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Flavonoid Function and Activity to Plants and Other Organisms

Flavonoid Function and Activity to Plants and Other Organisms

Biological Sciences in Space, Vol.17 No.1 (2003): 24-44 function and activity © 2003 Jpn. Soc. Biol. Sci. Space

Flavonoid Function and Activity to and Other Organisms

Tsukasa Iwashina

Tsukuba Botanical Garden, National Science Museum, 4-1-1 Amakubo, Tsukuba-shi, Ibaraki, 305-0005,

Abstract Flavonoid compounds distribute widely in vascular plants and Bryophytes, and ca. 5,000 kinds have been reported as naturally occurring substances. Many biological activities of the were found until now. They include pollinator attractants, oviposition stimulants, feeding attractants and deterrents, allelopathy and phytoalexins. This paper reviews function and activity of flavonoids against plants and other organisms. Key words: flavonoids, pollinator attractants, feeding attractants and deterrents, allelopathy, phytoalexins

Introduction di-P-coumaroylglucoside) and 3-O-(3´´,6´´-di- Pinus sylvestris Flavonoid is the general name of compounds that have P-coumaroylglucoside) in (Pinaceae) (Jungblut et al., 1995), quercetin 3-O-galactoside, a fifteen-carbon skeleton, which consists of two phenyl O O rings (A- and B-rings) connected by a three-carbon bridge 3- -rutinoside and two P-coumaroyl 3- - Quercus ilex et al., (C-ring). In general, vascular plants and Bryophytes alone glucoside in (Fagaceae) (Skaltsa 1994), and of quercetin, and in Olea possess the biosynthetic ability of the flavonoids, except europea et al green algae, Nitella hookeri (Characeae) (Markham & (Oleaceae) (Karabourniotis ., 1992) act as UV- Porter, 1969), fungi, Aspergillus candidus and Phallus absorbing substances. More recently, it was proved that the major UV shield in the translucent and leaves of impudicus (Marchelli & Vining, 1973; Bohm, 1975), and nobile marine coral, Echinophora lamellosa (Sanduja et al., 1984). the Himalayan alpine , (), O The flavonoids are divided into several classes, i.e., are five quercetin glycosides, quercetin 3- -glucoside, 3- O-galactoside, 3-O-rutinoside, 3-O-arabinopyranoside and anthocyanins, , , flavanones, dihydro- O et al flavonols, chalcones, , and proantho- new acylated 3- -glucoside (Iwashina ., unpublished cyanidins, etc. (Iwashina, 2000). Moreover, data). The occurrence of anthocyanins as pollinator attractants numerous sorts of flavonoid occur in plants with additional hydroxyl, methoxyl, methyl and/or glycosyl substitution is well-known as a function of the flavonoids in plants. Additionally, it is known that flavones and flavonols, which patterns. Additionally, aromatic and aliphatic acids, sulfate, prenyl or methylenedioxyl groups also attach to flavonoid can hardly see by human eyes, also act as pollinator nucleus and their glycosides. Thus, ca. 5,000 kinds of attractants in addition to visible anthocyanins. Recently, other functions, oviposition stimulants, feeding attractants, flavonoids have been reported as naturally occurring compounds (Harborne & Baxter, 1999). The isolation and feeding deterrents, allelopathy and phytoalexins of naturally identification, structures, distribution and biosynthesis of occurring flavonoids, were found by many authors. In this paper, the flavonoid function and activity to the flavonoids in plants were reviewed by many authors (e.g., Geissman, 1962; Markham, 1982; Stafford, 1990; plants and other organisms are reviewed. Mabry et al., 1970; Harborne et al., 1975; Harborne & Mabry, 1982; Harborne, 1988, 1994; Iwashina, 2000). The Pollinator attractants flavonoids as medicinal resources were also reviewed (e.g., Majority of the entomophilous in plants Cody et al., 1986, 1988). Especially, the pigments, kingdom were colored by various pigments. For example, anthocyanins were recently noticed as antioxidant, carotenoids are found as major pigments in many yellow antitumol, astoringents etc. (Ohba et al., 2000). However, flowers, such as Helianthus annuus, Taraxacum officinale the secondary metabolites involving the flavonoids were (Compositae) and Potentilla spp. (Rosaceae). On the other considered to be waste products of plant metabolism in the hand, anthochlor pigments are reported from Cosmos, early days of 20th century. One of the most important Anthirrhinum, Dahlia and Dianthus species and so on. function of flavonoids may be to serve as ultraviolet filter Betaxanthin pigments occur in yellow flowers of the order in land plants. It was shown by survey of some plants that except Caryophyllaceae and the flavonoids act as UV shield. Indeed, it was shown that Molluginaceae. Almost orange, red, purple and blue two acylated flavonol glycosides, kaempferol 3-O-(3´´,6´´- flowers, e.g., Rosa, Tulipa, Commerina, Delphinium, Viola etc. are due to the anthocyanin pigments, except those of Received: May 29, 2003 the order Caryophyllales including betalain pigments. The Address for correspondence: Tsukasa Iwashina so-called “black flowers” such as Fritillaria Tsukuba Botanical Garden, National Science Museum, camtschatcensis (Liliaceae) are also due to the 4-1-1 Amakubo, Tsukuba-shi, Ibaraki, 305-0005, Japan anthocyanins. These visible pigments act as pollinator E-mail: [email protected] attractants. In addition, it was proved that flavones and

－ 24 － Iwashina, T.

flavonols are also the pollinator attractants (Table 1). (Harborne & Smith, 1978). Though a major pigment of Flavones and flavonols have two absorbing bands in UV Crocosmia × crocosmiiflora orange-yellow flowers range (250-280 and 310-380 nm), but not in visible range. () is a water-soluble carotenoid, crocin (Ootani However, since some insects, especially bee, can & Hayashi, 1982), kaempferol 3-O-rhamnosylglucoside discriminate UV light (UV-A), flavones and flavonols also and quercetin 3-O-glucoside are accompanied (Ootani et act as attractants. Indeed, flavone and flavonol glycosides al., 1986). are detected from flowers of many plants, with visible color of Strongylodon macrobotrys (Legumi- pigments, anthocyanins, carotenoids and/or anthochlors, nosae) is bluish-green, in other words, jade color, and a and sometimes betalains. An acylated flavone, apigenin major visible pigment is anthocyanin, malvidin 3,5-di-O- 7-O-glucuronide-4´-O-(6´´-malonylglucoside) was isolated glucoside accompanied with C-glycosylflavones, from the deep purple flowers of Centaurea cyanus 7-O-glucoside and isovitexin (Iwashina et al., 1984b). (Compositae), with an acylated anthocyanin, cyanidin 3- The visible pigments in the flowers of cactaceous O-(6´´-succinylglucoside)-5-O-glucoside (Kondo et al., species are exclusively red purple betacyanins and yellow 1994). In this case, the flavone also acts as a copigment betaxanthins, and never synthesize the anthocyanins substance. On the other hand, isoflavonoids, flavanones, (Iwashina et al., 1985). However, other flavonoids occur dihydroflavonols, and flavan and proanthocyanidins do not in “betalain plant families”. Thus, quercetin 3-methyl ether seem to act as pollinator attractants, since absorption 7-O-glucoside and 4´-O-glucoside are present in the red maxima of those flavonoids are in 250-290 nm range alone, purple flowers of cactaceous plants, Neoporteria clavata which insects can not discriminate these UV range. and related species together with betacyanins (Iwashina et In case of tectorum (Iridaceae), though iso- al., 1986). In another cactus, Astrophytum myriostigma, flavonoids, such as and its 7-O-glucoside, the yellow flowers are due to flavonol aglycone, quercetin 7-O-glucoside and iristectorigenins are abundantly itself, which is contained in cells as the crystal form, without contained in , they were not detected from the betalain pigments (Iwashina et al., 1988). flowers (Iwashina & Ootani, 1998). Insteadly, the Similar situation was investigated in the genus Aloe anthocyanins, delphinidin 3-O-(P-coumaroylrutinoside)-5- (Liliaceae) and related genera. Aloe species can not O-glucoside and 3-O-rutinoside-5-O-glucoside (Ishikura, apparently synthesize the anthocyanins (Iwashina, 1980) and a C-glycosylflavone, embigenin 2´´-O- unpublished data). Their yellow and yellow orange flowers rhamnoside (Hirose et al., 1962) are present in the flowers are due to anthraquinone pigments such as barbaloin and as pollinator attractants. aloe-emodin (Iwashina et al., 1986). C-Glycosylflavones, Two rare flavonol allosides, kaempferol 3-O-alloside e.g., (Fig. 1-1) and (Fig. 1-2) coexist and rhamnocitrin 3-O-alloside, are found from the reddish with the anthraquinones, and may be function as pollinator purple flowers of Glaucidium palmatum (Glaucidiaceae), attractants (Iwashina et al., 1986). endemic to Japan (Iwashina & Ootani, 1990). Flavones and flavonols are present not only in yellow, In the flowers of Iris species, C-glycosylflavones and red, purple and blue flowers but also in almost wild white their O-glycosides, isovitexin (Fig. 1-12), (Fig. 1- ones. Thus, the insects, especially bee, can visit to white 13), swertisin (Fig. 1-14) and isovitexin 2´´-O-rhamnoside flowers. and 2´´-O-xyloside are present as pollinator attractants, with anthocyanins, malvidin and petunidin 3-O-(P- Oviposition stimulants coumaroylrutinoside)-5-O-glucosides (Hayashi et al., 1978, One of the most complex aspects of plant-insect et al 1980, 1989; Iwashina ., 1996; Iwashina & Ootani, interactions involves the oviposition response of insects to C 1996; Yabuya, 1987). A xanthone -, mangiferin, chemical substances. Many insects lay eggs on plants which has absorption maxima in UV range, is also present species, and various naturally occurring compounds Iris rossii et al in (Hayashi ., 1980). including flavonoids may be act as oviposition stimulants. The visible pigments in yellow flowers, such as Some chemicals, e.g., sterols, sinigrin, glucobrassicin, allyl Chimonanthus praecox (Calycanthaceae), Coronilla spp. isothiocyanate, α-farnesene, chlorogenic acid, adenosine, Helianthus annuus (Leguminosae), are carotenoids. In aristolochic acid etc., have been reported from some plants, flowers of these plants, flavonoid glycosides co-exist with such as Oryza sativa (Gramineae), Brassica oleracea carotenoids. Thus, quercetin 3-O-rutinoside, quercetin 3- (Cruciferae) and Citrus unshiu (Rutaceae) as oviposition O O -glucoside and kaempferol 3- -rutinoside are present in stimulants (Harborne, 1993). Some flavonoid compounds C. praecox et al O (Iwashina ., 2001), and 3- -glucoside-7,4´- are also listed as ovipotion stimulants (Table 2). The di-O-rhamnoside, 3-O-glucoside-7-O-rhamnoside and 3- flavonoids are inactive alone in many cases, and act as O O -glucoside of kaempferol (Fig. 1-5), and 3- -glucoside- stimulants by coexistence with other compounds. O O 7- -rhamnoside and 3- -glucoside of quercetin (Fig. 1- It has been reported by Nishida et al. (1987) that a C- 3) in Coronilla emerus (Harborne & Boardley, 1983), glycosylflavone, vicenin-2 (Fig. 2-2), two flavanones, O O haplogenin 3- -rutinoside and limocitrin 3- -rutinoside (Fig. 1-19) and hesperetin 7-O-rutinosides, and C. valentina glauca in subsp. (Harborne, 1981), and a flavonol, quercetin 3-O-rutinoside are oviposition quercetin 7-O-glucoside and 3-O-glucoside in H. annuus stimulants of swallowtail butterfly, Papilio xuthus, which

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lay eggs on young leaves of Citrus plants. However, the Fig. 2-5) were also reported (Ohsugi et al., 1985; Feeny et flavonoids were inactive by themselves alone, but elicited al., 1988; Tebayashi et al., 1995), , chalcone, oviposition behavior when mixed with other compounds, and anthocyanin were not known as oviposition 5-hydroxy-Nω-methyltriptamin and adenosine (Ohsugi stimulants. et al., 1985; Nishida et al., 1987). Similar situation has been reported in the case of a butterfly, Papilio protenor Feeding attractants demetrius and Citrus plants interaction. The oviposition Many insect larvae are “vegetarian”, and some P. protenor demetrius stimulants of are two flavanone secondary substances act as feeding attractants as well as O glycosides, naringenin 7- -neohesperidoside and ovipositin stimulants. For example, glucosinolate and hesperetin 7-O-rutinoside, but they were also inactive sinigrin, which are contained in the Cruciferae plants such without the presence of other compounds, L-( － )- as Brassica campestris, are toxic to many insects, but stachydrine, D-( － )-quinic acid, ( － )-synephrine and L- feeding attractant to an aphid, Brevicoryne brassicae ( )-proline (Honda, 1986, 1990). － (Harborne, 1993). Flavonoid compounds are also utilized Papilio polyxenes Another swallowtail butterfly, lay by some insects as attractants. Daucus carota eggs on carrot, (Umbelliferae), but not The feeding stimulants of silkworm, Bombix mori to Citrus plants. The stimulants were identified as luteolin Morus alba and M. nigra (Moraceae) have been reported O trans 7- -(6´´-malonylglucoside) and -chlorogenic acid. by Hamamura et al. (1962). Common flavonoid glycoside, These were also inactive alone, but in combination quercetin 3-O-glucoside (isoquercitrin) or a rare flavonol accounted for ca. 70% of the response to the parent extract. attached a hydroxyl group to 2´-position, (Fig. 3-1), In this case, though the acylated flavonoid conjugated was isolated and identified as ones of biting factors with a malonic acid is active, deacylated glycoside, luteolin 7-O- terpenoid, β -sitosterol. Morin occurs in mulberry wood glucoside is inactive (Feeny et al., 1988). rather than in the leaves, so that B. mori is unlikely to Luedorfia japonica A zeryntiine swallowtail butterfly, encounter it in its food in appreciable quantities. Therefore, Asarum Heterotropa lay eggs on the leaves of the genus (= ) it was described by Kato (1978) that morin can not be a (Aristolochiaceae). A new flavonol glycoside, natural feeding stimulant to silkworm. In addition, five O O 3- -glucosyl-(1 → 6)-galactoside-7- -glucoside, was essential oils, citral, terpinyl acetate, linalyl acetate, linalol isolated and identified from the leaves of A. asperum (= H. and β,γ-hexenol were found as attractants, and cellulose aspera) as an oviposition stimulant (Nishida, 1994, 1995). as swallowing factor with co-factors, sucrose, inositol, However, this flavonoid was also inactive alone but induced phosphate and silica. the specific oviposition response of L. japonica when tested Monophagous flea beetle, Phyllotreta armoraciae feeds as a mixture with other unidentified compounds. horseradish, Armoracia rusticana (Cruciferae) in nature. The flavonoids as oviposition stimulants have also been Two flavonol glycosides, kaempferol and quercetin 3-O- reported from the family Asclepiadaceae. The monarch xylosylgalactosides were isolated from the leaves of Danaus plexippus butterfly, lay eggs on the leaves of horseradish. Of their flavonoids, kaempferol glycoside Asclepias species. Haribal and Renwick (1996) isolated stimulated feeding in the flea beetle. However, this seven quercetin glycosides as oviposition stimulants from flavonoid was inactive alone, but elicited feeding behavior A. currassavica the fresh young terminal leaves of , and six when mixed allylglucosinolate as some cases of oviposition O O were identified as 3- -(2´´,6´´-di- -rhamnosyl)-(1 → 2)- stimulants (Nielsen et al., 1979). The stimulant flavonoid galactoside, 3-O-glucosyl-(1 6)-galactoside, 3-O- → was later identified as new glycoside, kaempferol 3-O- rhamnosyl-(1 2)-galactoside, 3-O-rutinoside, 3-O- → xylosyl-(1 → 2)-galactoside and inactive one as quercetin galactoside and 3-O-glucoside, and one was presumed as 3-O-xylosyl-(1 → 2)-galactoside (Larsen et al., 1982). 3-O-(2´´,6´´-di-O-rhamnosyl)-(1 2)-glucoside. Of these → Three plant hoppers, Nilaparvata lugens, Sogatella glycosides, tri- and di-glycosides especially function as furcifera and Laodelphax striatellus, are known as stimulants. important rice pests. Besson et al. (1985) reported that In contrast with oviposition stimulant, it was reported their feeding stimulants are eight flavone C-glycosides in by Tabashnik (1987) that the flavonoid act as oviposition the whole plants of Oryza sativa. They were identified as and feeding deterrent. He found that oviposition by schaftoside (apigenin 6-C-glucoside-8-C- α -L- butterfly, Pieris rapae is deterred by spraying quercetin 3- arabinopyranoside, Fig. 3-2), neoschaftoside (apigenin 6- O-rutinoside and also coumarin on Brassica oleracea. It C-glucoside-8-C- β -L-arabinopyranoside, Fig. 3-3), is noteworthy that quercetin 3-O-rutinoside acts as carlinoside (luteolin 6-C-glucoside-8-C- α -L- stimulant to Danaus plexippus, but as deterrent to Pieris arabinopyranoside, Fig. 3-5), neocarlinoside (luteolin 6- rapae. C-glucoside-8-C- β -L-arabinopyranoside, Fig. 3-6), Many flavonoids which are active as oviposition isoorientin 2´´-O-glucoside, isoscoparin 2´´-O-glucoside, stimulants belong to flavanone and flavonol glycosides. isoscoparin 2´´-O-(6´´´-P-coumaroylglucoside) and C Though -glycosylflavone (vicenin-2), acylated flavone isoscoparin 2´´-O-(6´´´-feruloylglucoside). O O -glycoside (luteolin 7- -(6´´-malonylglucoside), flavan A flavone O-glycoside was isolated from the whole 3-ol (D-, Fig. 2-4) and dihydroflavonol (,

－ 26 － Iwashina, T.

none Centaurea cyanus (deep purple) (Compositae) (Kondo et al., 1994) apigenin 7-O-glucuronide-4´-O-(6´´-malonylglucoside) cyanidin 3-O-(6´´-succinylglucoside)-5-O-glucoside (anthocyanin) Chimonanthus praecox (yellow) (Calycanthaceae) (Iwashina et al., 2001) quercetin 3-O-rutinoside, quercetin 3-O-glucoside, kaempferol 3-O- rutinoside carotenoids Coronilla emerus (yellow) (Leguminosae) (Harborne & Boardley, 1983) kaempferol 3-O-glucoside-7,4´-di-O-rhamnoside, kaempferol 3-O- glucoside-7-O-rhamnoside, kaempferol 3-O-glucoside, quercetin 3-O-glucoside-7-O-rhamnoside, quercetin 3-O-glucoside carotenoids Coronilla valentina subsp. glauca (yellow) (Leguminosae) (Harborne, 1981) haplogenin 3-O-rutinoside, limocitrin 3-O-rutinoside carotenoids Crocosmia × crocosmiiflora (orange-yellow) (Iridaceae) (Ootani & Hayashi, 1982; Ootani et al., 1986) kaempferol 3-O-rhamnosylglucoside, quercetin 3-O-glucoside crocin (water-soluble carotenoid), cyanidin 3-O-glucoside (anthocya- nin) Eriophyllum spp. (yellow) (Compositae) (Harborne & Smith, 1978) 7-O-glucoside, 7-O-glucoside, quercetin 5-O- glucoside none Geraea canescens (yellow) (Compositae) (Harborne & Smith, 1978) corniculatusin 3-O-glucoside none Glaucidium palmatum (reddish purple) (Glaucidiaceae) (Iwashina & Ootani, 1990) kaempferol 3-O-alloside, rhamnocitrin 3-O-alloside delphinidin 3-O-diglucoside (anthocyanin) Helianthus annuus (yellow) (Compositae) (Harborne & Smith, 1978) quercetin 7-O-glucoside, quercetin 3-O-glucoside carotenoids Iris ensata (purple) (Iridaceae) (Hayashi et al., 1978; Iwashina et al., 1996) isovitexin, isovitexin 2´´-O-rhamnoside, isovitexin 2´´-O-xyloside malvidin 3-O-(P-coumaroylrutinoside)-5-O-glucoside, petunidin 3-O- (P-coumaroylrutinoside)-5-O-glucoside (anthocyanin) Iris laevigata (purple) (Iridaceae) (Yabuya, 1987; Iwashina & Ootani, 1996) isovitexin, vitexin, swertisin malvidin 3-O-(P-coumaroylrutinoside)-5-O-glucoside, petunidin 3-O- (P-coumaroylrutinoside)-5-O-glucoside (anthocyanin) Iris rossii (blue-purple) (Iridaceae) (Hayashi et al., 1980) swertisin, mangiferin* acylated delphinidin triglucoside (anthocyanin) Iris setosa (pale purple) (Iridaceae) (Hayashi et al., 1989) isovitexin X´´-O-glucoside, vitexin, isovitexin malvidin 3-O-(P-coumaroylrutinoside)-5-O-glucoside, petunidin 3-O- (P-coumaroylrutinoside)-5-O-glucoside (anthocyanin) Magnolia spp. (pink) (Magnoliaceae) (Francis & Harborne, 1966) kaempferol 3-O-rhamnosylglucoside, quercetin 3-O-rhamnosyl- Fig. 1. Chemical structures of flavonoids as pollinator attractants. glucoside, quercetin 3-O-glucoside, quercetin 1 = orientin, 2 = isoorientin, 3 = quercetin, 4 = apigenin, 5 kaempferol, 6 peonidin 3-O-rhamnosylglucoside-5-O-glucoside, peonidin 3-O- = haplogenin, 7 = limocitrin, 8 = quercetagetin, 9 = patuletin, 10 = rhamnosylglucoside, peonidin 3,5-di-O-glucoside, peonidin 3-O- corniculatusin, 11 = rhamnocitrin, 12 = isovitexin, 13 = vitexin, 14 = glucoside, cyanidin 3-O-rhamnosylglucoside, cyanidin 3-O- swertisin, 15 = , 16 = luteolin, 17 = quercetin 3-methyl ether, glucoside (anthocyanin) 18 = chalcononaringenin, 19 = naringenin, 20 = cirsiliol, 21 = butein and Mimulus luteus (yellow with reddish spots) (Scrophulariaceae) (Bloom 22 = sulphuretin. & Vickery, 1973) quercetin 7-O-glucoside, quercetin 3-O-glucoside, kaempferol 7-O- glucoside, kaempferol 3-O-glucoside, apigenin 7-O-glucoside, herbacetin 7-O-glucoside, luteolin 7-O-glucoside carotenoids, cyanidin 3-O-glucosie (anthocyanin) Neoporteria clavata (red purple) (Cactaceae) (Iwashina et al., 1983, 1984a; Iwashina & Ootani, 1986) quercetin 3-methyl ether 7-O-glucoside, quercetin 3-methyl ether 4´- Table 1 Flavonoids as pollinator attractants O-glucoside Species (Flower color) (References) betacyanins (betalain) Major flavonoids Oenothera hookeri subsp. venusta (yellow) (Onagraceae) (Dement & Major visible pigments (Classes) Raven, 1974) chalcononaringenin 2´-O-glucoside Aloe capitata (yellow orange) (Liliaceae) (Iwashina et al., 1986) carotenoids orientin, isoorientin Potentilla spp. (yellow) (Rosaceae) (Harborne & Nash, 1984) barbaloin (anthraquinone) chalcononaringenin 2´-O-glucoside, quercetin 3-O-glucoside, Astrophytum myriostigma (yellow) (Cactaceae) (Iwashina et al., 1988) quercetin 3-O-glucuronide, quercetin 3´-O-glucoside, naringenin quercetin 7-O-glucoside carotenoids

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Table 1 (continue) Rudbeckia hirta (yellow) (Compositae) (Thompson et al., 1972) quercetagetin, patuletin, circiliol 3-O-glucoside carotenoids Silene armeria (red purple) (Caryophyllaceae) (Iwashina & Ootani, 1987) isovitexin, isoorientin cyanidin 3-O-rhamnosylglucoside, cyanidin 3-O-glucoside (anthocya- nin) Strongylodon macrobotrys (bluish-green) (Leguminosae) (Iwashina et al., 1984b) isovitexin, isovitexin 7-O-glucoside malvidin 3,5-di-O-glucoside Viguiera laciniata (yellow) (Compositae) (Harborne & Smith, 1978) butein 4´-O-glucoside, sulphuretin 6-O-glucoside carotenoids Viguiera spp. (yellow) (Compositae) (Rieseberg & Schilling, 1985) butein 4´-O-glucoside, sulphuretin 6-O-glucoside, quercetin 3-methyl ether 7-O-glucoside, quercetin 3-methyl ether 7-O-glucuronide, quercetin 3-methyl ether 7-O-galactoside, luteolin 7-O-glucoside, quercetin 7-O-glucoside none * C-Glycosylxanthone.

Fig. 3. Chemical structures of flavonoids as feeding attractants. 1 = morin, 2 = schaftoside, 3 = neoschaftoside, 4 = , 5 = carlinoside, 6 = neocarlinoside, 7 = , 8 = isoscoparin, 9 = and 10 = . Quercetin, kaempferol and isoorientin (see, Fig. 1), and taxifolin and catechin (see, Fig. 2).

Table 3 Flavonoids as feeding attractants Fig. 2. Chemical structures of flavonoids as oviposition stimulants. Flavonoids 1 = hesperetin, 2 = vicenin-2, 3 = isorhamnetin, 4 = catechin and 5 = Host plants Insects (References) taxifolin. Luteolin, naringenin and quercetin (see, Fig. 1). quercetin 3-O-glucoside, morin, [ β -sitosterol], [sucrose], [inositol] (biting factor), [cirtal], [linalol], [terpinyl acetate], [lynalyl acetate], [ β,γ-hexenol] (attractants), [cellulose], [silicate], [phosphate] Table 2 Flavonoids as oviposition stimulants (swallowing factor) Flavonoids Morus alba, M. tinctoria (Moraceae) Bombix mori (Hamamura et Plants Insects (References) al., 1962; Kato, 1978) kaempferol 3-O-xylosyl-(1 → 2)-galactoside, [allylglucosinolate] luteolin 7-O-(6´´-malonylglucoside), [trans-chlorogenic acid] Armoracia rusticana (Cruciferae) Phyllotreta armoraciae Daucus carota (Umbelliferae) Papilio polyxenes (Feeny et al., (Nielsen et al., 1979; Larsen et al., 1982) 1988) schaftoside, neoschaftoside, carlinoside, isoorientin 2´´-O-glucoside, vicenin-2, naringenin 7-O-rutinoside, hesperetin 7-O-rutinoside, neocarlinoside, isoscoparin 2´´-O-glucoside, isoscoparin 2´´-O- quercetin 3-O-rutinoside, [5-hydroxy-Nω-methyltryptamine], (6´´´-P-coumaroylglucoside), isoscoparin 2´´-O-(6´´´-feruloyl- [adenosine] glucoside) Citrus unshiu (Rutaceae) Papilio xuthus (Ohsugi et al., 1985; Oryza sativa (Gramineae) Nilaparvata lungens, Sogatella furcifera, Nishida et al., 1987) Laodelphax striatellus (Besson et al., 1985) naringenin 7-O-neohesperidoside, hesperetin 7-O-rutinoside, [L-( － )- nepetin 7-O-rhamnoside stachydrine], [D-( －)-quinic acid], [( －)-synephrine], [L-( －)- Alternanthera phylloxeroides (Amaranthaceae) Agasicles sp. proline] (Zielske et al., 1972) Citrus unshiu, C. natsudaidai, Fagara ailanthoides (Rutaceae) taxifolin, aromadendrin, pinocembrin Papilio protenor demetrius (Honda, 1986, 1990) Prunus armeniaca (Rosaceae) Scolytus mediterraneus (Levy et al., isorhamnetin 3-O-glucosyl-(1 → 6)-galactoside-7-O-glucoside, 1974) [unknown compounds] phloretin 2´-O-glucoside Asarum aspera (= Heterotropa asperum) (Aristolochiaceae) Malus spp. (Rosaceae) Aphis pomi, Rhapalosiphum insertum Luehdorfia japonica (Nishida, 1994) (Klingauf, 1971) D-catechin, taxifolin, quercetin 7-O-glucoside (+)-catechin 7-O-xyloside, [lupeyl cerotate] Vigna angularis (Leguminosae) Callosobruchus chinensis Ulmus americana (Ulmaceae) Scolytus multistriatus (Doskotch et (Tebayashi et al.,1995) al., 1973) quercetin 3-O-(2´´,6´´-di-O-rhamnosyl)-galactoside, quercetin 3-O- quercetin 3-O-rutinoside (2´´,6´´-di-O-rhamnosyl)-glucoside, quercetin 3-O-glucosyl-(1 → commercial agent Schistoceruca americana (Bernays et al., 1991) 6)-galactoside, quercetin 3-O-rhamnosyl-(1 → 2)-galactoside, quercetin 3-O-rutinoside, [chlorogenic acid] quercetin 3-O-rutinoside, quercetin 3-O-galactoside, quercetin 3- commercial agents Manduca sexta (de Boer & Hanson, 1987) O-glucoside [ ] = non-flavonoid compounds. Asclepias curassavica (Asclepiadaceae) Danaus plexippus (Haribal & Renwick, 1996) quercetin 3-O-rutinoside* Brassica oleraceae (Cruciferae) Pieris rapae (Tabashnik, 1987) *Oviposition deterrent. [ ] = non-flavonoid compounds.

－ 28 － Iwashina, T.

plants of alligatorweed, Alternanthera phylloxeroides Nine having feeding deterrent activity (Amaranthaceae) as feeding stimulant of the chrysomelid against two pasture scarabs, Costelytra zealandica and beetle, Agasicles sp. nov. (Zielske et al., 1972). The Heteronychus arator larvae were isolated from the compound was identified as nepetin 7-O- α -L- of Lupinus angustifolius (Lane et al., 1987). They were rhamnoside. identified as (Fig. 4-31), (Fig. 4-32), The genera Prunus and Malus include important 2´-hydroxygenistein (Fig. 4-33), (Fig. 4-34), economic fruits such as peach, plum, almond, apricot and licoisoflavone A (Fig. 4-35), angustone A (Fig. 4-37), apple. The harmful insects feeding those fruits are also licoisoflavone B (Fig. 4-36), angustone B (Fig. 4-38), and induced by flavonoid stimulants. In apricot, Prunus angustone C (Fig. 4-41). Of these isoflavones, licoiso- armeniaca, six flavonoids, and each one chromone and flavone B, luteone, licoisoflavone A and wighteone showed coumarin were isolated from the bark infected by fruit tree not only feeding deterrent activity but also high antifungal bark beetle, Scolytus mediterraneus. Of their compounds, activity against two fungi, Colletrichum gloeosporioides three dihydro-flavonols, aromadendrin (= and Cladosporium cladosporioides as described later (Lane dihydrokaempferol, Fig. 3-7), taxifolin (= et al., 1987). Moreover, Lane et al. (1985) have proved dihydroquercetin, Fig. 2-5) and pinocembrin (Fig. 3-9) that other thirteen isoflavonoids act as feeding deterrents showed high activity as feeding stimulants of S. against Costelytra zealandica using the authentic mediterraneus, wheleas other compounds naringenin, flavonoids (Table 4). kaempferol, quercetin, 5,7-dihydroxy-2-methylchromone (3R)-(－)-Vestitol (Fig. 4-16) was isolated from Lotus and scopoletin exhibited low activity (Levy et al., 1974). pedunculatus as a isoflavonoid having feeding deterrent In case of apple, Malus spp., dihydrochalcone glycoside, activity against Costelytra zealandica (Russell et al., 1978). phloretin 2´´-O-glucoside (phloridzin) was reported as a The compound was also shown to have phytoalexin activity. feeding stimulant of Rhopalosiphum insertum and Aphis Other flavonoid classes have been reported to be feeding pomi (Klingauf, 1971). deterrents in the Leguminosae. Three flavanones, i.e., 5- A flavan 3-ol as one of the feeding stimulants of the hydroxyisoderricin, 7-methoxy-8-(3-methylbutadienyl)- smaller European elm bark beetle, Scolytus multistriatus, flavanone and 5-methoxyisoronchocarpin, were isolated was isolated from Ulmus americana (Ulmaceae). The from three Tephrosia species, T. villosa, T. purpurea and T. stimulant was identified as (+)-catechin 7-O-xyloside vogelii, respectively (Simmonds et al., 1990). Those (Doskotch et al., 1973). However, the flavonoid was compounds were proved to be feeding deterrents against inactive alone, but elicited feeding behavior when coexisted Spodoptera exempta and S. littoralis. In another Tephrosia with a wax, lupeyl cerotate (Doskotch et al., 1973). species, T. hildebrandtii, two flavan 4-ols, methyl- De Boer & Hanson (1987) investigated feeding hildgardtol A (Fig. 4-14) and methylhildgardtol B (Fig. 4- responses to quercetin 3-O-rutinoside () using larvae 15) act as deterrents against the same harmful insects of the tobacco hornworm, Manduca sexta. As the results, (Simmonds et al., 1990). Four chalcones, derricin (Fig. 4- rutin was a feeding stimulant of the hornworm. Its activity 11), lonchocarpin (Fig. 4-10), derricidin (Fig. 4-12) and is due to the glycosylated structure, since both the quercetin, isocordoin (Fig. 4-9) from Lonchocarpus neuroscapha and the sugar moieties, rutinose, glucose and are were shown to be deterrents with a flavanone, isoderricidin neural. Moreover, removal of the glucose part of quercetin (Fig. 4-8) against Spodoptera exempta and S. littoralis 3-O-rutinoside, as in quercetin 3-O-rhamnoside, results in (Simmonds et al., 1990). In another Lonchocarpus species, feeding deterrent activity. L. minimiflorus, five new flavanones lonchocarpols A - E Quercetin 3-O-rutinoside was also demonstrated to be (Fig. 4-2, 3, 5, 6 and 7) were isolated from the leaves a phagostimulant for the grasshopper, Schistocerca (Roussis et al., 1987). Three of them contain an unusual americana (Bernays et al., 1991). In this case, aglycone, prenyl cyclization. It was proved that all the flavanones quercetin was much less stimulating than quercetin 3-O- from this species escape attack of the leafcutter , Atta rutinoside, while sugar, rutinose alone was somewhat cephalotes (Roussis et al., 1987). deterrent. Though dihydrochalcone, phloretin 2´-O-glucoside (phloridzin) in apples is feeding stimulant against Aphis Feeding deterrents pomi and Rhapalosiphum insertum, the compound was deterrent against Acyrthosiphum pisum (Klingauf, 1971). Many flavonoids are used as feeding deterrents against harmful insects by some plants, together with terpenoids, also act as feeding deterrents. Two flavans, alkaloids, hydrocarbons and so on (Harborne, 1993). Some 4´-hydroxy-7-methoxyflavan (Fig. 4-29) and ( － )-7,3´- dihydroxy-4´-methoxy-8-methylflavan (Fig. 4-30) were flavonoid classes, e.g., flavonols, flavones, proantho- Lycoris radiata cyanidins, flavan 3-ols, flavanones, flavans and iso- isolated from the bulbs of red spider lily, flavonoids, are reported as feeding deterrents. Of these (Amaryllidaceae) with six alkaloids, lycorine, lycorenine, lycoricidinol, lycoricidine, demethylhomolycorine and flavonoids, isoflavonoids are mainly isolated from the et al., legume plants as derterrents, since these occurrence mostly hippeastrine (Numata 1983). These two flavans and centers on the Leguminosae (ca. 85%) (Iwashina, 2000). six alkaloids were considered as antifeedants for the larvae of the yellow buttefly, Eurema hecabe mandarina.

－29－ Flavonoid function and activity

Naturally occurring flavones, flavonols and dihydro- (Leguminosae) also utilize the proanthocyanidins as flavonols were also reported from some plant species as feeding deterrents. In P. aquilinum, procyanidins and feeding deterrents. Wheat and corn are important grain in cyanogenesis were deterrents against the phytophagous the world. Each one flavone feeding deterrents were locust, Schistocerca gregaria, and also sheep and deer isolated from the stems and leaves (wheat), and corn . (Cooper-Driver et al., 1977). In groundnut, procyanidin The deterrent from Triticum aestivum (Gramineae) was polymer in leaves was found to be deterrent against the identified as (Fig. 4-1) (Dreyer & Jones, 1981), and aphid, Aphis craccivora (Grayer et al., 1992). These one from Zea mays (Gramineae) as new flavone C- proanthocyanidins are not completely characterized. glycoside, luteolin 6-C-(6-deoxy-xylo-hexos-4-uloside)- Procyanidin was also isolated from aphid-resistant lines 2´´-O-rhamnoside (Elliger et al., 1980b). The former of sorghum, Sorghum bicolor (Gramineae) as feeding compound acts as feeding deterrent with unknown more deterrent against Schizaphis graminum, together with other polar phenols against two aphid species, Schizaphis compounds, P-hydroxybenzaldehyde, P-hydroxybenzoic graminum and Myzus persicae, and latter inhibits growth acid and dhurrin (Dreyer et al., 1981). Luteolin 7-O- and development of the corn earworm, Heliothis zea (Waiss glucoside was also detected, but it is inactive. et al., 1979). Beside the naturally occurring flavonoids, Dreyer & Flavonol deterrents were found from foetida Jones (1981) and Elliger et al. (1980a) showed that a (Passifloraceae) and cotton, Gossypium spp. (Malvaeae). number of authentic flavonoids act as feeding deterrents Ten flavonoids (two flavanones, two flavones and six against Schizaphis graminum and Myzus persicae, or flavonols) were isolated from the leaves resin of P. foetida. Heliothis zea. They include flavones, flavonols, Of these flavonoid aglycones, (kaempferol 7,4´- flavanones, dihydroflavonols, chalcones, dihydchalcones dimethyl ether, Fig. 4-28) is only chemical defense in P. and their O- or C-glycosides (Table 4). foetida against the phytophagous larvae, Dione juno (Echeverri et al., 1991). On the other hand, common Allelopathy O flavonols, quercetin, quercetin 3- -glucoside and quercetin The word “allelopathy” was defined by Molish (1973), 3-O-rutinoside were reported from cotton as deterrents using it in the widest sense to refer to ‘biochemical Pectinophora gossypiella against the pink bollworm, , interactions between all types of plant and including both Heliothis zea H. virescens and the tobacco budworm, with deleterious and advantageous interactions. In contrast, yellow polyphenolic pigment, gossypol (Shaver & Muller (1970) prefers to restrict the term allelopathy to Lukefahr, 1969). Apart from the results described above, higher plant - higher plant interactions. In this section, I Chan et al., (1978b) reported that quercetin in the leaves define allelopathy according to Muller. Biochemical Gossypium of spp. is growth inhibitor of the same noxious interactions between higher plants and microorganisms are insects, together with terpene aldehyde, cyclopropenoid described in next section (phytoalexins). Allelopathic plant fatty acids and condensed tannins. In tomato, Lycopersicon polyphenols have been reviewed by Inderjit (1996). esculentum (Solanaceae), it was reported that major The flavonoids as allelopathy were reported by some O phenolic compounds, quercetin 3- -rutinoside and also authors. They include chalcones, dihydrochalcones, chlorogenic acid inhibit early larvae growth of Heliothis dihydroflavonols, flavanones, flavonols and isoflavonoids. zea (Isman & Duffey, 1982). Chalcones, dihydrochalcones and flavanones were Fagus sylvatica In extracts of inner and outer bark of reported to be allelopathy by Star (1980). They are (Fagaceae), qualitative dependence of the phenolic contained in frond exudate of gymnogrammoid ferns, Cryptococcus compounds on infection with beech scale, Pityrogramma spp. and identified as 2´,6´-dihydroxy-4´- fagisuga feeding in the parenchyma tissue was observed methoxychalcone (Fig. 5-1), 2´,6´-dihydroxy-4´- (Dübeler et al., 1997). Of seven compounds isolated, three methoxydihydrochalcone (Fig. 5-4) and izalpinin (Fig. 5- O dihydroflavonol glycosides, (2R,3R)-(+)-taxifolin 3- - 7). These compounds were inhibitory to spore gemination O glucoside and 3- -xyloside, and (2S,3S)-(－)-taxifolin 3- and gametophyte development of Pityrogramma O-glucoside strongly infected with beech scale. They are calomeranos itself. However, some concentration Nectria also effective active against the bark cancer fungus, stimulated spore germination. coccinea et al (Dübeler ., 1997). The similar situation was investigeted in sunflower, Proanthocyanidins (= condensed tannins) are also used Helianthus annuus. A flavonol, two chalcones and two to plants as feeding deterrents against some insects, flavanones were isolated from the leaves and identified as Porthetria dispar, Euproctis chrysorrhoea, Operophtera tambulin, kukulcanin B (Fig. 5-3), and three new brumata etc. (Bernays, 1981). Feeny (1968) and Feeny & flavonoids, heliannones A - C (Fig. 5-2, 5 and 6). They Bostock (1968) reported that proanthocyanidins, (+)- inhibit shoot growth of Lycopersicon esculentum and catechin, (+)-gallocatechin (Fig. 4-20) and other vanillin- Hordeum vulgare seedlings. Moreover, two chalcones, positive compounds in the leaves of Quercus robur kukulcanin B and heliannone A, affected germination and (Fagaceae) appear in late May and inhibit winter moth radical length (Macías et al., 1997). Operophtera brumata larvae, attack. Fern, bracken Three flavonoids, i.e., hesperetin 7-O-rutinoside Pteridium aquilinum and groundnut, Arachys hypogaea

－ 30 － Iwashina, T.

Fig. 4. Chemical structures of flavonoids as feeding deterrents. 1 = tricin, 2 = lonchocarpol A, 3 = lonchocarpol B, 4 = isolonchocarpin, 5 = lonchocarpol C, 6 = lonchocarpol D, 7 = lonchocarpol E, 8 = isoderricidin, 9 = isocordoin, 10 = lonchocarpin, 11 = derricin, 12 = derricidin, 13 = 3-hydroxyisolonchocarpin, 14 = methylhildgardtol A, 15 = methylhildgardtol B, 16 = vestitol, 17 = eriodictyol, 18 = homoeriodictyol, 19 = myricetin, 20 = gallocatechin, 21 = , 22 = , 23 = , 24 = , 25 = hypoleatin 3´,4´- dimethyl ether, 26 = , 27 = robinetin, 28 = ermanin, 29 = 4´- hydroxy-7-methoxyflavan, 30 = 7,3´-dihydroxy-4´-methoxy-8- methylflavan, 31 = genistein, 32 = wighteone, 33 = 2´-hydroxygenistein, 34 = luteone, 35 = licoisoflavone A, 36 = licoisoflavone B, 37 = angustone A, 38 = angustone B, 39 = phaseollinisoflavan, 40 = phaseollin, 41 = angustone C, 42 = , 43 = claussequinone, 44 = 2´-hydroxy- , 45 = (－)-maackiain, 46 = (－)-, 47 = , 48 = kievitone, 49 = phaseollidin, 50 = maysin and 51 = maysin 3´-methyl ether. Quercetin, luteolin, chalcononaringenin, naringenin, isoorientin and vitexin (see, Fig. 1), taxifolin and catechin (see, Fig. 2), and phloretin and morin (see, Fig. 3).

－31－ Flavonoid function and activity

Table 4 Flavonoids as feeding deterrents Flavonoids [demethylhomolycorine], [hippeastrine], [lycorine], [lycorenine] Lycoris radiata (Amaryllidaceae) Eurea hecobe mandarina Plants Insects (References) (Numata et al., 1983) proanthocyanidin lonchocarpol A, lonchocarpol B, lonchocarpol C, lonchocarpol D, Gossypium hirsutum (Malvaceae) Heliothis verescens (Chan et al., lonchocarpol E 1978a) Lonchocarpus minimiflorus (Leguminosae) Atta cephalotes genistein, wighteone, 2´-hydroxygenistein, luteone, licoisoflavone A, (Roussis et al., 1987) angustone A, licoisoflavone B, angustone B, angustone C phloretin 2´-O-glucoside Lupinus angustifolius (Leguminosae) Costelytra zealandica, Malus spp. (Rosaceae) Acyrthosiphum pisum (Klingauf, 1971) Heteronychus arator (Lane et al., 1987) quercetin 3-O-rhamnoside procyanidin, [P-hydroxybenzaldehyde], [P-hydroxybenzoic acid], commercial agent Manduce sexta (de Boer & Hanson, 1987) [dhurrin] tricin, [unknown more polar phenols] Sorghum bicolor (Gramineae) Schizaphis graminum (Dreyer et Triticum aestivum (Gramineae) Schizaphis graminum (Dreyer & al., 1981) Jones, 1981) quercetin 3-O-rutinoside, [coumarin] isoderricidin, derricidin, isocordoin, derricin, lonchocarpin commercial agents Pieris rapae (Tabashnik, 1987) Lonchocarpus neuroscapha (Leguminosae) Spodoptera exempta, S. ( )-phaseollinisoflavan, ( )-phaseollin, ( )-rotenone, (+)-2´- littoralis et al － － － (Simmonds ., 1990) methoxyphaseollinisoflavan, ( － )-7-methoxyphaseollin, isolonchocarpin, 3-hydroxyisolonchocarpin licoisoflavone B, ( －)-phaseollidin, ( － )-claussequinone, ( － )- Lonchocarpus eriocaulinalis (Leguminosae) Spodoptera exempta, S. vestitol, 2´-hydroxyformononetin, 2´-hydroxygenistein, ( )- littoralis et al － (Simmonds ., 1990) maackiain, ( －)-medicarpin, (+)-pisatin, kievitone, luteone methylhildgardtol A, methylhildgardtol B commercial agents Costelytra zealandica (Lane et al., 1985) Tephrosia hilbrandtii (Leguminosae) Spodoptera exempta, quercetin 3-O-rutinoside, [chlorogenic acid] S. littoralis (Simmonds et al., 1990) Lycopersicon esculentum (Solanaceae) Heliothis zea (Isman & 5-hydroxyisoderricin Duffey, 1982) Tephrosia villosa (Leguminosae) Spodoptera exempta, S. littoralis catechin (Simmonds et al., 1990) Rosa sp. (Rosaceae) Macrosiphum rosae (Peng & Miles, 1988) 7-methoxy-8-(3-methylbutadienyl)-flavanone Tephrosia purpurea (Leguminosae) Spodoptera exempta, [ ] = non-flavonoid compounds. S. littoralis (Simmonds et al., 1990) 5-methoxyisoronchocarpin Tephrosia vogelii (Leguminosae) Spodoptera exempta, S. littoralis (Simmonds et al., 1990) (3R)-( － )-vestitol Lotus pedunculatus (Leguminosae) Costelytra zealandica (Russell et al., 1978) 3,2´,6´-trihydroxy-4-methoxy-4´-carboxymethyldihydrochalcone, 3,2´,6´-trihydroxy-4-methoxy-4´-sulfopropyldihydrochalcone, 3,2´,4´,6´-tetrahydroxy-4-methoxydihydrochalcone-4´-O- glucoside, luteolin, quercetin 3-O-rutinoside, myricetin 3-O- rhamnoside commercial agents Schizaphis graminum (Dreyer & Jones, 1981) phloretin, phloretin 2´-O-glucoside, 3,2´,4´,6´-tetrahydroxy-4- methoxydihydrochalcone 4´-O-neohesperidoside, chalcononaringenin 4´-O-neohesperidoside, naringenin, eriodictyol, homoeriodictyol, taxifolin, vitexin, quercetin, quercetin 3-O-rhamnoside, morin commercial agents Schizaphis graminum, Myzus persicae (Dreyer & Jones, 1981) proanthocyanidins, (+)-catechin, (+)-gallocatechin Quercus robur (Fagaceae) Operophtera brumata (Feeny, 1968; Feeny & Bostock, 1968) procyanidins, [cyanogenesis] Pteridium aquilinum (Pteridaceae) Schistocerca gregaris (Cooper- Driver et al., 1977) procyanidin polymer Arachys hypogaea (Leguminosae) Aphis craccivora (Grayer et al., 1992) fisetin, 5,7,2´,3´-tetrahydroxyflavone, luteolin, eriodictyol, orobol, isoorientin, maysin, maysin 3´-methyl ether, scutellarein, isoscutellarein, 3´,4´-dimethyl ether, tricetin, robinetin, quercetin, taxifolin, quercetin 3-O-rhamnoside, taxifolin 3-O- rhamnoside, quercetin 3-O-rutinoside, D-catechin, myricetin Fig. 5. Chemical structures of flavonoids as allelopathy. commercial agents Heliothis zea (Elliger et al., 1980a) 1 = 2´,6´-dihydroxy-4´-methoxychalcone, 2 = heliannone A, 3 = luteolin 6-C-(6-deoxy-xylo-hexos-4-uloside)-2´´-O-rhamnoside kukulkanin B, 4 = 2´,6´-dihydroxy-4´-methoxydihydrochalcone, 5 = Zea mays (Gramineae) Heliothis zea (Waiss et al., 1979; Elliger et heliannone B, 6 = heliannone C, 7 = izalpinin, 8 = , 9 = al., 1980b) and 10 = formononetin. Kaempferol, quercetin and quercetin 3- ermanin Passiflora foetida (Passifloraceae) Dione juno (Echeverri et al., methyl ether (see, Fig. 1), taxifolin and hesperetin (see, Fig. 2), and 1991) genistein and ( －)- maackiain (see, Fig. 4). (2R,3R)-(+)-taxifolin 3-O-glucoside, (2R,3R)-(+)-taxifolin 3-O- xyloside, (2S, 3S)-( －)-taxifolin 3-O-glucoside Fagus sylvatica (Fagaceae) Cryptococcus fagisuga (with bark cancer fungus) (Dübeler et al., 1997) quercetin, quercetin 3-O-glucoside, quercetin 3-O-rutinoside, cotton condensed tannin, [gossypol], [heliocide I], [heliocide II], [hemigossypolone], [sterclic acid], [malvalic acid] Gossypium spp. (Malvaceae) Pectinophora gossypiella, Hiliothis zea, H. virescens (Shaver & Lukefahr, 1969; Chan et al., 1978b) 4´-hydroxy-7-methoxyflavan, ( － )-7,3´-dihydroxy-4´-methoxy-8- methylflavan, [lycoricidinol], [lycoricidine],

－ 32 － Iwashina, T.

Table 5 Flavonoids as allelopathy & Ootani, 1986). As the results obtained, all of them Flavonoids inhibited growth of Arabidopsis thaliana seedlings (Parvez Source plants Inhibited plants (References) et al., 2002). It was also observed that quercetin 3-methyl 2´,6´-dihydroxy-4´-methoxychalcone, izalpinin, 2´,6´-dihydroxy-4´- ether and its glycosides are stronger inhibitors than methoxydihydrochalcone quercetin and its glycosides. Moreover, quercetin 3-methyl Pityrogramma spp. (Parkeriaceae) Pityrogramma calomeranos (Parkeriaceae) (Star, 1980) ether and its glycosides showed inhibiting activity on heliannone A, heliannone B, heliannone C, kukulkanin B, tambulin conidial germination of a fungus, Neurospora crassa Helianthus annuus (Compositae) Lycopersicon esculentum (Solanaceae), Hordeum vulgare (Gramineae) (Macías et al., 1997) (Parvez et al., 2002). taxifolin 3-O-arabinoside, hesperetin 7-O-rutinoside, formononetin 7- Isoflavonoid allelopathy was reported from red clover, O-glucoside Pluchea lanceolata (Compositae), Brassica juncea, Raphanus Trifolium pratense. T. pratense has been well known to sativus (Criciferae), Lycopersicon esculentum (Inderjit & exhibit homogeneous allelopathy, so called ‘clover Dakshini, 1991, 1994) kaempferol, quercetin, myricetin sickness’. Tamura and coworkers found that the leaves Erica australis (Ericaceae) Trifolium pratense, Phleum pratense and stems extracts show considerable inhibitory action on (Gramineae) (Carballeira, 1980) the seed germination of the same plant. Ten isoflavonoids quercetin, quercetin 3-O-arabinofuranoside, quercetin 3-O-galactoside, quercetin 3-O-glucoside, quercetin 3-methyl ether, quercetin 3- and their glycosides were isolated and identified as methyl ether 4´-O-glucoside, quercetin 3-methyl ether 7-O- biochanin A (Fig. 5-8) and its 7-O-glucoside, 7-O- glucoside, quercetin 3-O-rhamnoside Astrophytum, Parodia, Neochilenia, Notocactus spp. (Cactaceae) glucoside-5-malonate and 5-malonate, daidzein (Fig. 5-9) Arabidopsis thaliana (Cruciferae) (Parvez et al., 2002) and formononetin (Fig. 5-10) and their 7-O-glucosides, biochanin A, biochanin A 7-O-glucoside, biochanin A 7-O-glucoside-5- malonate, biochanin A 5-malonate, daidzein, daidzein 7-O- genistein, and ( － )-maackiain 3-O-glucoside (Tamura et glucoside, formononetin, genistein, ( －)-maackiain 3-O-glucoside al., 1967, 1969; Chang et al., 1969). They inhibit not only Trifolium pratense (Leguminosae) Trifolium spp. (Tamura et al., seed germination and seedling growth of T. pratense itself 1967,1969; Chang et al., 1969) 2,4-dihydroxy-6,4´-dimethoxychalcone, bifloridin, 7-hydroxy-4´- but also those of related species, T. repense and T. hydrium. methoxyflavan Imperata cylindrica (Gramineae) grows abundantly in Pancratium biflorum (Amaryllidaceae) Imperata cylindrica (Gramineae) (Ghosal et al., 1986) the vicinity of the bulbed plant, Pancratium biflorum (Amaryllidaceae). The main roots of the grass are often found to penetrate the bulbs of P. biflorum. A rare incidence of phanerogamic parasitism by I. cylindrica on P. biflorum (flavanone), taxifolin 3-O-arabinoside (dihydroflavonol) and the concomitant chemical changes from the and formononetin 7-O-glucoside () were isolated hypersensitive responses in the host plants were reported. with phloroglucinol, simple phenol, chlorogenic acid and These compounds were identified as 2,4-dihydroxy-6,4´- methylated coumarin from the roots of Pluchea lanceolata dimethoxychalcone, bifloridin and 7-hydroxy-4´- (Compositae) and soils associated with this weed as methoxyflavan, and five alkaloids, hippadine, lycorine, allelopathy (Inderjit & Dakshini, 1991, 1992, 1994). These ungeremine, 4,5-dehydroanhydrolycorine and compounds inhibit seed germination and seedling growth pancrassidine (Ghosal et al., 1986). of radish, mustard and tomato. Flavonol allelopathy have been reported by Carballeira Phytoalexins (1980) and more recently Parvez et al. (2002). Fifteen The plants produce certain chemical substances at the phenolic compounds were isolated from the flowers, leaves, time of infection of microorganisms. Their compounds stems or roots of Erica australis and the associated soil ward off the disease organisms from the plants and are (Carballeira, 1980). All of them were contained in roots called as “phytoalexin”. Many kinds of chemicals e.g., and characterized as three flavonols (kaempferol, quercetin simple phenolics, alkaloids, , coumarins, and myricetin), nine organic acids (P-hydroxybenzoic acid, polyacetylenes, terpenoids and so on, were reported as protocatechic acid, vanillic acid, syringic acid, gentisic acid, phytoalexins (Harborne, 1993). Flavonoid compounds caffeic acid, P-coumaric acid, ferulic acid and sinapic acid), were also reported as phytoalexins from various plant two coumarins (aesculetin and scopoletin) and a simple species. Moreover, some flavonoids are known to be phenol (orcinol). These compounds were strong inhibitors inducers of nitrogen fixing bacteria, Rhizobium, to growth and germination of Trifolium pratense and Azorhizobium and Bradyrhizobium, to certain flowering Phleum pratense (Carballeira, 1980). plants, especially those of the Leguminosae (e.g., Zaat et It was shown by Parvez et al. (2002) that quercetin and al., 1989; Firmin et al., 1986; Bassam et al., 1988). its 3-O-glycosides and methoxyl derivatives are allelopathic Majority of the flavonoid phytoalexins were mainly isolated substances. Quercetin and its 3-O-glucoside, 3-O- from underground parts, roots, rhizomes, hypocotyls, or galactoside, 3-O-rhamnoside and 3-O-arabinofuranoside, seeds. The functions of the flavonoids have been and quercetin 3-methyl ether (Fig. 1-17) and its 7-O- described by Rao (1990) and the flavonoids as phytoalexins glucoside and 4´-O-glucoside, which were tested in this were mentioned. Ingham (1972) have reviewed about experiment, have been isolated from the flowers of phytoalexin and other natural products including flavonoids cactaceous species, Astrophytum, Notocactus, Parodia and as factors in plant disease resistance. Neochilenia spp. (Iwashina et al., 1984a, 1988; Iwashina

－33－ Flavonoid function and activity

In this section, flavonoids as phytoalexins and inducers characterized. These compounds induced germination of of nitrogen fixing bacteria are described. Rhizobium leguminosarum viovar. viciae or trifolii, or R. Anthocyanins commonly affect as plant pigments in meliloti. Zaat et al. (1989) also reported that many flowers, autumn leaves or fruits, and are important flavonoids including flavanones, dihydroflavonols, pollinator attractants described in former section. On the flavones, flavonols, isoflavones and dihydrochalcone other hand, a few anthocyanins act as phytoalexins. Two obtained from various plant sources induce R. 3-deoxyanthocyanidins, apigeninidin (Fig. 6-1) and leguminosarum viovar. viciae or trifolii, or R. meliloti. luteolinidin (Fig. 6-2) were isolated from the leaves of Three flavan phytoalexins were isolated from the bulbs sorghum (Sorghum bicolor) as phytoalexins (Nicholson et of daffodil, Narcissus pseudonarcissus inoculated with al., 1987, 1988; Snyder et al., 1991). They inhibit Botrytis cinerea (Coxon et al., 1980). They were identified germination of the fungi, Helminthosporium maydis and as 7-hydroxyflavan (Fig. 6-11), cassiaflavan (Fig. 6-9) and Colletotrichum graminicola. A 3-deoxyanthocyanin 7,4´-dihydroxy-8-methylflavan (Fig. 6-10). O’Neill & glycoside was also found as phytoalexin from inoculated Mansfield (1982) tested many authentic hydroxyflavans leave tissue of sorghum and identified as apigeninidin 5- and other flavonoids in addition to three daffodil flavans, O-(5´´-caffeoylarabinoside) (Hipskind et al., 1990). Since and showed that some flavonoids act as phytoalexins apigeninidin and luteolinidin were not treated by hot against Botrytis cinerea and Cladosporium herbarum. inorganic acid when they were extracted and isolated, they It was also reported that naturally occurring flavanones may be natural compounds but not artifacts. act as phytoalexins. Betagarin (5,2´-dihydroxy-6,7- Aurone phytoalexin was found from a cactus species. methylenedioxyflavanone, Fig. 6-12) was found as A red pigment was observed to accumulate in phytoalexin against Cercospora beticola which is Cephalocereus senilis, in whole plants and in culture responsible for sugarbeet leaf spot disease, together with a following inoculation with various microorganisms (Pare isoflavone, betavulgarin (2´-hydroxy-5-methoxy-6,7- et al., 1991). The aurone was isolated from chitin-treated methylenedioxyisoflavone, Fig. 6-47) from Beta vulgaris liquid suspension cultures of this cactus, and identified as (Chenopodiaceae) (Geigert et al., 1973; Johnson et al., new compound, 6-hydroxy-4,5-methylenedioxyaurone 1976; Martin, 1977). Another flavanone phytoalexin was (cephalocerone, Fig. 6-3) (Pare et al., 1991). The results isolated from the infected roots of sugarbeet, with each of the antimicrobial assay showed that cephalocerone is two dihydroflavonols and isoflavones, and a flavone active against Escherichia coli and Pseudomonas (Takahashi et al., 1987). They were identifed as new aeruginosa. Naturally occurring aurone possessing methylenedioxylated flavonoids, 3,5-dihydroxy-6,7- biological activity was reported for the first time. methylenedioxyflavanone (Fig. 6-14), 5,2´-dihydroxy-6,7- A chalcone was reported as phytoalexin. It was isolated methylenedioxyisoflavone and 5-hydroxy-6,7- with each one flavone and isoflavonoid from alfalfa methylenedioxyflavone, and inhibit germination of (Medicago sativa) callus and identified as β - Rhizoctonia solani with known compounds, betagarin, hydroxychalcone, 4,2´,4´, β -tetrahydroxychalcone betavulgarin and 3,5-dihydroxy-6,7-methylenedioxy- (Kobayashi et al., 1988). The β-hydroxychalcone shows flavanone. antifungal activity against Pyricularia oryzae. Though Six flavanones were isolated from the bark of Prunus accompanied flavone, 7,4´-dihydroxyflavone (Fig. 6-22) cerasus (Rosaceae) with each three flavones and also exhibits antifungal activity, but isoflavonoid, 6- isoflavones. Of these flavanones, naringenin and hydroxy-7,4´-dimethoxyisoflavone is inactive. sakuranetin (Fig. 6-18) were strongly toxic at higher On the other hand, another chalcone from alfalfa concentrations against a fungus, Cystospora persoonii, and induced nitrogen fixing bacteria. 2´- pinostrobin, naringenin 7-O-glucoside and sakuranetin 5- methyl ether (Fig. 6-4) from the seeds and roots was known O-glucoside were moderately, but dihydrowogonin 7-O- to be strong inducer of Rhizobium meliloti (Hartwig et al., glucoside was not toxic (Geibel, 1995). Other flavonoids, 1989; 1990b; Maxwell et al., 1989). Moreover, the author (Fig. 6-21), tectochrysin (Fig. 6-33) and its 5-O- reported that other flavonoids, luteolin, 7,4´- glucoside, genistein, and (Fig. 6-65) and its 5-O- dihydroxyflavone, (Fig. 6-13) and glucoside showed more or less toxicity against C. persoonii. (Fig. 6-20) strongly induce nitrogen fixing bacteria. It is Five flavanone phytoalexins were isolated from the noteworthy that 7,4´-dihydroxyflavone inhibits germination xylem of Pinus taeda and P. strobus (Yamada & Ito, 1993). of Pyricularia oryzae and Cladosporium herbarium These compounds were identified as (Fig. 6- (Kobayashi et al., 1988), but induce Rhizobium meliloti 16), pinocembrin and pinostrobin (Fig. 6-17), and (Maxwell et al., 1989). immobilize nematode, Bursaphelenchus xylophilus. A very Other flavonoids also act as inducers of Rhizobium rare flavanone, sigmoidin B 3´-methyl ether (Fig. 6-19) bacteria. Zaat et al. (1989) isolated seven flavonoid was isolated from the stem bark of Erythrina berteroana inducers from the root exudate of Vicia sativa. Six of them (Leguminosae) and shown to be antifungal against are flavanones and dihydroflavonols, and two were Cladosporium cucumerinum (Tomás-Barberán et al., identified as taxifolin 4´-methyl ether (Fig. 6-7) and 7,3´- 1988b). dihydroxy-4´-methoxyflavanone, but other ones were not Polymethylated flavones and flavonols were reported

－ 34 － Iwashina, T.

Fig. 6. Chemical structures of flavonoids as phytoalexins. 1 = apigeninidin, 2 = luteolinidin, 3 = cephalocerone, 4 = isoliquiritigenin 2´-methyl ether, 5 = dihydroisorhamnetin, 6 = fustin, 7 = taxifolin 4´-methyl ether, 8 = broussin, 9 = cassiaflavan, 10 = 7,4´-dihydroxy-8-methylflavan, 11 = 7-hydroxyflavan, 12 = betagarin, 13 = liquiritigenin, 14 = 3,5-dihydroxy- 6,7-methylenedioxyflavanone, 15 = isosakuranetin, 16 = pinobanksin, 17 = pinostrobin, 18 = sakuranetin, 19 = sigmoidin B 3´-methyl ether, 20 = chrysoeriol, 21 = chrysin, 22 = 7,4´-dihydroxyflavone, 23 = 5,4´-dihydroxy-6,7,8,3´-tetramethoxyflavone, 24 = xanthomicrol, 25 = 5,7-dimethoxyflavone, 26 = , 27 =flavone, 28 = geraldone, 29 = isopratol, 30 = demethylnobiletin, 31 = , 32 = , 33 = tectochrysin, 34 = 5,6,7,8- tetramethoxyflavone, 35 = trimethyl ether, 36 = , 37 = , 38 = chrysosplenol D, 39 = isokaempferide, 40 = 3,5,6,7,8- pentamethoxyflavone, 41 = quercetin 3,3´-dimethyl ether, 42 = resokaempferol, 43 = 3,5,6,7-tetramethoxyflavone, 44 = herbacetin 3,8-dimethyl ether, 45 = trimethyl ether, 46 = , 47 = betavulgarin, 48 = coumesterol, 49 = dalbergioidin, 50 = demethylvestitol, 51 = dihydrowighteone, 52 = erybraedin B, 53 = erybraedin C, 54 = I, 55 = glyceollin II, 56 = glyceollin III, 57 = homopterocarpin, 58 = erybraedin A, 59 = erythrabyssin II and 60 = medicarpin. Naringenin, apigenin, luteolin, kaempferol, quercetin and isoorientin (see, Fig. 1), taxifolin, catechin, hesperetin and isorhamnetin (see, Fig. 2), aromadendrin, pinocembrin and morin (see, Fig. 3), eriodyctiol, homoeriodyctiol, fisetin, myricetin, genistein, 2´-hydroxygenistein, kievitone, licoisoflavone A, licoisoflavone B, luteone, maackiain, medicarpin, phaseollin, phaseollinisoflavone, pisatin, vestitol, wighteone and phaseollidin (see, Fig. 4), and biochanin A, daidzein and formononetin (see, Fig. 5). (continue)

－35－ Flavonoid function and activity

cassiaflavan Narcissus pseudonarcissus (Amaryllidaceae), commercial agent Botrytis cinerea (Coxon et al., 1980; O’Neill & Mansfield, 1982), Cladosporium herbarum (O’Neill & Mansfield, 1982) 7,4´-dihydoxy-8-methylflavan Narcissus pseudonarcissus, commercial agent Botrytis cinerea (Coxon et al., 1980; O’Neill & Mansfield, 1982), Cladosporium herbarum (O’Neill & Mansfield, 1982) flavan commercial agent Botrytis cinerea, Cladosporium herbarum (O’Neill & Mansfield, 1982) 7-hydroxyflavan Narcissus pseudonarcissus, commercial agent Botrytis cinerea (Coxon et al., 1980; O’Neill & Mansfield, 1982), Cladosporium herbarum (O’Neill & Mansfield, 1982) Flavan 3-ol (+)-catechin commercial agent Aspergillus spp. (Weidenbörner et al., 1990b) Flavanone betagarin Beta vulgaris Fig. 6. Chemical structures of flavonoids as phytoalexins (continue). Cercospora beticola (Johnson et al., 1976; Martin, 1977; Geigert et 61 = isoneorautenol, 62 = lupinalbin A, 63 = lupiwighteone, 64 = phaseol, al., 1973), Rhizoctonia solani (Takahashi et al., 1987) 65 = prunetin, 66 = sativan, 67 = lupalbigenin and 68 = tuberosin. liquiritigenin Medicago sativa, commercial agent Rhizobium meliloti* (Hartwig et al., 1989; Maxwell et al., 1989), Rhizobium spp.* (Bassam et al., 1988) 5,7-dihydroxy-6-methoxyflavanone Beta vulgaris Rhizoctonia solani (Takahashi et al., 1987) 7,3´-dihydroxy-4´-methoxyflavanone Vicia sativa Table 6 Flavonoids as phytoalexins, and inducers of nitrogen fixing Rhizobium leguminosarum* (Zaat et al., 1989) bacteria eriodictyol commercial agent Rhizobium leguminosarum* (Firmin et al., 1986; Zaat et al., 1989), Classes Rhizobium meliloti* (Peters & Long, 1988) Flavonoids Sources eriodictyol 7-O-glucoside commercial agent Inhibited microorganisms (References) Rhizobium leguminosarum* (Zaat et al., 1989) flavanone commercial agent Anthocyanin Verticillium albo-atrum (Picman et al., 1995), Aspergillus spp. apigeninidin Sorghum bicolor (Gramineae) (Weidenbörner et al., 1990b) Colletotrichum graminicola, Helminthosporium maydis (Nicholson et hesperetin commercial agent al., 1987, 1988; Snyder et al., 1991) Verticillium albo-atrum (Picman et al., 1995), Aspergillus spp. apigeninidin 5-O-(5´´-caffeoylarabinoside) Sorghum bicolor (Weidenbörner et al., 1990b), Rhizobium leguminosarum* (Firmin Colletotrichum graminicola, Helminthosporium maydis (Hipskind et et al., 1986; Zaat et al., 1989) al., 1990) hesperetin 7-O-rutinoside commercial agent luteolinidin Sorghum bicolor Verticillium albo-atrum (Picman et al., 1995) Colletotrichum graminicola, Helminthosporium maydis (Nicholson et homoeriodictyol commercial agent al., 1987, 1988; Snyder et al., 1991) Rhizobium leguminosarum* (Zaat et al., 1989) isosakuranetin commercial agent Aurone Rhizobium leguminosarum* (Zaat et al., 1989) cephalocerone Cephalocereus senilis (Cactaceae) naringenin Prunus cerasus (Rosaceae), Vigna angularis Escherichia coli, Pseudomonas aeruginosa (Pare et al., 1991) (Leguminosae), commercial agent Verticillium albo-atrum (Picman et al., 1995), Aspergillus spp. Chalcone (Weidenbörner et al., 1990b), Cystospora persoonii (Geibel, 1995), isoliquiritigenin 2´-methyl ether Medicago sativa (Leguminosae) Rhizobium leguminosarum* (Firmin et al., 1986; Zaat et al., 1989), Rhizobium meliloti* (Hartwig et al., 1989, 1990b; Maxwell et al., Cephalosporium gregatum (Abe et al., 1987), Rhizobium spp.* 1989) (Bassam et al., 1988) 4,2´,4´, β -tetrahydroxychalcone Medicago sativa naringenin 7-O-glucoside Prunus cerasus, commercial agent Pyricularia oryzae, Cladosporium herbarum (Kobayashi et al., Cystospora persoonii (Geibel, 1995), Rhizobium leguminosarum* 1988) (Zaat et al., 1989) naringenin 7-O-neohesperidoside Acacia farnesiana (Leguminosae), Dihydroflavonol commercial agent aromadendrin commercial agent Verticillium albo-atrum (Picman et al., 1995), Aspergillus carneus Rhizobium leguminosarum* (Zaat et al., 1989) etc. (El-Gammal & Mansour, 1986) dihydroisorhamnetin commercial agent pinobanksin Pinus strobus, P. taeda (Pinaceae) Rhizobium leguminosarum* (Zaat et al., 1989) Bursaphelenchus xylophilus (Yamada & Ito, 1993) 3,5-dihydroxy-6,7-methylenedioxyflavanone pinocembrin Pinus strobus, P. taeda, commercial agent Beta vulgaris (Chenopodiaceae) Rhizobium leguminosarum* (Zaat et al., 1989), Bursaphelenchus Rhizobium solani (Takahashi et al., 1987) xylophilus (Yamada & Ito, 1993) fustin commercial agent pinostrobin Prunus cerasus Rhizobium leguminosarum* (Zaat et al., 1989) Cystospora persoonii (Geibel, 1995) taxifolin commercial agent sakuranetin Prunus cerasus Rhizobium leguminosarum* (Zaat et al., 1989) Cystospora persoonii (Geibel, 1995) (2R,3R)-(+)-taxifolin 3-O-glucoside Fagus sylvatica (Fagaceae) sakuranetin 5-O-glucoside Prunus cerasus Nectria coccinea (with beech scale) (Dübeler et al., 1997) Cystospora persoonii (Geibel, 1995) (2R,3R)-(+)-taxifolin 3-O-xyloside Fagus sylvatica sigmoidin B 3´-methyl ether Erythrina berteroana (Leguminosae) Nectria coccinea (with beech scale) (Dübeler et al., 1997) Cladosporum cucumerinum (Tomás-Barberán et al., 1988b) (2S,3S)-( － )-taxifolin 3-O-glucoside Fagus sylvatica Nectria coccinea (with beech scale) (Dübeler et al., 1997) Flavone taxifolin 4´-methyl ether Vicia sativa (Leguminosae) apigenin commercial agent Rhizobium leguminosarum* (Zaat et al., 1989) Verticillium albo-atrum (Picman et al., 1995), Rhizobium leguminosarum* (Firmin et al., 1986; Zaat et al., 1989), Rhizo- Flavan bium meliloti* (Peters & Long, 1988), Rhizobium spp.* (Bassam et broussin Broussonetia papyrifera (Moraceae) al., 1988) Bipolaris leersiae (Takasugi et al., 1980) (continue)

－ 36 － Iwashina, T. Table 6 (continue)

apigenin 7-O-glucoside commercial agent etc. (El-Gammal & Mansour, 1986), Rhizobium spp.* (Bassam et Rhizobium leguminosarum* (Firmin et al., 1986; Zaat et al., 1989) al., 1988) apigenin 7-O-neohesperidoside commercial agent kaempferol 3-O-robinobioside-7-O-rhamnoside Andropogon Verticillium albo-atrum (Picman et al., 1995) scoparium (Gramineae) chrysoeriol Medicago sativa Nitrosomonas sp., Nitrobacter sp. (Rice & Pancholy, 1974) Rhizobium meliloti* (Hartwig et al., 1990b) morin commercial agent chrysin Prunus cerasus, commercial agent Verticillium albo-atrum (Picman et al., 1995) Verticillium albo-atrum (Picman et al., 1995), Cystospora persoonii myricetin Geranium mascatense (Geraniaceae), Sorghastrum (Geibel, 1995) nutans (Gramineae), commercial agent 7,4´-dihydroxyflavone Verticillium albo-atrum (Picman et al., 1995), Aspergillus carneus Trifolium repens, Medicago sativa, commercial agent etc. (El-Gammal & Mansour, 1986), Nitrosomonas sp., Nitrobacter Rhizobium trifolii* (Redmond et al., 1986; Djordjevic et al., 1987), sp. (Rice & Pancholy, 1974) Rhizobium meliloti* (Hartwig et al., 1989; Maxwell et al., 1989), 3,5,6,7,8-pentamethoxyflavone Helichrysum nitens Pyricularia oryzae, Cladosporium herbarum (Kobayashi et al., Cladosporium cucumerinum (Tomás-Barberán et al., 1988a, 1988b) 1988), Rhizobium spp* (Bassam et al., 1988) quercetin Pinus ponderosa (Pinaceae), Geranium dissectum 7,8-dihydroxyflavone commercial agent (Geraniaceae) Rhizobium leguminosarum*(Zaat et al., 1989) Nitrosomonas sp., Nitrobacter sp. (Lodhi & Killingbeck, 1980), 5,4´-dihydroxy-6,7,8,3´-tetramethoxyflavone Citrus spp. Aspergillus carneus etc. (El-Gammal & Mansour, 1986) Deuterophoma tracheiphila (Piattelli & Impellizzeri, 1971) quercetin 3,3´-dimethyl ether Psiadia trinervia xanthomicrol Citrus spp. Bacillus cereus (Wang et al., 1989) Deuterophoma tracheiphila (Pinkas et al., 1968) quercetin 3-O-glucoside commercial agent 5,7-dimethoxyflavone Helichrysum nitens (Compositae) Verticillium albo-atrum (Picman et al., 1995) Cladosporum cucumerinum (Tomás-Barberán et al., 1988a, 1988b) quercetin 4´-O-glucoside Haplopappus ciliatus (Compositae) diosmetin 7-O-rutinoside commercial agent Nitrosomonas sp., Nitrobacter sp. (Rice & Pancholy, 1974) Verticillium albo-atrum (Picman et al., 1995) quercetin 3-methyl ether 7-O-diglucoside-4´-O-glucoside flavone commercial agent Andropogon scoparius, A. gerardi (Gramineae) Verticillium albo-atrum (Picman et al., 1995), Aspergillus spp. Nitrosomonas sp., Nitrobacter sp. (Rice & Pancholy, 1974) (Weidenbörner et al., 1990b) quercetin 3-O-rutinoside Eucalyptus camaldulensis (Myrtaceae) geraldone Trifolium repens Aspergillus carneus etc. (El-Gammal & Mansour, 1986) Rhizobium trifolii* (Redmond et al., 1986) resokaempferol Panicum virgatum (Gramineae) 7-hydroxyflavone commercial agent Nitrosomonas sp., Nitrobacter sp. (Rice & Pancholy, 1974) Aspergillus spp. (Weidenbörner et al., 1990b), Rhizobium 3,5,6,7-tetramethoxyflavone Helichrysum nitens leguminosarum* (Zaat et al., 1989) Cladosporium cucumerinum (Tomás-Barberán et al., 1988a, 1988b) isopratol Trifolium repens herbacetin 3,8-dimethyl ether Psiadia trinervia Rhizobium trifolii* (Redmond et al., 1986) Cladosporium cucumerinum, Bacillus cereus (Wang et al., 1989) 5-hydroxy-6,7-methylenedioxyflavone Beta vulgaris galangin trimethyl ether Helichrysum nitens Rhizoctonia solani (Takahashi et al., 1987) Cladosporium cucumerinum (Tomás-Barberán et al., 1988a, 1988b) demethylnobiletin Citrus spp. Deuterophoma tracheiphia (Piattelli & Impellizzeri, 1971) C-Glycosylflavone luteolin Medicago sativa, commercial agent isoorientin Ambrosia psilostachya (Compositae) Verticillium albo-atrum (Picman et al., 1995), Rhizobium meliloti* Nitrosomonas sp., Nitrobacter sp. (Rice & Pancholy, 1974) (Peters et al., 1986; Peters & Long, 1988; Caetano-Anollés et al., 1988; Hartwig et al., 1989, 1990a), Rhizobium leguminosarum* Isoflavonoid (Firmin et al., 1986; Zaat et al., 1989), Rhizobium spp.* (Bassam acetoxydimethoxypterocarpan Swartzia madagascariensis et al., 1988) (Leguminosae) luteolin 7-O-glucoside commercial agent Momilinia fructicola (Perrin & Cruickshank, 1969) Verticillium albo-atrum (Picman et al., 1995), Rhizobium acetoxymethoxypterocarpan Swartzia madagascariensis leguminosarum* (Zaat et al., 1989) Momilinia fructicola (Perrin & Cruickshank, 1969) nobiletin Citrus reticulata, Citrus spp. acetoxymethylenedioxypterocarpan Swartzia madagascariensis Deuterophoma tracheiphila (Ben-Aziz, 1967; Piattelli & Momilinia fructicola (Perrin & Cruickshank, 1969) Impellizzeri, 1971), Fusarium moniliforme, Sclerotium rolfsii alpinumisoflavone Lupinus albus (Leguminosae) (Pinkas et al., 1968) Cladosporium herbarum (Ingham et al., 1983) tangeretin Citrus spp. betavulgarin Beta vulgaris Deuterophoma tracheiphila (Piattelli & Impellizzeri, 1971), Cerospora beticola (Johnson et al., 1976; Martin, 1977; Geigert et Fusarium moniliforme, Sclerotium rolfsii (Pinkas et al., 1968) al., 1973), Rhizoctonia solani (Takahashi et al., 1987) tectochrysin Prunus cerasus biochanin A commercial agent Cystospora persoonii (Geibel, 1995) Rhizoctonia solani, Sclerotium rolfsii (Weidenbörner et al., 1990a), 5,6,7,8-tetramethoxyflavone Helichrysum nitens Rhizobium spp.* (Bassam et al., 1988) Cladosporum cucumerinum (Tomás-Barberán et al., 1988a, 1988b) biochanin A-isoflavanone commercial agent 7,3´,4´-trihydroxyflavone commercial agent Rhizoctonia solani, Sclerotium rolfsii (Weidenbörner et al., 1990a) Rhizobium leguminosarum* (Firmin et al., 1986) coumesterol commercial agent baicalein trimethyl ether Helichrysum nitens Verticillium albo-atrum (Picman et al., 1995), Rhizobium spp.* Cladosporum cucumerinum (Tomás-Barberán et al., 1988a, 1988b) (Bassam et al., 1988) daidzein Glycine max (Leguminosae), commercial agent Flavonol Verticillium albo-atrum (Picman et al., 1995), Bradyrhizobium ayanin Psiadia trinervia (Compositae) japonicum* (Kosslak et al., 1987), Rhizobium spp.* (Bassam et Cladosporium cucumerinum (Wang et al., 1989) al., 1988) casticin Psiadia trinervia dalbergioidin Vigna angularis Cladosporium cucumerinum (Wang et al., 1989) Cephalosporium gregatum (Abe et al., 1987) chrysosplenol D Psiadia trinervia 6a,11a-dehydroglyceollin commercial agent Cladosporium cucumerinum, Bacillus cereus (Wang et al., 1989) Fusarium solani, Aphanomyces euteiches (VanEtten, 1976) fisetin commercial agent 6a,11a-dehydrotuberosin commercial agent Verticillium albo-atrum (Picman et al., 1995) Fusarium solani, Aphanomyces euteiches (VanEtten, 1976) flavonol commercial agent demethylvestitol Vigna angularis Aspergillus spp. (Weidenbörner et al., 1990b) Cephalosporium gregatum (Abe et al., 1987) isokaempferide Psiadia trinervia dihydrowighteone Vigna angularis Bacillus cereus (Wang et al., 1989) Cephalosporium gregatum (Abe et al., 1987) isorhamnetin commercial agent 7,2´-dihydroxyisoflavan commercial agent Verticillium albo-atrum (Picman et al., 1995) Botrytis cinerea, Cladosporium herbarum (O’Neill & Mansfield, kaempferol Tribulus pentandrus (Zygophyllaceae), commercial 1982) agent 5,7-dihydroxy-4´-methoxyisoflavan commercial agent Verticillium albo-atrum (Picman et al., 1995), Aspergillus carneus Rhizoctonia solani, Sclerotium rolfsii (Weidenbörner et al., 1990a)

(continue)

－37－ Flavonoid function and activity Table 6 (continue)

6,7-dihydroxy-3´-methoxyisoflavan commercial agent Colletrichum gloeosporioides, Cladosporium cladosporioides (Lane Aspergillus spp. (Weidenbörner et al., 1989) et al., 1987) 6,7-dihydroxy-4´-methoxyisoflavan commercial agent licoisoflavone B Lupinus angustifolius, L. albus Rhizoctonia solani, Sclerotium rolfsii (Weidenbörner et al., 1990a) Cladosporium herbarum (Harborne et al., 1976; Ingham et al., 1983), 7,8-dihydroxy-4´-methoxyisoflavan commercial agent Colletrichum gloeosporioides, Cladosporium cladosporioides (Lane Aspergillus spp. (Weidenbörner et al., 1989) et al., 1987) 6,4´-dihydroxy-7-methoxyisoflavan commercial agent lupalbigenin Lupinus albus Rhizoctonia solani, Sclerotium rolfsii (Weidenbörner et al., 1990a) Cladosporium herbarum (Ingham et al., 1983) 7,4´-dihydroxy-6-methoxyisoflavan commercial agent lupinalbin A Vigna angularis Rhizoctonia solani, Sclerotium rolfsii (Weidenbörner et al., 1990a) Cephalosporium gregatum (Abe et al., 1987) 5,2´-dihydroxy-6,7-methylenedioxyisoflavone Beta vulgaris lupinisoflavone Lupinus albus, L. luteus Rhizoctonia solani (Takahashi et al., 1987) Cladosporium herbarum (Harborne et al., 1976; Ingham et al., 1983) erybraedin A Erythrina mildbraedii lupiwighteone Vigna angularis Staphylococcus aureus, Mycobacterium smegmatis (Mitscher et al., Cephalosporium gregatum (Abe et al., 1987) 1988) luteone Lupinus angustifolius, Lupinus spp. erybraedin B Erythrina mildbraedii Cladosporium herbarum (Harborne et al., 1976; Ingham et al., 1983), Staphylococcus aureus, Mycobacterium smegmatis (Mitscher et al., Colletrichum gloeosporioides, Cladosporium cladosporioides (Lane 1988) et al., 1987) erybraedin C Erythrina mildbraedii maackiain Trigonella spp. (Leguminosae) Staphylococcus aureus, Mycobacterium smegmatis (Mitscher et al., Helminthosporium carbonum (Ingham & Harborne, 1976) 1988) (+)-maackiain Sophora japonica (Leguminosae) erythrabyssin-II Erythrina mildbraedii Momilinia fructicola (Perrin & Cruickshank, 1969) Staphylococcus aureus, Mycobacterium smegmatis (Mitscher et al., ( － )-maackiain Trifolium pratense 1988) Momilinia fructicola (Bredenberg & Hietala, 1961a, 1961b; Perrin & formononetin Medicago arabica (Leguminosae), Trifolium repens, Cruickshank, 1969) commercial agent ( － )-maackiain 3-O-glucoside Trifolium pratense Fusarium solani, Aphanomyces euteiches (VanEtten, 1976), Helminthosporium carbonum (Ingham & Harborne, 1976) Aspergillus carneus etc, (El-Gammal & Mansour, 1986), medicarpin Trigonella spp. (Leguminosae) Rhizobium trifolii (Djordjevic et al., 1987), Rhizobium spp.* Helminthosporium carbonum (Ingham & Harborne, 1976) (Bassam et al., 1988) (+)-medicarpin commercial agent genistein Glycine max, Lupinus spp., commercial agent Fusarium solani, Aphanomyces euteiches (VanEtten, 1976) Verticillium albo-atrum (Picman et al., 1995), Cladosporium ( ± )-medicarpin commercial agent herbarum (Ingham et al., 1983), Bradyrhizobium japonicum* Fusarium solani, Aphanomyces euteiches (VanEtten, 1976) (Kosslak et al., 1987), Rhizoctonia solani, Sclerotium rolfsii ( － )-3-hydroxy-9-methoxypterocarpan commercial agent (Weidenbörner et al., 1990a), Rhizobium spp.* (Bassam et al., Fusarium solani, Aphanomyces euteiches (VanEtten, 1976) 1988) (+)-2´-methoxyphaseollin-isoflavan commercial agent genistein 7-O-glucoside commercial agent Fusarium solani, Aphanomyces euteiches (VanEtten, 1976) Verticillium albo-atrum (Picman et al., 1995) phaseol Vigna angularis genistein-isoflavanone commercial agent Cephalosporium gregatum (Abe et al., 1987) Rhizoctonia solani, Sclerotium rolfsii (Weidenbörner et al., 1990a) phaseollidin Leguminosae sp. glyceollin Glycine max Corynebacterium fascians, Bacillus subtilis, Micrococcus luteus Phytophthora megasperma (Stössel, 1982) (Gnanamanickam & Smith, 1980), Botrytis cinerea (Fraile et al., Glycine max 1982) Meloidogyne incognita (Kaplan et al., 1980a, 1980b) phaseollin Phaseollus vulgaris glyceollin II Glycine max Corynebacterium fascians, Bacillus subtilis, Micrococcus luteus Meloidogyne incognita (Kaplan et al., 1980a, 1980b) (Gnanamanickam & Smith, 1980), Fusarium spp. etc. (VanEtten, glyceollin III Glycine max 1973), Botrytis cinerea (Fraile et al., 1982) Meloidogyne incognita (Kaplan et al., 1980a, 1980b) ( － )-phaseollin Phaseollus vulgaris, commercial agent ( －)-glyceollin commercial agent Fusarium solani, Aphanomyces euteiches (VanEtten, 1976), Fusarium solani, Aphanomyces euteiches (VanEtten, 1976) Momilinia fructicola (Perrin & Cruickshank, 1969) ( － )-homopterocarpin Pterocarpus sp. phaseollin-isoflavan Leguminosae sp. Momilinia fructicola (Perrin & Cruickshank, 1969) Corynebacterium fascians, Bacillus subtilis, Micrococcus luteus 6-hydroxy-7,4´-dimethoxyisoflavan commercial agent (Gnanamanickam & Smith, 1980), Botrytis cinerea (Fraile et al., Rhizoctonia solani, Sclerotium rolfsii (Weidenbörner et al., 1990a) 1982) 7-hydroxy-6,4´-dimethoxyisoflavan commercial agent ( －)-phaseollin-isoflavan commercial agent Rhizoctonia solani, Sclerotium rolfsii (Weidenbörner et al., 1990a) Fusarium solani, Aphanomyces euteiches (VanEtten, 1976) 2´-hydroxy-7,4´-dimethoxyisoflavan commercial agent pisatin Pisum sativum Botrytis cinerea, Cladosporium herbarum (O’Neill & Mansfield, Fusarium spp. etc. (VanEtten, 1973) 1982) (+)-pisatin Pisum sativum, commercial agent 2´-hydroxygenistein Lupinus spp., Vigna angularis Fusarium solani, Aphanomyces euteiches (VanEtten, 1976), Cladosporium herbarum (Ingham et al., 1983), Cephalosporium Monilinia fructicola (Perrin & Cruickshank, 1969), many gregatum (Abe et al., 1987) microorganisms (Cruickshank, 1962) 7-hydroxyisoflavan commercial agent prunetin Prunus cerasus Botrytis cinerea, Cladosporium herbarum (O’Neill & Mansfield, Cytospora persoonii (Geibel, 1995) 1982) sativan Trigonella spp. 2´-hydroxyisoflavan commercial agent Helminthosporium carbonum (Ingham & Harborne, 1976) Botrytis cinerea, Cladosporium herbarum (O’Neill & Mansfield, ( －)-sativan commercial agent 1982) Fusarium solani, Aphanomyces euteiches (VanEtten, 1976) 7-hydroxy-2´-methoxyisoflavan commercial agent 6,7,4´-trimethoxyisoflavan commercial agent Botrytis cinerea, Cladosporium herbarum (O’Neill & Mansfield, Rhizoctonia solani, Sclerotium rolfsii (Weidenbörner et al., 1990a) 1982) (+)-tuberosin commercial agent 3-hydroxy-8,9-methylenedioxy-6a,11a-dehydropterocarpan Fusarium solani, Aphanomyces euteiches (VanEtten, 1976) commercial agent vestitol Trigonella spp. Fusarium solani, Aphanomyces euteiches (VanEtten, 1976) Helminthosporium carbonum (Ingham & Harborne, 1976) isoneorautenol Erythrina mildbraedii ( － )-vestitol commercial agent Staphylococcus aureus, Mycobacterium smegmatis (Mitscher et Fusarium solani, Aphanomyces euteiches (VanEtten, 1976) al., 1988) (3R)-vestitol Vigna angularis kieviton Leguminosae sp. Cephalosporium gregatum (Abe et al., 1987) Corynebacterium fascians, Bacillus subtilis, Micrococcus luteus wighteone Lupinus angustifolius, Lupinus spp. (Gnanamanickam & Smith, 1980), Botrytis cinerea (Fraile et al., Cladosporium herbarum (Harborne et al., 1976; Ingham et al., 1983), 1982) Colletrichum gloeosporioides, Cladosporium cladosporioides (Lane licoisoflavone A Lupinus angustifolius et al., 1987) *Nitrogen fixing bacteria induced by flavonoids.

－ 38 － Iwashina, T.

as phytoalexins against certain microorganisms. Six Isoflavonoid phytoalexins were obtained from the roots compounds were isolated from the aerial parts of and/or leaves of Lupinus albus and related species and Helichrysum nitens (Compositae), and identified as fully shown to be inhibitors against Cladosporium herbarum methylated flavones and flavonols, 5,7-dimethoxyflavone (Harborne et al., 1976; Ingham et al., 1983). (Fig. 6-25), baicalein trimethyl ether (Fig. 6-35), galangin Nine antifungal stress flavonoids were isolated from trimethyl ether (Fig. 6-45), 5,6,7,8-tetramethoxyflavone the roots of adzuki bean, Vigna angularis, which had been (Fig. 6-34), 3,5,6,7-tetramethoxyflavone (Fig. 6-43), treated with pathogenic fungus, Cephalosporium gregatum 3,5,6,7,8-pentamethoxyflavone (Fig. 6-40) (Tomás- (Abe et al., 1987). The fungus causes brown stem rot Barberán et al., 1988a, 1988b). They inhibit growth of disease on the host plants. These compounds were eight Cladosporium cucumerinum, but two 5-hydroxylated isoflavonoids, dihydrowighteone (Fig. 6-51), dalbergioidin flavones, alnetin (5-hydroxy-6,7,8-trimethoxyflavone) and (Fig. 6-49), phaseol (Fig. 6-64), 2´-hydroxygenistein, 5-hydroxy-6,7-dimethoxyflavone which were accompanied lupiwighteone (Fig. 6-63), lupinalbin A (Fig. 6-62), (3R)- with methylated flavonoids were inactive. Other fully ( － )-vestitol and demethylvestitol (Fig. 6-50), and methylated flavones, nobiletin (Fig. 6-31) and tangeretin flavanone, naringenin. (Fig. 6-32) were isolated from the leaves of Citrus spp. It was reported by Kaplan et al. (1980a, 1980b) that together with 5,4´-dihydroxy-6,7,8,3´-tetramethoxyflavone (Fig. 6-54, 55 and 56), which are phytoalexins (Fig. 6-23), xanthomicrol (Fig. 6-24) and demethylnobiletin against Phytophthora megasperma (Stössel, 1982), in the (Fig. 6-30) (Piattelli & Impellizzeri, 1981; Pinkas et al., roots of Glycine max, were also accumulated by infection 1968). They were shown to display antifungal activity of the root-knot nematode, Meloidogyne incognita to against Deuterophoma tracheiphila which is responsible roots. for the highly destructive citrus disease known as “Mal- Four , erythrabyssin-II (Fig. 6-59), secco”. In addition, nobiletin and tangeretin also inhibited erybraedins A - C (Fig. 6-58, 52 and 53) and isoneorautenol growth of other pathogenic fungi, Fusalium moniliforme, (Fig. 6-61) from Nigerian legume species, Erythrina Sclerotium rolfsii and Verticillium albo-atrum (Pinkas et mildbraedii were shown to be antimicrobial against al., 1968). Staphylococcus aureus and Mycobacterium smegmatis Antimicrobial flavonols were reported from Psiadia (Mitscher et al., 1988). However, accompanied alkaloids trinervia (Compositae) which are used in African traditional fractions were inactive. medicine (Wang et al., 1989). Thirteen 3-methylated In addition to naturally occurring flavonoids, VanEtten flavonols were isolated from the leaves. Four of them, (1976), O’Neill & Mansfield (1982), Weidenbörner et al. ayanin (Fig. 6-36), casticin (Fig. 6-37), chrysosplenol D (1990a) have reported that many flavonoids, especially (Fig. 6-38) and herbacetin 3,8-dimethyl ether (Fig. 6-44) isoflavonoids inhibit growth of many microorganisms. were resposible for the antifungal activity against Cladosporium cucumerinum. Moreover, chrysosplenol D, As described in this paper, many flavonoids have isokaempferide (Fig. 6-39), quercetin 3,3´-dimethyl ether various biological activity such as pollinator attractants, (Fig. 6-41) and herbacetin 3,8-dimethyl ether displayed oviposition stimulants, feeding stimulants and deterrents, antibacterial activity against Bacillus cereus, but remained allelopathy or phytoalexins. However, the activity is ones were inactive. surveyed to a small number of naturally occurring The inhibition of nitrification by climax ecosystem was flavonoids, in spite of ca. 5,000 kinds of flavonoids have observed. Though hydrolyzable and condensed tannins, been found in plant kingdom. It is hoped that the function and tannin derivatives are important inhibitors of and activity of the flavonoids to plants and other organisms nitrification (Rice & Pancholy, 1973), flavonols and other are further elucidated. phenolic compounds also inhibit nitrification by bacteria, Nitrobacter sp. and Nitrosomonas sp. (Rice & Pancholy, Acknowledgements 1974). Phenolic inhibitors were myricetin, quercetin 4´- The author expresses his sincere gratitude to Dr. Kaori O-glucoside, quercetin 3-methyl ether 4´-O-glucoside-7- Tomita-Yokotani of University of Tsukuba, who gave him O O O -diglucoside, kaempferol 3- -robinobioside-7- - a chance to write this review. rhamnoside (miss-described as kaempferol 3-O-rabinoside- 7-O-rhamnoside by original paper?) and C- glycosylflavone, isoorientin, from the various plant species. References Caffeic acid, chlorogenic acid, neochlorogenic acid and Abe, N., Sato, H. and Sakamura, S. (1987) Antifungal stress ferulic acid were also shown to be inhibitors. compounds from adzuki bean, Vigna angularis, treated with Cephalosporium gregatum type B. Agric. Biol. Chem., 51, 349- Isoflavonoids may retain most phytoalexin substances 353. among the flavonoid classes, and majority of them occur Bassam, B.J., Djordjevic, M.A., Redmond, J.W., Batley, M. and in the Leguminosae. Perrin & Cruickshank (1969) reported Rolfe, B.G. (1988) Identification of a nodD-dependent locus many isoflavonoid phytoalexins from various legume in the Rhizobium strain NGR234 activated by phenolic factors species. These compounds belong to and secreted by soybean and other legumes. Mol. Plant-Microbe inhibited growth of fungus, Monilinia fructicola. Interact., 1, 161-168. Ben-Aziz, A. (1967) Nobiletin is main fungistat in tangerines

－39－ Flavonoid function and activity

resistant to Mal Secco. Science, 155, 1026-1027. flavonoids and related phenolics towards Schizaphis graminum Bernays, E.A. (1981) Plant tannins and insect behaviors: an and Myzus persicae: aphid feeding deterrents in wheat. appraisal. Ecol. Entomol., 6, 353-360. Phytochemistry, 20, 2489-2493. Bernays, E.A., Howard, J.J., Champagne, D. and Estesen, B.J. Dreyer, D.L., Reese, J.C. and Jones, K.C. (1981) Aphid feeding (1991) Rutin: a phagostimulant for the polyphagous acridid deterrents in sorghum. Bioassey, isolation, and Schistocerca americana. Entomol. Exp. Appl., 60, 19-28. characterization. J. Chem. Ecol., 7, 273-284. Besson, E., Dellamonica, G., Chopin, J., Markham, K.R., Kim, Dübeler, A., Voltmer, G., Gora, V., Lunderstädt, J. and Zeeck, A. M., Koh, H.-S. and Fukami, H. (1985) C-Glycosylflavones (1997) Phenols from Fagus sylvatica and their role in defence from Oryza sativa. Phytochemistry, 24, 1061-1064. against Cryptococcus fagisuga. Phytochemistry, 45, 51-57. Bloom, M. and Vickery, R.K. (1973) Pattern partitioning of floral Echeverri, F., Cardona, G., Torres, F., Pelaez, C., Quiñones, W. flavonoids in the Mimulus luteus complex. Phytochemistry, and Renteria, E. (1991) Ermanin: an insect deterrent flavonoid 12, 165-167. from Passiflora foetida resin. Phytochemistry, 30, 153-155. Bohm, B.A. (1975) Chalcones, aurones and dihydrochalcones. El-Gammal, A.A. and Mansour, R.M.A. (1986) Antimicrobial In Harborne, J.B., Mabry, T.J. and Mabry, H. (eds.) The activities of some flavonoid compounds. Zentralbl. Mikrobiol., flavonoids. Chapman and Hall, London. pp. 442-504. 141, 561-565. Bredenberg, J.B. and Hietala, P.K. (1961a) Investigation of the Elliger, C.A., Chan, B.C. and Waiss Jr., A.C. (1980a) Flavonoids structure of trifolirhizin, an antifungal compound from as larval growth inhibitors. Naturwissenschaften, 67, 358-360. Trifolium pratense L. Acta Chem. Scand., 15, 696-699. Elliger, C.A., Chan, B.C., Waiss Jr., A.C., Lundin, R.E. and Bredenberg, J.B. and Hietala, P.K. (1961b) Confirmation of the Haddon, W.F. (1980b) C-Glycosylflavones from Zea mays that structure of trifolirhizin. Acta. Chem. Scand., 15, 936-937. inhibit insect development. Phytochemistry, 19, 293-297. Caetano-Anollés, G., Crist-Estes, D.K. and Bauer, W.D. (1988) Feeny, P.P. (1968) Effect of oak leaf tannins on larval growth of Chemotaxis of Rhizobium meliloti to the plant flavone luteolin the winter moth Operophtera brumata. J. Insect Physiol. 14, requires functional nodulation genes. J. Bacteriol., 170, 3164- 805-817. 3169. Feeny, P.P. and Bostock, H. (1968) Seasonal changes in the tannin Carballeira, A. (1980) Phenolic inhibitors in Erica australis L. content of oak leaves. Phytochemistry, 7, 871-880. and in associated soil. J. Chem. Ecol., 6, 593-596. Feeny, P., Sachdev, K., Rosenberry, L. and Carter, M. (1988) Chang, C.-F., Suzuki, A., Kumai, S. and Tamura, S. (1969) Luteolin 7-O-(6´´-O-malonyl)- β -D-glucoside and trans- Chemical studies on “clover sickness” part II. Biological chlorogenic acid: oviposition stimulants for the black functions of isoflavonoids and their related compounds. Agric. swallowtail butterfly. Phytochemistry, 27, 3439-3448. Biol. Chem., 33, 398-408. Firmin, J.L., Wilson, K.E., Rossen, L. and Johnston, A.W.B. Chan, B.G., Waiss Jr., A.C. and Lukefahr, M. (1978a) Condensed (1986) Flavonoid activation of nodulation genes in Rhizobium tannin, an antibiotic chemical from Gossypium hirsutum. J. reversed by other compounds present in plants. Nature, 324, Insect Physiol., 24, 113-118. 90-92. Chan, B.G., Waiss Jr., A.C., Binder, R.G. and Elliger, C.A. (1978b) Fraile, A., García-Arenal, F., García-Serrano, J.J. and Sagasta, Inhibition of Lepidopterous larval growth by cotton E.M. (1982) Toxicity of phaseollin, phaseollidin, phaseollin- constituents. Entomol. Exp. Appl., 24, 94-100. isoflavan and kievitone to Botrytis cinerea. Phytopath. Z., 105, Cody, V., Middleton Jr., E. and Harborne, J.B. (1986) Plant 161-169. flavonoids in biology and medicine. Biochemical, Francis, F.J. and Harborne, J.B. (1966) Anthocyanins and flavonol pharmacological, and structure-activity relationships. Alan R. glycosides of Magnolia flowers. Proc. Amer. Soc. Hort. Sci., Liss, New York. 89, 657-665. Cody, V., Middleton Jr., E., Harborne, J.B. and Beretz, A. (1988) Geibel, M. (1995) Sensitivity of the fungus Cytospora persoonii Plant flavonoids in biology and medicine II. Biochemical, to the flavonoids of Prunus cerasus. Phytochemistry, 38, 599- cellular, and medicinal properties. Alan R. Liss, New York. 601. Cooper-Driver, G., Finch, S., Swain, T. and Bernays, E. (1977) Geigert, J., Stermitz, F.R., Johnson, G., Maag, D.D. and Johnson, Seasonal variation in secondary plant compounds in relation D.K. (1973) Two phytoalexins from sugarbeet (Beta vulgaris) to the palatability of Pteridium aquilinum. Biochem. Syst. leaves. Tetrahedron, 29, 2703-2706. Ecol., 5, 177-183. Geissman, T.A. (1962) The chemistry of flavonoid compounds. Coxon, D.T., O’Neill, T.M., Mansfield, J.W. and Porter, A.E.A. Pergamon Press, Oxford. (1980) Identification of three hydroxyflavan phytoalexins from Ghosal, S., Kumar, Y., Chakrabarti, D.K., Lal, J. and Singh, S.K. daffodil bulbs. Phytochemistry, 19, 889-891. (1986) Parasitism of Imperata cylindrica on Pancratium Cruickshank, I.A.M. (1962) Studies on phytoalexins. IV. The biflorum and the concomitant chemical changes in the host antimicrobial spectrum of pisatin. Aust. J. Biol. Sci., 15, 147- species. Phytochemistry, 25, 1097-1102. 159. Gnanamanickam, S.S. and Smith, D.A. (1980) Selective toxicity de Boer, G. and Hanson, F.E. (1987) Feeding responses to of isoflavonoid phytoalexins to gram-positive bacteria. solanaceous allelochemicals by larvae of the tobacco Phytopathology, 70, 894-896. hornworm, Manduca sexta. Entomol. Exp. Appl. 45, 123-131. Grayer, R.J., Kimmins, F.M., Padgham, D.E., Harborne, J.B. and Dement, P.H. and Raven, P.H. (1974) Pigments responsible for Rao, D.V.R. (1992) Condensed tannin levels and resistance ultraviolet patterns in flowers of Oenothera (Onagraceae). of groundnuts (Arachis hypogaea) against Aphis craccivora. Nature, 252, 705-706. Phytochemistry, 31, 3795-3800. Djordjevic, M.A., Redmond, J.W., Bathey, M. and Rolfe, B.G. Hamamura, Y., Hayashiya, K., Naito, K.-I, Matsuura, K. and (1987) Clover secrete specific phenolic compounds which Nishida, J. (1962) Food selection by silkworm larvae. Nature, either stimulate or repress nod gene expression in Rhizobium 194, 754-755. trifolii. EMBO J., 6, 1173-1179. Harborne, J.B., Mabry, T.J. and Mabry, H. (1975) The flavonoids. Doskotch, R.W., Mikhail, A.A. and Chatterji, S.K. (1973) Chapman and Hall, London. Structure of the water-soluble feeding stimulant from Scolytus Harborne, J.B., Ingham, J.L., King, L. and Payne, M. (1976) The multistriatus: a revision. Phytochemistry, 12, 1153-1155. isopentenyl isoflavone luteone as a pre-infectional antifungal Dreyer, D.L. and Jones, K.C. (1981) Feeding deterrency of agent in the genus Lupinus. Phytochemistry, 15, 1485-1487.

－ 40 － Iwashina, T.

Harborne, J.B. and Smith, D.M. (1978) Anthochlors and other Inderjit and Dakshini, K.M.M. (1992) Formononetin 7-O- flavonoids as honey guides in the Compositae. Biochem. Syst. glucoside (), an additional growth inhibitor in soils Ecol., 6, 287-291. associated with the weed, Pluchea lanceolata (DC.) C.B. Harborne, J.B. (1981) Two methyl ethers as ultraviolet Clarke (Asteraceae). J. Chem. Ecol., 18, 713-718. patterning guides in the flowers of Coronilla valentina. Inderjit and Dakshini, K.M.M. (1994) Allelopathic potential of Phytochemistry, 20, 1117-1119. the phenolics from the roots of Pluchea lanceolata. Physiol. Harborne, J.B. and Mabry, T.J. (1982) The flavonoids: advances Plant., 92, 571-576. in research. Chapman and Hall, London. Inderjit (1996) Plant phenolics in allelopathy. Bot. Rev., 62, 186- Harborne, J.B. and Boardley, M. (1983) Trisubstituted flavonol 202. glycosides in Coronilla emerus flowers. Phytochemistry, 22, Ingham, J.L. (1972) Phytoalexins and other natural products as 622-625. factors in plant disease resistance. Bot. Rev., 38, 343-424. Harborne, J.B. and Nash, R.J. (1984) Flavonoid pigments Ingham, J.L. and Harborne, J.B. (1976) Phytoalexin induction as responsible for ultraviolet patterning in petals of the genus a new dynamic approach to the study of systematic Potentilla. Biochem. Syst. Ecol., 12, 315-318. relationships among higher plants. Nature, 260, 241-243. Harborne, J.B. (1988) The flavonoids: advances in research since Ingham, J.L., Tahara, S. and Harborne, J.B. (1983) Fungitoxic 1980. Chapman and Hall, London. isoflavones from Lupinus albus and other Lupinus species. Z. Harborne, J.B. (1993) Introduction to ecological biochemistry. Naturforsch., 38c, 194-200. Fourth edition. Academic Press, London. Ishikura, N. (1980) Anthocyanins in iris flowers. Experientia, Harborne, J.B. (1994) The flavonoids: advances in research since 36, 656-657. 1986. Chapman and Hall, London. Isman, M.B. and Duffey, S.S. (1982) Toxicity of tomato phenolic Harborne, J.B. and Baxter, H. (1999) The handbook of natural compounds to the fruitworm, Heliothis zea. Entomol. Exp. flavonoids Vol. 1 and 2. John Wiley & Sons, Chichester. Appl., 31, 370-376. Haribal, M. and Renwick, J.A.A. (1996) Oviposition stimulants Iwashina, T., Ootani, S. and Hayashi, K. (1984a) Neochilenin, a for the monarch butterfly: flavonol glycosides from Asclepias new glycoside of 3-O-methylquercetin, and other flavonols curassavica. Phytochemistry, 41, 139-144. in the of Neochilenia, Neoporteria and Parodia species Hartwig, U.A., Maxwell, C.A., Joseph, C.M. and Phillips, D.A. (Cactaceae). Bot. Mag. , 97, 23-30. (1989) Interactions among flavonoid nod gene inducers Iwashina, T., Ootani, S. and Hayashi, K. (1984b) Pigment released from alfalfa seeds and roots. Plant Physiol., 91, 1138- components in the flower of Strongylodon macrobotrys, and 1142. spectrophotometric analyses of fresh petal and intact cells. Hartwig, U.A., Maxwell, C.A., Joseph, C.M. and Phillips, D.A. Res. Inst. Evolut. Biol. Sci. Rep., 2, 67-74. (1990a) Chrysoeriol and luteolin released from alfalfa seeds Iwashina, T., Ootani, S. and Kondo, N. (1985) Flower colors and induce nod genes in Rhizobium meliloti. Plant Physiol., 92, their betalain constituents in Cereoideae species. Res. Inst. 116-122. Evolut. Biol. Sci. Rep., 2, 95-118. Hartwig, U.A., Maxwell, C.A., Joseph, C.M. and Phillips, D.A. Iwashina, T. and Ootani, S. (1986) Distribution of flavonol (1990b) Effects of alfalfa nod gene-inducing flavonoids on glycosides and their sugar-free forms in subfamily Cereoideae. nodABC transcription in Rhizobium meliloti strains containing Ann. Tsukuba Bot. Gard., 4, 25-42. different nodD genes. J. Bacteriol., 172, 2769-2773. Iwashina, T., Amano, M., Mizuno, S. and Ootani, S. (1986) Hayashi, K., Ootani, S., Sato, K., Tuyama, T. and Ishikura, N. Flavonoid and quinonoid pigments in the perianths of Aloe (1978) Chemotaxonomical studies on Japanese irises in species: identification and inter- and intra-specific variation. relation to the flavonoids in flowers. Res. Inst. Evolut. Biol. Res. Inst. Evolut. Biol. Sci. Rep., 3, 116-131. Sci. Rep., 1, 1-16. Iwashina, T. and Ootani, S. (1987) Characterization of C- Hayashi, K., Ootani, S. and Iwashina, T. (1980) Paperchromato- glycosylflavones and anthocyanins in several species of graphic analysis and crystallization of pigment components Caryophyllaceae. Ann. Tsukuba Bot. Gard., 6,19-30. of Iris rossii. Res. Inst. Evolut. Biol. Sci. Rep., 1, 17-26. Iwashina, T., Ootani, S. and Hayashi, K. (1988) On the pigmented Hayashi, K., Ootani, S. and Iwashina, T. (1989) Comparative spherical bodies and crystals in tepals of cactaceous species analysis of the flavonoid and related compounds occurring in in reference to the nature of betalains or flavonols. Bot. Mag. three varieties of Iris setosa in the flora of Japan. Res. Inst. Tokyo, 101, 175-184. Evolut. Biol. Sci. Rep., 6, 30-60. Iwashina, T. and Ootani, S. (1990) Three flavonol allosides from Hipskind, J.D., Hanau, R., Leite, B. and Nicholson, R.L. (1990) Glaucidium palmatum. Phytochemistry, 29, 3639-3641. Phytoalexin accumulation in sorghum: identification of an Iwashina, T. and Ootani, S. (1996) Flavonoids in the flowers of apigeninidin acyl ester. Physiol. Mol. Plant Pathol., 36, 381- Iris laevigata (Iridaceae). Res. Inst. Evolut. Biol. Sci. Rep., 8, 396. 41-48. Hirose, Y., Hayashi, S. and Kawagishi, E. (1962) Studies on the Iwashina, T., Kamenosono, K. and Yabuya, T. (1996) Isolation valuable utilization of plant products. V. A new flavonoid and identification of flavonoid and related compounds as co- occurring in the flowers of Iris tectorum Maxim. 1. - as a pigments from the flowers of Iris ensata. J. Jap. Bot., 71, 281- preliminary -. Kumamoto Pharm. Bull., 5, 324-326. 287. Honda, K. (1986) Flavanone glycosides as oviposition stimulants Iwashina, T. and Ootani, S. (1998) Flavonoids of the genus Iris; in a papilionid butterfly, Papilio protenor. J. Chem. Ecol., 12, structures, distribution and function (review). Ann. Tsukuba 1999-2010. Bot. Gard., 17, 147-183. Honda, K. (1990) Identification of host-plant chemicals Iwashina, T. (2000) The structure and distribution of the flavonoids stimulating oviposition by swallowtail butterfly, Papilio in plants. J. Plant Res., 113, 287-299. protenor. J. Chem. Ecol., 16, 325-337. Iwashina, T., Konta, F. and Kitajima, J. (2001) Anthocyanins and Inderjit and Dakshini, K.M.M. (1991) Hesperetin 7-rutinoside flavonols of Chimonanthus praecox (Calycanthaceae) as (hesperidin) and taxifolin 3-arabinoside as germination and flower pigments. J. Jap. Bot., 76, 166-172. growth inhibitors in soils associated with the weed, Pluchea Johnson, G., Maag, D.D., Johnson, D.K. and Thomas, R.D. (1976) lanceolata (DC.) C.B. Clarke (Asteraceae). J. Chem. Ecol., The possible role of phytoalexins in the resistance of sugarbeet 17, 1585-1591.

－41－ Flavonoid function and activity

(Beta vulgaris) to Cercospora beticola. Physiol. Plant Pathol., Markham, K.R. (1982) Techniques of flavonoid identification. 8, 225-230. Academic Press, London. Jungblut, T.P., Schnitzler, J.P., Heller, W., Hertkorn, N., Metzger, Martin, S.S. (1977) Accumulation of the flavonoids betagarin and J.W., Szymczak, W. and Sandermann, J.H. (1995) Structures betavulgarin in Beta vulgaris infected by the fungus of UV-B induced sunscreen pigments of the scot pine (Pinus Cercospora beticola. Physiol. Plant Pathol., 11, 297-303. sylvestris L.). Angew. Chem. Int. Ed. Engl., 34, 312-314. Maxwell, C.A., Hartwig, U.A., Joseph, C.M. and Phillips, D.A. Kaplan, D.T., Keen, N.T. and Thomason, I.J. (1980a) Association (1989) A chalcone and two related flavonoids released from of glyceollin with the incompatible response of soybean roots alfalfa roots induce nod genes of Rhizobium meliloti. Plant to Meloidogyne incognita. Physiol. Plant Pathol., 16, 309- Physiol., 91, 842-847. 318. Mitscher, L.A., Okwute, S.K., Gollapudi, S.R., Drake, S. and Kaplan, D.T., Keen, N.T. and Thomason, I.J. (1980b) Studies on Avona, E. (1988) Antimicrobial pterocarpans of Nigerian the mode of action of glyceollin in soybean incompatibility to Erythrina mildbraedii. Phytochemistry, 27, 3449-3452. the root knot nematode, Meloidogyne incognita. Physiol. Plant Molish, H. (1937) Der Einfluss einer Pflanze auf die andere- Pathol., 16, 319-325. Allelopathie. Fisher, Jena. Karabourniotis, G., Papadopoulos, K., Papamarkou, M. and Muller, C.H. (1970) Phytotoxins as plant habitat variables. Rec. Manetas, Y. (1992) Ultraviolet-B radiation absorbing capacity Adv. Phytochem., 3, 106-121. of leaf hairs. Physiol. Plant., 86, 414-418. Nicholson, R.L., Kollipara, S.S., Vincent, J.R., Lyons, P.C. and Kato, M. (1978) Phenols as indispensible components of the Cadena-Gomez, G. (1987) Phytoalexin synthesis by the synthetic diet of the silkworm, Bombix mori. Entomol. Exp. sorghum mesocotyl in response to infection by pathogenic and Appl., 24, 285-290. nonpathogenic fungi. Proc. Natl. Acad. Sci. USA, 84, 5520- Klingauf, F. (1971) Die Wirkung des Glucosids auf das 5524. Wirtswahlverhalten von Rhopolosiphum insertum (Walk.) und Nicholson, R.L., Jamil, F.F., Snyder, B.A., Lue, W.L. and Aphis pomi De Geer (Homoptera: Aphididae). Z. Ang. Hipskind, J. (1988) Phytoalexin synthesis in the juvenile Entomol., 68, 41-55. sorghum leaf. Physiol. Mol. Plant Pathol., 33, 271-278. Kobayashi, A., Yata, S. and Kawazu, K. (1988) A β -hydroxy- Nielsen, J.K., Larsen, L.M. and Sørensen, H. (1979) Host plant chalcone and flavonoids from alfalfa callus stimulated by a selection of the horseradish flea beetle Phyllotreta armoraciae fungal naphthoquinone, PO-1. Agric. Biol. Chem., 52, 3223- (Coleoptera: Chrysomelidae): identification of two flavonol 3227. glycosides stimulating feeding in combination with Kondo, T., Ueda, M., Tamura, H., Yoshida, K., Isobe, M. and glucosinolates. Entomol. Exp. Appl., 26, 40-48. Goto, T. (1994) Composition of protocyanin, a self-assembled Nishida, R., Ohsugi, T., Kokubo, S. and Fukami, H. (1987) supramolecular pigment from the blue cornflower, Centaurea Oviposition stimulants of a Citrus-feeding swallowtail cyanus. Angew. Chem. Int. Ed. Engl., 33, 978-979. butterfly, Papilio xuthus L. Experientia, 43, 342-344. Kosslak, R.M., Bookland, R., Barkei, J., Paaren, E. and Nishida, R. (1994) Oviposition stimulant of a zeryntiine Appelbaum, E.R. (1987) Induction of Bradyrhizobium swallowtail butterfly, Luehdorfia japonica. Phytochemistry, japonicum common nod genes by isoflavones isolated from 36, 873-877. Glycine max. Proc. Natl. Acad. Sci. USA, 84, 7428-7432. Nishida, R. (1995) Oviposition stimulants of swallowtail butterfly. Lane, G.A., Biggs, D.R., Russell, G.B., Sutherland, O.R.W., In Scriber, J.M., Tsubaki, Y. and Lederhouse, R.C. (eds.) Williams, E.M., Maindonald, J.H. and Donnell, D.J. (1985) Swallowtail butterflies: their ecology and evolutionary biology. Isoflavonoid feeding deterrents for Costelytra zealandica. Scientific Publishers, Gainesville. Structure - activity relationships. J. Chem. Ecol., 12, 1713- Numata, A., Takemura, T., Ohbayashi, H., Katsuno, T., Yamamoto, 1735. K., Sato, K. and Kobayashi, S. (1983) Antifeedants for the Lane, G.A., Sutherland, O.R.W. and Skipp, R.A. (1987) larvae of the yellow butterfly, Eurema hecabe mandarina, in Isoflavonoids as insect feeding deterrents and antifungal Lycoris radiata. Chem. Pharm. Bull., 31, 2146-2149. components from root of Lupinus angustifolius. J. Chem. Ecol., Ohba, R., Igarashi, K. and Tsukui, A. (2000) Anthocyanins. Food 13, 771-783. color with health benefits. Kenpakusha, Tokyo. Larsen, L.M., Nielsen, J.K. and Sørensen, H. (1982) Identification Ohsugi, T., Nishida, R. and Fukami, H. (1985) Oviposition of 3-O-[2-O-(β-D-xylopyranosyl)-β-D-galactopyranosyl] stimulant of Papilio xuthus, a Citrus-feeding swallowtail flavonoids in horseradish leaves acting as feeding stimulants butterfly. Agric. Biol. Chem., 49, 1897-1900. for a flea beetle. Phytochemistry, 21, 1029-1033. O’Neill, T.M. and Mansfield, J.W. (1982) Antifungal activity of Levy, E.C., Ishaaya, I., Gurevitz, E., Cooper, R. and Lavie, D. hydroxyflavans and other flavonoids. Trans. Britain Mycol. (1974) Isolation and identification of host compounds eliciting Soc., 79, 229-237. attraction and bite stimuli in the fruit tree bark beetle, Scolytus Ootani, S. and Hayashi, K. (1982) Further search for water-soluble mediterraneus. J. Agric. Food Chem., 22, 376-379. carotenoids in yellow flowers of several plants. Res. Inst. Lodhi, M.A.K. and Killingbeck, K.T. (1980) Allelopathic Evolut. Biol. Sci. Rep., 1, 71-76. inhibition of nitrification and nitrifying bacteria in a ponderosa Ootani, S., Ito, T. and Iwashina, T. (1986) Identification of pine (Pinus ponderosa Dougl.) community. Amer. J. Bot., 67, anthocyanin and other pigments, and their distribution in the 1423-1429. perianth tissues of a cultivar, Crocosmia × crocosmiiflora Mabry, T.J., Markham, K.R. and Thomas, M.B. (1970) The (Iridaceae). Ann. Tsukuba Bot. Gard., 5, 47-53. systematic identification of flavonoids. Springer, Berlin. Pare, P.W., Dmitrieva, N. and Mabry, T.J. (1991) Phytoalexin Macías, F.A., Molinillo, J.M.G., Torres, A., Varela, R.M. and aurone induced in Cephalocereus senilis liquid suspension Castellano, D. (1997) Bioactive flavonoids from Helianthus culture. Phytochemistry, 30, 1133-1135. annuus cultivars. Phytochemistry, 45, 683-687. Parvez, M.M., Tomita-Yokotani, K., Fujii, Y., Konishi, T. and Marchelli, R. and Vining, L.C. (1973) The biosynthetic origin of Iwashina, T. (2002) Function of flavonoids as allelopathic chloroflavonin, a flavonoid antibiotic from Aspergillus substances. Third World Congress on Allelopathy. p. 247. candidus. Can. J. Biochem., 51, 1624-1629. Peng, Z. and Miles, P.W. (1988) Acceptability of catechin and its Markham, K.R. and Porter, L.J. (1969) Flavonoids in the green oxidative condensation products to the rose aphid, algae (Chlorophyta). Phytochemistry, 8, 1777-1781. Macrosiphum rosae. Entomol. Exp. Appl., 47, 255-265.

－ 42 － Iwashina, T.

Perrin, D.R. and Bottomley, W. (1962) Studies on phytoalexins. Tabashnik, B.E. (1987) Plant secondary compounds as oviposition V. The structure of pisatin from Pisum sativum L. J. Amer. deterrents for cabbage butterfly, Pieris rapae (Lepidoptera, Chem. Soc., 84, 1919-1923. Pieridae). J. Chem. Ecol., 13, 309-316. Perrin, D.R. and Cruickshank, I.A.M. (1969) The antifungal Takahashi, H., Sasaki, T. and Ito, M. (1987) New flavonoids activity of pterocarpans towards Monilinia fructicola. isolated from infected sugarbeet roots. Bull. Chem. Soc. Japan, Phytochemistry, 8, 971-978. 60, 2261-2262. Peters, N.K., Frost, J.W. and Long, S.R. (1986) A plant flavone, Takasugi, M., Kumagai, Y., Nagao, S., Masamune, T., Shirata, A. luteolin, induces expression of Rhizobium meliloti nodulation and Takahashi, K. (1980) The co-occurrence of flavan and genes. Science, 233, 977-980. 1,3-diphenylpropane derivatives in wounded paper mulberry. Peters, N.K. and Long, S.R. (1988) Alfalfa root exudates and Chem. Lett., p. 1459-1460. compounds which promote or inhibit induction of Rhizobium Tamura, S., Chang, C.-F., Suzuki, A. and Kumai, S. (1967) meliloti nodulation genes. Plant Physiol., 88, 396-400. Isolation and structure of a novel isoflavone derivative in red Piattelli, M. and Impellizzeri, G. (1971) Fungistatic flavones in clover. Agric. Biol. Chem., 31, 1108-1109. the leaves of Citrus species resistant and susceptible to Tamura, S., Chang, C.-F., Suzuki, A. and Kumai, S. (1969) Deuterophoma tracheiphila. Phytochemistry, 10, 2657-2659. Chemical studies on “clover sickness” part I. Isolation and Picman, A.K., Schneider, E.F. and Picman, J. (1995) Effect of structural elucidation of two new isoflavonoids in red clover. flavonoids on mycelial growth of Verticillium albo-atrum. Agric. Biol. Chem., 33, 391-397. Biochem. Syst. Ecol., 23, 683-693. Tebayashi, S.-i., Matsuyama, S., Suzuki, T., Kuwahara, Y., Pinkas, J., Lavie, D. and Chorin, M. (1968) Fungistatic Nemoto, T. and Fujii, K. (1995) Quercimeritrin: the third constituents in citrus varieties resistant to the mal-secco oviposition stimulant of the azuki bean weevil from the host disease. Phytochemistry, 7, 169-174. azuki bean. J. Sci., 20, 299-305. Rao, A.S. (1990) Root flavonoids. Bot. Rev., 56, 1-84. Thompson, W.R., Meinwald, J., Aneshansley, D. and Eisner, T. Redmond, J.W., Batley, M., Djordjevic, M.A., Innes, R.W., (1972) Flavonols: pigments resposible for ultraviolet Kuempel, P.L. and Rolfe, B.G. (1986) Flavones induce absorption in nectar guide of flower. Science, 177, 528-530. expression of nodulation genes in Rhizobium. Nature, 323, Tomás-Barberán, F.A., Msonthi, J.D. and Hostettmann, K. (1988a) 632-635. Antifungal epicuticular methylated flavonoids from Rice, E.L. and Pancholy, S.K. (1973) Inhibition of nitrification Helichrysum nitens. Phytochemistry, 27, 753-755. by climary ecosystems. II. Additional evidence and possible Tomás-Barberán, F.A., Millard, M. and Hostettmann, K. (1988b) role of tannins. Amer. J. Bot., 60, 691-702. Antifungal flavonoids from the leaf surfaces of Helichrysum Rice, E.L. and Pancholy, S.K. (1974) Inhibition of nitrification nitens and from the stem bark of Erythrina berteroana. Plant by climax ecosystems III. Inhibitors other than tannins. Amer. flavonoids in biology and medicine II. Biochemical, cellular, J. Bot., 61, 1095-1103. and medicinal properties. In Cody, V., Middleton Jr., E. Rieseberg, L.H. and Schilling, E.E. (1985) Floral flavonoids and Harborne, J.B. and Beretz, A. (eds) Aran R. Liss, Inc. New ultraviolet patterns in Viguiera (Compositae). Amer. J. Bot., York, pp. 61-65. 72, 999-1004. VanEtten, H.D. (1973) Differential sensitivity of fungi to pisatin Roussis, V., Ampofo, S.A. and Wiemer, D.F. (1987) Flavanones and to phaseollin. Phytopathology, 63, 1477-1482. from Lonchocarpus miniflorus. Phytochemistry, 26, 2371- VanEtten, H.D. (1976) Antifungal activity of pterocarpans and 2375. other selected isoflavonoids. Phytochemistry, 15, 655-659. Russell, G.B., Sutherland, O.R.W., Hutchins, R.F.N. and Waiss, A.C., Chan, B.G., Elliger, C.A., Wiseman, B.R., Christmas, P.E. (1978) Vestitol: a phytoalexin with insect McMillian, W.W., Widstrom, N.W., Zuber, M.S. and Keaster, feeding-deterrrent activity. J. Chem. Ecol., 4, 571-579. A.J. (1979) Maysin, a flavone glycoside from corn silks with antibiotic activity toward corn earworm. J. Econ. Entomol., Sanduja, R., Martin, G.E., Weinheimer, A.J., Alam, M., Hossain, 72, 256-258. M.B. and Van der Helm, D. (1984) Secondary metabolites of Wang, Y., Hamburger, M., Gueho, J. and Hostettmann, K. (1989) the coelenterate Echinophora lamellosa. J. Heterocycl. Chem., Antimicrobial flavonoids from Psiadia trinervia and their 21, 845-848. methylated and acetylated derivatives. Phytochemistry, 28, Shaver, T.N. and Lukefahr, M.J. (1969) Effect of flavonoid 2323-2327. pigments and gossypol on growth and development of the Weidenbörner, M., Hindorf, H., Jha, H.C., Tsotsonos, P. and Egge, bollworm, tobacco budworm, and pink bollworm. J. Econ. H. (1989) Antifungal activity of isoflavonoids against storage Entomol., 62, 643-646. fungi of the genus Aspergillus. Phytochemistry, 28, 3317-3319. Simmonds, M.S.J., Blaney, W.M., Monache, F.D. and Bettolo, Weidenbörner, M., Hindorf, H., Jha, H.C., Tsotsonos, P. and Egge, G.B.M. (1990) Insect antifeedant activity associated with H. (1990a) Antifungal activity of isoflavonoids in different compounds isolated from species of Lonchocarpus and reduced stages on Rhizoctonia solani and Sclerotium rolfsii. Tephrosia. J. Chem. Ecol., 16, 365-380. Phytochemistry, 29, 801-803. Skaltsa, H., Verykokidou, E., Harvala, C., Karabouriotis, G. and Weidenbörner, M., Hindorf, H., Jha, H.C. and Tsotsonos, P. Manetas, Y. (1994) UV-B Protective potential and flavonoid (1990b) Antifungal activity of flavonoids against storage fungi content of leaf hairs of Quercus ilex. Phytochemistry, 37, 987- of the genus Aspergillus. Phytochemistry, 29, 1103-1105. 990. Yabuya, T. (1987) High-performance liquid chromatographic Snyder, B.A., Leite, B., Hipskind, J., Butler, L.G. and Nicholson, analysis of anthocyanins in induced amphidiploids of Iris R.L. (1991) Accumulation of sorghum phytoalexins induced laevigata Fisch. × I. ensata Thunb. Euphytica, 36, 381-387. by Colletorichum graminicola at the infection site. Physiol. Yamada, T. and Ito, S.-i. (1993) Chemical defense responses of Mol. Plant Pathol., 39, 463-470. wilt-resistant pine species, Pinus strobus and P. taeda, against Burssaphelenchus xylophilus infection. Ann. Phytopath. Soc. Stafford, H.A. (1990) Flavonoid metabolism. CRC Press, Boca Japan, 59, 666-672. Raton. Zaat, S.A.J., Schripsema, J., Wijffelman, C.A., van Brussel, Star, A.E. (1980) Frond exudate flavonoids as allelopathic agents A.A.N. and Lugtenberg, B.J.J. (1989) Analysis of the major in Pityrogramma. Bull. Torrey Bot. Club, 107, 146-153. inducers of the Rhizobium nodA promoter from Vicia sativa Stössel, P. (1982) Glyceollin production in soybean. Phytopath. root exudate and their activity with different nodD genes. Plant Z., 105, 109-119. Mol. Biol., 13, 175-188.

－43－ Flavonoid function and activity

Zielske, A.G., Simons, J.N. and Silverstein, R.M. (1972) A flavone feeding stimulant in alligatorweed. Phytochemistry, 11, 393- 396.

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