkunen-Tiitto R., Aphalo P. J.. Red : far-red light ratio and UV‐B radiation: their effects on leaf phenolics and growth of silver birch seedlings.  Plant, Cell and Environment. (2004);  27 1005-1013
  • 123 Teklemariam T., Blake T. J.. Effects of UV‐B preconditioning on heat tolerance of cucumber (Cucumis sativus L.).  Environmental and Experimental Botany. (2003);  50 169-182
  • 124 Thoison O., Sévenet T., Niemeyer H. M., Russell G. B.. Insect antifeedant compounds from Nothofagus dombeyi and N. pumilio.  Phytochemistry. (2004);  65 2173-2176
  • 125 Tomita-Yokotani K., Kato T., Parvez M. M., Mori Y., Goto N., Hasegawa K.. Approach of allelopathy study with Arabidopsis thaliana (L.) Hevnh. and Neurospora crassa.  Weed Biology and Management. (2003);  3 93-97
  • 126 Treutter D., Feucht W.. The pattern of flavan-3-ols in relation to scab resistance of apple cultivars.  Journal of Horticultural Science. (1990);  65 511-517
  • 127 VanLoon J. J. A., Wang C. Z., Nielsen J. K., Gols R., Qiu Y. T.. Flavonoids from cabbage are feeding stimulants for diomandback moth larvae additional to glucosinolates: chemoreception and behaviour.  Entomologia Experimentalis et Applicata. (2002);  104 27-34
  • 128 Venisse J.-S., Malnoy M., Faize M., Paulin J.-P., Brisset M.-N.. Modulation of defense responses of Malus ssp. during compatible and incompatible interactions with Erwinia amylovora.  Molecular Plant-Microbe Interactions. (2002);  15 1204-1212
  • 129 Webster G., Jain V., Davey M. R., Gough C., Vasse J., Dénarié J., Coking E. C.. The flavonoid naringenin stimulates the intercellular colonization of wheat roots by Azorhizobium caulinodans.  Plant, Cell and Environment. (1998);  21 373-383
  • 130 Widstrom N. W., Snook M. E.. Recurrent selection for maysin, a compound in maze silks, antibiotic to earworm.  Plant Breeding. (2001);  120 357-359
  • 131 Winkel-Shirley B.. Evidence for enzyme complexes in the phenylpropanoid and flavonoid pathways.  Physiologia Plantarum. (1999);  107 142-149
  • 132 Yamamoto M., Nakatsuka S., Otani H., Kohmoto K., Nishimura S.. (+)-Catechin acts as an infection-inhibiting factor in strawberry leaf.  Phytopathology. (2000);  90 595-600
  • 133 Zhang D., Quantick P. C.. Effects of chitosan coating on enzymatic browning and decay during postharvest storage of litchi (Litchi chinensis Sonn.) fruit.  Postharvest Biologa and Technology. (1997);  12 195-202

D. Treutter

FG Obstbau
Technische Universität München

Alte Akademie 16

85350 Freising

Germany

Email: dieter.treutter@wzw.tum.de

Guest Editor: R. Matyssek