why leaves turn red · (blue) wavelengths, overlapping with the absorbance of chlorophyll,...

Many forests, like those spreadthroughout New England, have

just changed color in a spectacularway, as they do each fall. The phenom-enon is familiar as well as dramatic, yetwhy it should happen has been a long-standing enigma. When we were inschool, the standard textbooks saidthat foliage changes color because thebreakdown of green chlorophyll mole-cules unmasks other pigments, like theyellow-to-orange xanthophylls and thered-or-blue anthocyanins, which, wewere told, serve no particular functionduring the autumn senescence ofleaves. Now botanists know better.

Indeed, a completely new apprecia-tion for these colorful pigments has de-veloped over the past decade or so, inpart from our studies of trees in theHarvard Forest, a nature sanctuary incentral Massachusetts maintained forscientific research. There, during Sep-tember and October, one sees theleaves on dozens of woody specieschanging color. In some plants, such asthe witch hazel (Hamamelis virginiana),it is indeed the loss of chlorophyll thatreveals yellow carotenoid pigments,just as the textbooks say. However, for

the forest’s 70 percent of tree speciesthat contain anthocyanin pigments(which produce colors ranging frombrown to red, depending on howmuch chlorophyll the leaves retain),the story is quite different. For exam-ple, the brilliant fall foliage of the redoak (Quercus rubra) results from the ac-cumulation of anthocyanin in the vac-uoles (large, fluid-filled cavities) ofcells lying just under the leaves’ upperepidermis layer.

Anthocyanins are elaborate pigmentmolecules, widespread among landplants. They account not only for theautumn hues of temperate woodlands,but also for the flushes of developingred foliage seen in tropical forests, onthe undersurface of shaded leaves andin crop plants suffering drought or nu-trient deficiency. But plants can alsohave other red pigments. Carotenoids,often rhodoxanthin, produce red colorin the senescing leaves of some conifersas well as in the common box (Buxussempervirens), which decorates manysuburban lawns. Betalain pigmentscolor leaves red in a single order offlowering plants, and a few other mis-cellaneous pigments produce bur-gundy hues in very rare cases. But ofall the red pigments, the anthocyaninsare the most widespread.

We have collaborated in studying an-thocyanin pigments since 1993 and arebeginning to develop some workinghypotheses about their function. It’s cu-rious that an understanding has beenso long in coming, given the fact thesered pigments have been subjected toscientific scrutiny for nearly 200 years.

The Discovery of AnthocyaninsAnthocyanins had been observed forcenturies as “colored cell sap.” In 1835the German botanist Ludwig Marquart

gave them their name, deriving antho-cyanin from the Greek anthos, meaningflower, and kyanos, meaning blue.Many long-standing misconceptionsabout anthocyanin function date fromthese early observations, notably thatthese pigments arise from the break-down of chlorophyll during autumn.

Given how striking and attractivered foliage is, it may seem baffling thatbotanists remained ignorant about thephenomenon for so long. There arevarious reasons for this. First, becauseanthocyanins are responsible for thecolors of fruits and flowers as well as ofleaves, it was natural to concentrate onpigmentation in the former economi-cally important organs, for which thefunction of anthocyanin seems obvi-ous—to attract animals for pollinationand seed dispersal. Second, becausethe discoveries of Richard Willstätterand his colleagues about the molecu-lar structure of anthocyanins from 1912to 1916 were made shortly after the re-discovery of Mendel’s laws of inheri-tance, the anthocyanins became an ear-ly subject of research in moleculargenetics, rather than physiology.(Mendel’s peas had distinctively col-ored flowers because of anthocyanins.)Third, the discovery that light can in-duce anthocyanin production inspiredmolecular biologists to study how lightexposure activates genes involved inanthocyanin synthesis, again at the ex-pense of research into anthocyaninfunction.

Botanists of the late 19th-century, mostnotably the Germans who studied plantanatomy and physiology, noticed thatanthocyanin production rises when aplant is subjected to low temperaturesand high light conditions. This observa-tion led to the popular explanations thatanthocyanins protect the photosynthetic

524 American Scientist, Volume 90

Why Leaves Turn Red

Pigments called anthocyanins probably protect leaves from light damageby direct shielding and by scavenging free radicals

David W. Lee and Kevin S. Gould

David Lee is a professor in the Department of Bio-logical Sciences at Florida International Universi-ty and Research Collaborator at Fairchild TropicalGarden in Miami. He has studied leaf color andfunction since 1973. He received his Ph.D. inbotany from Rutgers University in 1970. KevinGould is an associate professor in the School of Bi-ological Sciences at the University of Auckland inNew Zealand. He received his Ph.D. in botanyfrom the University of Manchester in 1985. Hehas applied his background in plant cell and devel-opmental biology to the mysteries of the functionalecology of New Zealand’s diverse plants. Addressfor Lee: Department of Biological Sciences, FloridaInternational University, Miami, FL 33199. Inter-net: [email protected]

©Sigma Xi, The Scientific Research Society. Reproduction withpermission only. Contact [email protected].

structures against intense sunlight andhelp to warm leaves by increasing theirrates of metabolism. These scientistslacked the instrumentation and detailedknowledge of photosynthesis to test theirideas. In the mid-20th century, investiga-tors became aware that ultraviolet (UV)radiation could induce anthocyanin syn-thesis, leading to the hypothesis that an-thocyanins protect plant tissues againstUV damage. But, as it turns out, antho-cyanins absorb rather weakly in the UV-B region of the spectrum (wavelengthsof 285–320 nanometers), which is mostresponsible for damage to biological tis-sues; other colorless flavonoid pigmentsthat are equally, or more, abundant in theleaves absorb UV-B much more strongly.Furthermore, anthocyanins are mostcommonly produced in the interiors ofleaves and hence are poorly placed toprotect leaves from the widespread ef-fects of UV-B. These weaknesses were re-futed by one of us (Lee) in 1987. So whatgood are anthocyanins to a leaf? Two re-cent discoveries have shed light on themystery.

Red SunscreenWhen surroundings are bright andcold, photosynthetic efficiency oftendeclines. The phenomenon, known asphotoinhibition, has been attributed inpart to impairment in one of the func-tional elements of photosynthesis. Nor-mally, two units consisting of pig-ments, proteins and electron-transfermolecules—known as photosystems Iand II—absorb light energy. Photoinhi-bition apparently involves a block inphotosystem II. Unchecked, this im-pairment can permanently damagechloroplasts, cells and tissues.

Investigators can observe photoinhi-bition because when photosynthetic tis-sues receive a pulse of intense light,they immediately emit a pulse of visi-ble light—that is, they fluoresce. De-tailed analysis of this flash revealsmuch about photosynthetic function.New techniques to measure this fluo-rescence have helped investigators testthe efficiency of the light reaction ofphotosynthesis under different condi-tions and to detect photoinhibition. A

variety of factors can contribute tophotoinhibition: intense sunlight; lowtemperature; acclimation of leaves toextreme shade with a subsequent ex-posure to high light; and inadequatephosphorus, which is important in theproduction of two energy-rich com-pounds crucial for photosynthesis—adenosine triphosphate (ATP) and thereduced form of nicotinamide adeninedinucleotide phosphate (NADPH).When chloroplasts are overwhelmedwith energy, the excess causes chemicaland, ultimately, physical damage.

Plants have evolved several strate-gies to prevent photoinhibitory damagefrom intense light, in particular the in-terconversion of certain xanthophyllpigments as a way of quenching theoverload of energy. Anthocyanins alsoefficiently protect against photoinhibi-tion because they soak up radiant ener-gy at wavelengths poorly absorbed byother accessory pigments, such as inthe green waveband at around 530nanometers. In intact tissues, the rangeof absorbance also extends into shorter

2002 November–December 525


Figure 1. Anthocyanins are common in the autumn leaves of mid-latitude trees, but these pigments also add flashes of red color to the foliageof tropical forests and to crop plants exposed to drought or nutrient deficiency. Occasionally, anthocyanins are present in leaves year-round, asin the variegated leaves of Horopito (Pseudowintera colorata), a common tree in New Zealand forests (above). The patterns of coloration in thisspecies make the leaves ideal for studying the antioxidant properties of these intriguing molecules. (Except where noted, all photographs by theauthors.)

(blue) wavelengths, overlapping withthe absorbance of chlorophyll, particu-larly with chlorophyll b, one of the twomajor forms of the pigment. In addi-tion, anthocyanins are very stable com-pounds in the mildly acidic environ-ment of the cell vacuoles that containthem. The hardy anthocyanins can thusshield the more delicate chlorophyllmolecules housed in the chloroplasts.

During the past decade fluorescencemeasurements have yielded growingevidence that the anthocyanins indeedprotect against photoinhibition. Tay-lor Field, then a graduate student atHarvard University and now a facultymember at the University of Toronto;Noelle Holbrook at Harvard; and one

of us (Lee) found support for the pro-tective function of anthocyanins in thered-osier dogwood (Cornus stolonifera).We were able to compare the photosyn-thetic responses of senescing leaves thatvaried only in the presence or absenceof anthocyanin near their surfaces. Wehypothesized that this pigment layerwould protect the photosynthetic tis-sues underneath. And we were right.

When exposed to intense light, thered leaves in our experimental collec-tion suffered less and recovered morequickly than the green leaves. The de-gree of protection was even greater atlow temperatures. When we illuminat-ed the red and green leaves from theirgreen undersurfaces, the anthocyanin

layer could not protect the photosyn-thetic tissues, and both red and greenshowed the same degree of photoinhi-bition. Workers in other laboratorieshave evidence that anthocyanins alsoprotect Antarctic mosses, pine needlesand understory plants found in tropi-cal rainforests.

Antioxidants by and for PlantsIn addition to protecting plants fromthe usually short-term problem ofphotoinhibition, anthocyanins appearto protect plants from permanent dam-age by acting as antioxidants. One con-sequence of the absorption of intensesunlight in leaves is increased produc-tion of reactive oxygen species and free



Figure 2. Some senescing autumn leaves, such as the witch hazel (Hamamelis virginiana, left) are yellow. A transverse section of a leaf (right)shows that the yellow pigments are clustered exclusively in the chloroplasts, which are degrading. The loss of chlorophyll reveals the yellowcarotenoid pigments. (Except where noted, all microscopic images are magnified 250 times.)

Figure 3. Many senescing leaves are red, as in the red oak (Quercus rubra, left). A transverse section (right) shows that the anthocyanin pigmentsresponsible for this color are located in vacuoles of the long, thin palisade cells, which are stacked upright just under the upper epidermis.

radicals (molecules with unpaired elec-trons), such as singlet oxygen (1O2),superoxide (•O2

–) and the extremelytoxic hydroxyl radical (•OH). The pres-ence of unpaired electrons makes mostfree radicals unstable and highly reac-tive. But not all of them are damagingto plants. Some are involved in thenormal formation of lignins, whichstrengthen cell walls; others fight offpathogens. However, when the con-centration of free radicals exceeds theability of natural antioxidants to quenchthem—particularly during periods ofstress—these reactive molecules can de-stroy the biological machinery aroundthem, including membranes, proteinsand DNA, potentially leading to celldeath. Leaves, with their relatively highconcentrations of oxygen from photo-synthesis and with their frequent expo-sure to intense sunlight, seem particu-larly vulnerable to oxidative damage.

Anthocyanins have the potential tocurtail photooxidative damage by ab-sorbing green wavelengths of light,thus shielding chloroplasts beneathfrom a portion of the spectrum thatthey cannot exploit for energy pro-duction. Thomas Vogelmann, who re-cently moved from the University ofWyoming to the University of Ver-mont, and his colleagues have shownthat the light energy that anthocyaninsabsorb does not subsequently transferto the chloroplasts. Instead, the energyeither is retained in the vacuole con-taining the anthocyanins (preliminaryevidence suggests that energy makesthe molecules vibrate and even hum)or, more likely, is dissipated graduallyas heat. Consequently, the chloroplastsin red leaves produce fewer free radi-cals. Samuel Neill, a Ph.D. student atthe University of Auckland, measuredlevels of superoxide produced by asuspension of chloroplasts taken fromleaves of lettuce. When the chloroplastswere irradiated with white light, theamount of superoxide rapidly in-creased, whereas they produced muchlower levels when irradiated with lightthat was of a similar intensity but hadbeen passed through a green-absorb-ing filter. Clearly, the absorption ofgreen light by anthocyanins impedessuperoxide production.

Anthocyanins may also help a plantbecause they are potent antioxidants.Solutions of cyanidin, the most preva-lent anthocyanin in leaves, have aboutfour times more antioxidant capacitythan ascorbic acid or vitamin E. People



Figure 4. Beta-carotene molecules (top) add yellow color to senescing leaves. The light ab-sorbance spectrum of leaves containing beta-carotene is compared with the absorbance spec-trum of the molecule alone. The most common anthocyanin molecule in leaves is cyanidin-3-glucoside (bottom). Again, the absorbance spectrum of leaves containing the pigment iscompared with the wavelengths of light absorbed by the isolated molecule. Because of thescattering of light within leaves, the absorbance spectra of the molecules are broader whenthey are in their native environment than when the pigments are isolated.

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who ingest anthocyanins from freshfruit and red wine can improve the an-tioxidant status of their blood plasma.In 1999 James Joseph and many collab-orators at the United States Departmentof Agriculture and at Tufts Universitydemonstrated dramatic reversals in thedecline of nervous system activity inmice that were fed anthocyanin-richblueberries (Vaccinium corymbosum).Widespread reporting about these re-sults led to a run on fresh blueberriesin supermarkets across the country.Now a growing body of evidenceshows the effects of anthocyanins asantioxidants, raising the possibilitythat perhaps these molecules are ashealth-promoting for the plants thatproduce them as for the animals thatingest them.

One of us (Gould) and his colleaguesstudied the potential for such protec-tion in a New Zealand shrub, Pseudo-wintera colorata. Parts of the upper sur-faces of its leaves are blotched red from

the accumulation of anthocyanins.When we punctured the leaves with afine needle, chloroplasts in the injuredarea produced strong bursts of the re-active oxygen compound hydrogenperoxide (H2O2), which we could de-tect and monitor over time. Chloro-plasts in both the green and red areasproduced hydrogen peroxide, but dif-ferences between the two regions be-came apparent within minutes of in-jury. Hydrogen peroxide continued toaccumulate in the green portions for 10minutes and then decreased only slow-ly. In contrast, levels in the red regionsdeclined rapidly to background countswithin the first five minutes.

How exactly do the anthocyaninsprotect from oxidative damage? Thephenomenon is rather enigmatic.Whereas the troublemaking oxygenmolecules do their damage in the chlor-oplasts or in the cytoplasm, the antho-cyanins are largely sequestered in cellvacuoles. Perhaps the anthocyanins,which are produced in the cytoplasm,carry out their antioxidative functionthere, before moving into vacuoles. Ormaybe these organelles act as spongesfor destructive hydrogen peroxide,which, unlike other reactive oxygenmolecules, can migrate across themembrane of a vacuole.

Even if biologists figure out how it isthat anthocyanins can protect plantcells from oxidative damage, it will behard to say whether these pigmentsevolved primarily to scavenge free rad-icals or to combat photoinhibition. It ispossible that these functions act simul-taneously to protect plant tissues fromintense sunlight. By absorbing light,anthocyanins would reduce the rate ofboth photoinhibition and photooxida-tive damage, and they could also neu-tralize whatever free radicals still endedup being produced. Both mechanismscould serve to protect plant tissues thatare especially vulnerable to such dam-age, such as those under environmen-tal stress or in developing leaves whenthe photosynthetic structures are beingassembled.

Despite the protective functions ofanthocyanins (particularly in bright,cold conditions), it is difficult to under-stand why plants invest energy to pro-tect foliage that is about to fall off.Shielding the photosynthetic appara-tus of a dying leaf would add little tothe carbon supply of a tree and is un-likely to justify the metabolic cost ofsynthesizing an elaborate pigment



Figure 5. Red or purple color is often seen onthe undersurfaces of leaves growing in thelower, more shaded parts of forests, especial-ly in the tropics. The herb shown (Triolenahirsuta) grows in the tropical understory ofCentral American forests. Whether or nottheir undersides are red varies, making thema good subject for research. (Photographcourtesy of George Valcarce.)

Figure 6. Investigators in the 19th century carefully observed the distribution of anthocyaninsin different plants. Belgian botanist Édouard Morren published these microscope observationsin 1858, showing the distribution of anthocyanins in the various organs of young seedlings ofred cabbage (Brassica oleracea).

molecule. But it is possible that thebenefits continue into the next grow-ing season, if, for example, the antho-cyanins in autumn leaves act to allowthe coordinated disassembly of thephotosynthetic apparatus, particularlythe breakdown of chlorophyll, beforethe leaves drop.

The critical issue may be the move-ment of nitrogen back into the plant.The photosynthetic apparatus in leavescontains much of the total nitrogen,which is wasted if the plant does notrecover it before the leaves detach.Anthocyanins could protect this dis-mantling process in leaves and in-crease the amount of nitrogen shiftedinto the woody tissues of the parenttree. Although the explanation is sim-ple enough, it may be difficult to obtain

clear support for it. Anthocyanic con-centration in foliage, which varies bothamong and within species, such as redmaple (Acer rubrum), should be corre-lated with lower nitrogen levels in leaftissues and higher efficiencies of ab-sorption into the plant. But the efficien-cy of nitrogen absorption can vary agreat deal, both among individualplants within the same species and inthe same plant from year to year. It’spossible that the increase in absorptionmay be rather small, and therefore hardto detect, and yet still provide signifi-cant advantage. We have obtained somepreliminary evidence supporting thishypothesis from shrubs and trees at theHarvard Forest, but much more re-search will be required to properly testthis prediction.

Ecological Functions of Anthocyanins Some biologists have speculated thatthe red colors in leaves may protectthem from being eaten. Anthocyaninsare members of a class of plant com-pounds (polyphenols) that sometimesdefend against predators, insects andmicrobes, but anthocyanins themselvesdon’t seem to act as poisonous deter-rents. However, the red appearance ofleaves may warn animals that theleaves are unpalatable. In many tropi-cal trees, for example, young red-pur-ple leaves hang from branch tips untilat the end of their development theyrapidly become green. Phyllis Coley ofthe University of Utah has shown thatthese anthocyanic leaves have very lownitrogen content and are seldom dam-aged by herbivores. She believes that



Figure 7. Red-osier dogwood (Cornus stolonifera), photographed in the Catskill Mountains of New York, has red leaves in the autumn as wellas some persisting green leaves (left). Green and red leaves on the plant differ in their relative photosynthetic efficiencies (right). Red leaves loseless efficiency when exposed to intense light and recover more rapidly after the exposure.

Figure 8. Puncturing the leaves of Pseudowintera colorata (the plant shown in Figure 1) with a needle leads to the release of hydrogen peroxide(H2O2), which can be revealed using a blue dye that loses its fluorescence when exposed to this highly reactive compound. When a green leafblade was tested (a), it was flooded with hydrogen peroxide, as shown by the lack of fluorescence around the puncture (b), and levels decreasedonly slowly. But when a red portion of a leaf was pricked (c), hydrogen peroxide levels returned to normal within five minutes (d).

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the anthocyanins may inhibit thegrowth of fungi that leaf-cutting antscultivate and thus reduce leaf collec-tion by the ants.

Paul Lucas of the University of HongKong and his colleagues have arguedthat young, red leaves in tropical forestsare edible, and indeed important in thediets of some primates. They haveshown that chimpanzees and monkeysof the Kibale Forest, in Uganda, preferyoung, red leaves, which are highlypalatable because of high protein lev-els and tenderness. Field tests of feed-ing activities suggested to them thatred-to-green shifts in leaf color are im-portant cues that led to the evolution ofthree-color vision in certain primates(including humans), unique among all

mammals. In rare cases, anthocyanincolor in leaves may attract animals toconsume fruits and disperse seeds, butfew of the red-senescing plants we havestudied produce fruits that persist solate in the growing season.

It’s conceivable that autumn col-oration evolved to deter herbivores, butthe deterrence would only lead to a se-lective advantage if it protected the treesfrom damage in subsequent seasons.The late William Hamilton of OxfordUniversity and Samuel Brown, currentlyat the University of Montpellier II inFrance, argued that autumn colorationcould warn aphids against laying eggson trees defended with plant com-pounds. Thus, the autumn colorationcould prevent leaves from being eaten

the following year, when the eggswould have hatched. So far this researchis based on literature surveys and mod-eling, with experiments and direct fieldobservations yet to be completed.

Problems Remain The research we have described in thisarticle is a dramatic shift toward the so-lution of a long-standing mystery, butit is just a beginning. Many questionsremain: For example, if anthocyaninsfulfill an important physiological orecological function for certain plants,why then do some plants not producesuch pigmentation? And why aren’tmore leaves red all the time? Interest-ingly, one large group of floweringplants, in the order Caryophyllales, are



Figure 9. Anthocyanins are common in the developing leaves of tropical plants, such as the cocoa plant (Theobroma cacao). The shrub (left) andleaves (middle) were photographed in French Guiana. An even closer view through the leaf surface (right) reveals that anthocyanins are locat-ed exclusively in the tips of hairs and in cells surrounding leaf veins.

Figure 10. In a single order of flowering plants, red leaf color arises not from anthocyanins but from the presence of nitrogen-containing betalain pig-ments. Bougainvillea (Bougainvillea spectabilis) is a tropical, shrubby vine whose developing leaves and flower bracts are red because of betalains,specifically the compound betanin (top right). A section through a leaf shows that the pigment is located in the epidermis and hairs (lower right).

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incapable of synthesizing anthocyanins,although they produce the precursorflavonoid pigments. Still, these plantsproduce red colors, in both vegetativeand reproductive organs, but with a to-tally different class of pigments—thebetalains. Beets are a good example.The nitrogen-containing betanin hassimilar absorbance characteristics tothe anthocyanins and also is a strongfree-radical scavenger. Do these mole-cules function as an equivalent to an-thocyanins in this order of floweringplants? If so, how did they originate?

In some cases, genes that promoteanthocyanin production in leaves mayalso promote production in flowersand other organs. This connection mayconfound efforts to interpret field tri-als that test whether plants with antho-cyanins are more likely to survive thanthose without these pigments. Butthese problems are not insurmount-able. For instance, investigators cancompare the performance of normalplants with those of natural mutants—or genetically engineered ones—vary-ing in the production of anthocyanin.We expect some exciting research onthe functions of anthocyanins in vege-tative organs in the near future.

AcknowledgmentsMuch of Gould’s research was supported bya Royal Society of New Zealand Marsdengrant. Lee’s research on autumn leaf colorchange, following earlier work in the tropics,was supported by a Bullard Fellowship atthe Harvard Forest in 1998. Both authors

learned much from many collaborators andfrom a symposium, “Why Leaves TurnRed,” that they organized at the BotanicalSociety of America Meetings in Albu-querque, New Mexico, in 2001—which ledto the edited book cited in the Bibliography.

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leaf colours and herbivore defense. Proceed-ings of the Royal Society of London B. BiologicalSciences 268:1489–1493.

Coley, P. D., and J. A. Barone. 1996. Herbivoryand plant defenses in tropical forests. An-nual Reviews of Ecology and Systematics27:305–335.

Dominy, N. J., and P. W. Lucas. 2001. Ecologicalimportance of trichromatic vision to pri-mates. Nature 410:363–366.

Field, T. S., D. W. Lee and N. M. Holbrook. 2001.Why leaves turn red in autumn. The role ofanthocyanins in senescing leaves of red-osierdogwood. Plant Physiology 127:566–574.

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Lee, D. W., S. Brammeier and A. P. Smith. 1987.The selective advantages of anthocyanins indeveloping leaves of mango and cacao.Biotropica 19:40–49.

Lee, D. W., and T. W. Collins. 2001. Phyloge-netic and ontogenetic influences on the dis-tribution of anthocyanins and betacyaninsin leaves of tropical plants. International Jour-nal of Plant Science 162:1141–1153.

Neill, S. O., K. S. Gould, P. A. Kilmartin, K. A.Mitchell and K. R. Markham. 2002. Antioxi-dant activities of red versus green leaves inElatostema rugosum. Plant Cell and Environ-ment 25:537–549

Simms, E. L., and M. A. Bucher. 1996. Pleiotrop-ic effects of flower color intensity on herbi-vore performance in Ipomoea purpurea. Evo-lution 50:957–963.

Tsuda, T., Y. Kato and T. Osawa. 2000. Mech-anism for the peroxynitrite scavengingactivity by anthocyanins. FEBS Letters484:207–210.

Wheldale, M. 1916. The Anthocyanin Pigments ofPlants. Cambridge: Cambridge UniversityPress.

Winkel-Shirley, B. 2001. Flavonoid biosynthe-sis: a colorful model for genetics, biochem-istry, cell biology and biotechnology. PlantPhysiology 126:485–493.



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