the ecophysiology of foliar anthocyanin

8/9/2019 the Ecophysiology of Foliar Anthocyanin

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T h e B o t a n i c a l R e v i e w 6 9 2 ) : 1 4 9 - 1 6 1

Th e Ecoph ys io logy of Fol ia r n thocyanin

D U G A L D C . CLOS E 1 AND HRISTOPHER L. BEAOCE t 2

~ C o o p e r at iv e R e s e a r c h C e n t r e f o r S u s t a i n a b l e P r o d u c t i o n F o r e s t r y

G P O B o x 2 5 2 - 1 2

H o b a r t 7 0 01 Ta s m a n i a

2 C S I R O F o r e s t r y a n d F o r e s t P r o d u c t s

G P O B o x 2 5 2 - 1 2

H o b a r t 7 0 01 Ta s m a n i a

I. A b stra ct . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 149II. I ntr od uc tio n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15 0

III . Anthocy anin Accumu la t ion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 150A. Expanding Leaves. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 150B. Autumn Senescence. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5C . N u tritio n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 151D . U ltr av io le t L ig ht . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 151E . H e rb iv o ry a nd D isease . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 52

IV. Anthocyanin and Photoprotection. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 153A . O sm o tic A d ju stm e nt . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 53B . A n tio x id an ts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 153C . L ig ht A tte nu atio n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 54

1. I nte rn a l L e a f D is tr ib u tio n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 542. Seedlings. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1543. Does Light Absorpt ion by Anthocy anin Provide Photoprotec tion? . . . . . . . . . . 155

V. C o nc lu sio n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 56V I. A c kn ow le dg m en ts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15 7

V II. L iteratu re C ite d . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 57

I A b s t r a c t

T h e a c c u m u l a t i o n o f f o l ia r a n t h o c y a n i n s c a n b e c o n s i s te n t l y a tt r ib u t e d to a s m a l l r a n g e o fc o n t e x ts . F o l i a r a n t h o c y a n i n a c c u m u l a t e s i n y o u n g , e x p a n d i n g f o li a g e, i n a u t u m n a l f o l ia g e o fd e c i d u o u s s p e c ie s , i n r e s p o n s e t o n u t r i e n t d e f i c ie n c y o r u l t r a v io l e t U V ) r a d i a t i o n e x p o s u r e ,a n d i n a s s o c ia t io n w i t h d a m a g e o r d e f e n s e a g a i n s t b r o w s i n g h e r b i v o r e s o r p a t h o g e n i c f u n g a li n f ec t io n . A c o m m o n t h r e a d t h r o u g h t h e s e c a u s a t i v e f a c to r s i s lo w p h o t o s y n t h e t i c c a p a c i ty o f

f o l ia g e w i t h a c c u m u l a t e d a n t h o c y a n i n r e la t iv e t o l e a v e s a t d i f f er e n t o n t o g e n e t i c s t a g e s o r u n a f -f e c t e d b y t h e e n v i r o n m e n t a l f ac t o r i n q u e s ti o n .

T h e e c o p h y s i o l o g i c a l f u n c ti o n o f a n t h o c y a n i n h a s b e e n h y p o t h e s i z e d a s : 1 ) a c o m p a t i b l es o l u t e c o n t r i b u t i n g t o o s m o t i c a d j u s t m e n t to d r o u g h t a n d f r o s t s tr e s s ; 2 ) a n a n t i o x i d a n t ; 3 ) a

C o p i e s o f t h is i ss u e [ 6 9 2 ) ] m a y b e p u r c h a s e d f r o m t h e N Y B G P r e s s ,T h e N e w Y o r k B o t a n i c a l G a r d e n , B r o n x , N Y 1 0 4 5 8 - 5 1 2 8 , U . S . A .;n y b g p r e s s @ n y b g . o rg . P l e a s e i n q u i r e a s t o p r ic e s .

I s s u ed 1 6 D e c e m b e r 2 0 0 39 2 0 0 3 T h e N e w Yo r k B o t a ni c al G a r d e n 1 4 9


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150 THE BOTA NICALREVIEW

U V protectant; and 4) protection from visible light. Review o f the internal le af distribution o fanthocyanin, o f experimental evidence u sing seedlings, and o f studies tha t directly investigatedl ight absorpt ion by anthocyanin and i t s development re la t ive to recognized processes ofpho topro tection support the hyp othes is that anthocyanins prov ide protection from visible light.

I I In t roduc t ion

A n t h o c y a n i n s ~ r e e kanthos (flower) andkyanos (dark b lue )~a re colored p igments tha tgiv e flowers their characteristic red, purple, an d blue hues. Less recog nized is the occu rrenc eo f antho cya nins in fruits, stems, and leaves. T he first section o f this rev iew considers the eco -physiolog ical role o f anthocyanin accum ulat ion in leaves that is associated with on togenetic(expanding and senescing leaves), abiotic (nutrient deficie ncy and UV light) and bio tic (her-bivo ry and pa thogen infection) effects . In the sec ond sect ion, the hypothesis that anthocyan incan prov ide a photoprotective role is developed in the context o f evidence for i ts function as an

antioxidant, its distribution in leaves, and its synthesis in seedlings. The various studies thatprovide direct evidence for its role in light attenuation are examined.

I lL A n t h o c y a n i n A c c u m u l a t i o n

A ccu m ulatio n of anthoeyanin is defined as an increase in foliar an thocy anin concentrationthat leads to increased absolute anthocyanin content. This can be consistently attributed to arelatively small range o f contexts. A nth oc yan in accumulation is often observe d in expandingfoliage. S uch foliag e is no t photostable beca use levels o f light utilization and its capa city todissipate excess e nerg y are low, creating a relatively high risk o f photodamage. An tho cya nin isalso clos ely associated with the co lors in the autumn foliage of deciduous species. V irtually allsuc h species exhibit visu ally striking anthocyan ins, tho ug h also carotenoids, d uring this stageo f leaf ontogeny. A ccu m ulation o f antho cyan in is also associated with m acronutrient deficien-cies, particularly with intensively m anag ed agricultural, horticultural, or forest prod uction w herethe nutrients con tained in pro du ce are remo ve d from the system and replaced th roug h fertilizerapplication. R esearch investigating the potential effects o f atmosph eric o zo ne depletion ha veindicated that exposure to increased levels of U V radiation induces the accumu lation o f foliaranthocyanin. Ac cum ulation of foliar anthocyanin m ay be linked to brows ing risk by herbivoresand to d efense against patho gen ic fungal infection.

A. EXPANDINGLEAVES

Photostability o f leaves during lea f expansion, m easu red as resistance to degradation o f thepho tosyn thetic apparatus und er natural light, is attained o nly after a critical am ou nt of chloro-phy ll has accu m ulated (Drumm -Herrel Mohr, 1985). This accumulation is associated withthe dev elopm ent of leaf anatom y and structure and coincides with an increase in photosyn-thetic rate (Drum m-H errel Mo hr, 19 85 ). Photostability is usu ally attained gra du ally duringlea f expansion (Drumm -Herrel Moh r, 1985; Tu oh y Choinski, 1990; Choinski John son,1993; Choinski W ise, 1999), tho ug h delay ed until after full expansion in m any rain-forestplants (K ursar Coley, 1992; Nii et al., 1995; Do dd et al., 1998; W oodall et al., 1998; Ka rimet al., 199 9). A ntho cya nin has been associated with both gradual (Drumm -Herrel Mohr,1985) and delaye d (Dod d et al., 199 8; W oodall et al., 1998 ) chloroph yll accumulation duringleaf expansion. Drum m-H errel and Mo hr (1985) sh owe d that photostabil ity was l inked to an-thoc yan in prod uction and that its accum ulation in exp and ing leaves contributed to greater ph o-tostability in inapsis alba than in esamum indicumseedlings.


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FOLIAR ANTHOCYANIN 151

B. AUT UM N SENESCENCE

It has been suggested that anthocy anin screens senescing fol iage from high levels o f inci-dent light (Ho ch et al. , 2001), the reby red ucing the potential for photoinhibition. This createsan env ironm ent for the efficient res orption o f foliar nutrients durin g a period o f restrictedpho topro tective capacity. Sp ecies at risk of photoinhibition durin g leaf senescence, such as latesuccessional species o r those occu rring in cold environments, are hyp othe sized to emp loy an-thoc yan in synthesis as a m ech anism o f pho topro tection (Ho ch et al., 2001). In contrast, Matile(2000: 155 ) considered anthocya nin accum ulat ion to represent a kind o f extravaga ncy with-out a vital function . To support this argument, h e contends that levels o f anth ocy anin acc um u-lation var y betw een yea rs, betw een individuals within a species, and within individuals andthat senescence in som e species---e.g., in copp er varieties o f bee chFa gus sylvatica)and h azelCorylus eornuta)-- ispreceded by the loss o f anthocyanin (Matile, 2000).

C. NUTRITION

Nutrient, and particularly nitrogen (N), deficits detrimentally affect ph otosy nthe tic functionand eff iciency and decrease the levels o f Calvin Cy cle enzym es (Terashima & E vans, 1988;Sugiharto et al ., 1990). This co m m on ly induce s or enha nces the accu m ulat ion o f fol iar antho-cyanin in leaves o f m any plant species (Ni tt le r & Kenny, 1976; Ho dges & Noz zol i l lo , 1996;K um ar & Shann a, 1999; Close e t a l. , 2000 , 2001 a , 2000b). H igher concent ra t ions of antho-cyan in in sheaths and lea f blades, t issues o f low er photosy nthetic com pete nce than leaves,occurred in N-def ic ient than N-suff ic ientZ e a m a y s(Law anso n et al. , 1975). Bon gue-B artels-m an and Phill ips (1995) dem onstrated that N stress pro duc es effects on expression o f gen es

encoding enzym es associa ted wi th anthocyanin b iosynthes is . Pho sphorus (P) def ic it, wh ichrestr icts pho spha te levels essential to energ y m etabo lism (Salisbury & R oss, 1992), increasedanthocyanin content in a range o f mo noc otyledo nou s and d icoty ledono us p lants (Atkinson,1973). M axim um levels of anthocyanin accum ula t ion in Zmays occurred af ter 5 days underpotass ium (K) def ic iency (K def ic i t impai rs photosynthet ic enzyme funct ion; Bhandal &M alik, 1988), 10 day s und er P deficiency, and 15 day s under N d eficienc y (La wa nso n et al. ,1972).

D. ULTRAVIOLETLIGHT

Expo sure to ultraviolet (UV ) l ight prom otes the produc tion of fol iar a nthocyanin (Lindo o& Caldwell , 1978), and i t has been hypothesized that anthocy anin provides a UV sunscreen(Lee & Low ry, 1980). An thocy anin isolated from juvenile fol iageofSyzgium luehmanniiandS. wilsoniicontributed little to the total absorbance o f U V -A an d UV -B radiation (Woodall &Stewart, 1998), with similar findings inZea mays(Begg s & W ellman, 1985) andLycopersiconesculentum (Brandt et al. , 19 95). The oc currence of anthocyan in in palisade an d/ o r spo ngym esop hy ll tissues o f m ost species investigated to date contradicts the theory that antho cyan inhas a UV -B filtering role (Gou ld & Q uinn, 1999; Lee & Collins, 2001).

Coleus blumeivar. Red W izard, wh ich was high in anthocyanin, had high er quantum y ieldand photosynthetic rate when ex posed to UV B and UV -C radiat ion than d idC. blumeivar.Green Rainbow, wh ich was low in anthocy anin: Each had similar chlorop hyll and carotenoidcharacteristics (Bu rger & Edwards, 199 6). Krause et al. (1999) hav e shown, u sing filters thatseparately absorb or transmit UV radiat ion, that photoche m ical eff iciency of t ropical rain-forest understory plants was increased when ei ther UV A or UV-B radiat ion was excluded.This was particularly evident in shade leaves exposed to full sunlight. Moreover,Pinguicula


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IV Anthocyanin and Photoprotec t ion

Three well-characterized mechanisms, the xantho phy ll cyc le, antioxidant activity, and ex-ternal foliar waxes, contribute to photop rotection across plant species. The xa ntho phy ll cyc le isubiquitous in hig he r plants (Mtfller et al., 2001). In this cy cle , tw o carotenoids, zea andantheraxanthin, are epoxidized to a third, violaxanthin, and in so doing light energ y abso rbedin excess is harmlessly dissipated (De m m ig-A dam s A dam s, 1992). Antioxidants (e.g., glu-tathione, ascorbate, tocopherols) occur in plant cells and scavenge free radicals arising fromelectron leakage fro m photosynthesis (Niy ogi, 1999). Levels of free radicals increase wh en thecapa city to utilize or dissipate excess light en ergy is depressed, for example, un der conditionso f nutrient deficit or co ld-in du ced photoinhibition (Polle et al., 1992; Po lle Renn enberg,1996; Lo ga n et al., 1999). External foliar w ax es reflect light, thereby pro vid ing a photoprotectivefunction (Robinson et al., 1993; Ro binso n Os m ond , 1994; Bark er et al., 1997).

Patterns o f anthocyanin dev elopm ent across different families an d orders o f plants suggest

strong conv ergen ce, and it has been hypothesized that the sam e ph ysio logica l basis has led tothis conve rgence (Kursar Coley, 19 92). However, the ecoph ysiological role o f foliar antho-cyanin remains contentious. Le af color has been described as a by-p roduc t of the general me -tabolism of f lavonoids, the color being expressed through anthocyanin as one o f the by-produ cts(Lee et al., 198 7). Conversely, it has been argue d that anthocyanin has fo ur important func -tions, as a compatible solute contributing to osmotic adjustment to drought and frost stress(Chalker-Scott, 199 9), as an antioxidant (Rice -Eva ns et al., 1996; Yam asaki et al., 1996; W anget al., 199 7), as a U V protectant (Lee Lowry, 1980; Bu rger Edwards, 1996; Jay aku m ar etal., 1999), and as protection from visible light through light attenuation (Gould et al., 1995;K rol et al., 1995; Ba rke r et al., 1997; D od d et al., 1998; Pietrini M assacci, 1998; M en de z etal., 1999; Neill Gou ld, 199 9; C lose et al., 2001a). C urrently, its role in light attenuationattracts the most support.

A. OSMOTICADJUSTMENT

It has been a rgued that foliar anthocyanin co nfers cold and drou ght hardiness b y contributing toosm otic adjustment in lea f tissues (C halker-Scott, 1999). Circum stantial evidence, that cold-hardy(Kakegawa et al. , 198 7; Len g et al. , 1993; Foo t et al. , 1996; Oren-Shamir Levi-Nissim, 1997)and drought-hardy (Tuohy Choinski, 19 90 ; Choinski Johnson, 199 3; Ronchi et al. , 1997;Sherwin Fan'ant, 1998) tissues contain anthocyanin, has been presented (Chalker-Scott, 1999).How ever, this evidence d id not exclude the possibility that cold- or drought-induced photoinhibitionoccurred in these studies. Thus anthocyanins may have been synthesized for photoprotection inresponse to photoinhibition rather than osmotic adjustment. Foliar anthocyanin does not alwayscorrelate with frost hardiness (e.g., Nozz olillo et al., 1989; Toivonen et al., 19 91). Leaves o fE u c alyp tus n i t ensseedlings exposed to freezing temperatures but protected from high light by open-topped shade-cloth shelters had negligible anthocyanin content compared with exposed seedlings(Close et al . , 2001a, 2002). Chalker-Scott (1999) concludes that anthocyanin may providephotoprotection but also prevents ice nucleation and desiccation through osm otic effects. It is notclear how this mechanism m ay explain anthocyanin accum ulation under low but no t freezing tem-

peratures (Tan, 1979; Arm itage Carlson, 1 98 1; Cristie et al., 1994 ; B oo et al., 1997).

B. ANTIOXIDANTS

A nth ocy an in functions as an antioxidant in vitro (Rice-E van s et al. , 1996; Yamasaki et al. ,1996; Wan g et al., 1997) and, by implication, in viv o (Yam asaki, 1997). Yam asaki (199 7)


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154 THE BOTANICAL REVIEW

argued that the prod uction o f dam agin g reactive ox yg en intermediates, by high light intensityand/or abiot ic s tress, prov ided evidenc e for an antioxidant role o f anthocyanin in the fol iage o fstressed plants. However, in two field studies (Grace et al., 1998; Close et al., 2001a), seasonalvariation in anthoc yan in levels was not associated with variation o f foliar com po un ds o f pro-

posed antioxidant capacity.

C. LIGH TATTENUATION

1 I n t e r n a l L e a f D i s t ri b u ti o n

An thocya nin is widely distributed in the palisade and/or spon gy mesoph yll cel ls o f m anyplant species (G ou ld & Quirm, 1 999; Le e & Collins, 2001). It abso rbs light between ca. 400and 60 0 nm (Pietrini & Massacci, 1998; Clo se et al., 2001a). This suggests that anthocyaninscan act to screen visible light. Sun et al. (1998) have sh ow n that green light can drive ca rbonfixation below the pal isade layer, where the sp ong y mesophy ll can contr ibute as mu ch as 40%o f carb on dioxide carbo xylation (Nishio et al. , 1993). Chloroplasts in outer leaf layers are welladapted to excess light absorption throu gh the activity o f the xanthophyll cyc le (e.g., Dem m ig-Ad am s & Adam s, 1992). Sudden chang es in levels o f incident l igh t--fo r example, sun f lecksthrough an o ve rsto ry- -ca n induce excess l ight absorption that requires pho toprotect ion via thexanthophylls cy cle (Lo gan et al., 1997; Thiele et al. , 1998 ). Shade-adapted chloroplasts o f lowchlorophyll a:b ratio may require photoprotection via anthocyanin during sun-fleck events toensure tha t they fix significant amounts o f carb on (G ould et al., 2000).

Du ring leaf expansion (Lee & L ow ry, 1980; Tu ohy & Choinski, 1990; Choinski & Joh nson,1993; Woodall et al., 1998), during senescence (Matile et al., 1992; Feild et al., 2001), and in

respo nse to abiotic stress (Tevini et al. , 1991; Krol et al. , 1995; Bu rger & Edwards, 1996; Closeet al., 2001 a, 2002), leaves syn thesize a nth oc ya nin in, or imm ediately b elow, epidermal layers.Th e requirement for photoprotection is large if the leaves are expo sed to high light conditions;this is consistent with anth ocy anin provid ing a photoprotective role.

2 S e e d l i n g s

Seedlings provide a mo del system for investigat ion o f the e cophy siological role o f antho-cyanin becau se yo un g leaves hav e an inherently low cap acity for l ight uti lization due to lowlevels o f chloro phy ll (Krause et al. , 1995; B arker et al., 1997; Do dd et al., 1998; Close et al.,

200 0, 2001b). Seedlings are also less adapted to abiotic stress su ch as frost- an d cold-inducedphotoinhibition associated with radiative c oo ling (Jordan & Sm ith, 19 95) and cold -air stratifi-catio n (Jordan & Sm ith, 19 94 ), drought, an d waterlogging (Burdett, 1990; Close, 2001). Seed-lings suffer transplant sh oc k du ring acclimation to ne w field environm ents (Sp unda et al.,1993; M oh am m ed & Parker, 1999; Close et al., 2000). Th us leaves of seedlings are oftenexp osed to conditions that require m ax im um photoprotective effort.

Anthocy anin content inPinus banksianawa s twofold greater in seedlings expo sed to 5~com pared with 15~ and in high l ight com pared with low light und er similar temperatureconditions (No zzollilo et al. , 1989 ). An tho cya nin coloration wa s linked to nutrient d eficit un-der low-temperature and high -light conditions in P.sylvestris(Toivonen et al. , 19 91). A nth o-cya nin conten t w as no t linked to photoinhibition or photop rotection in either o f these studies.Ho we ver, Krol et al. (1995) sho we d that the prod uction o f foliar antho cya nin is correlated withtolerance o f photoinhibition in seedlings o fP banksianaand proposed tha t an thocyanin canredu ce sensitivity to cold-indu ced photoinhibition. The re w as a two fold difference in qua ntumyield o f oxyg en evolution and in photoche mical eff iciency after t ransfer o f seedlings from a


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FOL IAR ANTHOCY ANIN 155

, l / . 5

, : ',, . . t :9 . - '~ . 5

~ 1 0

.~ - - ~ - - - ~ - - - 1- 0 .5

[ e - , ' ~ ' I ' ' 4 I I I I I I I o

9 14 16 18 21 24 27 30 35

Day o f l ea f deve lopment

Fig. 1. O verall reflectance of incident light from 400 to 700 nm ( leaf reflectance, ), an estimate ofrelative wax d evelopm ent ( /2) (wa x developm ent), and anthocyan in content (relative absorption at 530nm per gram leaf fresh weight) of developingCotyledon orbiculataleaves.Source:Adapted from Barkeret al., 1997.

20~ environ me nt to a 5~ environ me nt (Kro l et a l . , 1995). Photoin hibi t ion indu ced by nutr i -en t def ic i t was l inked to the dev elopm ent of fo l ia r an thocyanin in seedl ings ofEucalyptusnitens (Close e t a l . , 2001a) . Anthocyanin synthes is and breakdown were a l so l inked to thesever i ty of co ld- induced photo inhib i tion in seedl ings ofE nitensand E globulussoon af terthey w ere t ransp lanted from the nurse ry to the f ield (Close et a l ., 2000). This asso ciat ion be-tween an thocyanin content and the sever i ty of photo inhib i t ion was s imi la r ly demo nst ra ted us-i n g s h a d e - c l o t h s h e l t e r s , w h e r e t h e i r s u b s e q u e n t r e m o v a l i n d u c e d p h o t o i n h i b i t i o n a n danthocy anin synthesis (Close et a l . , 2002). Such repo rts s t rongly implica te synthesis of fol iaran thocyanin as a m echanism of photopro tec tion .

3 Doe s Light Absorp t ion by Anthocyanin Provide Photopro tec t ion?

Go uld e t a l . (1995) have a rgued tha t an thocyanin-conta in ing m esophyl l ce l l s pro tec t shade-adapted ch loroplast s deep w i th in the lea f as they absorb wavelengths be tween 500 and 600 nmthat over lap tha t o f ch lorophyl l b . Subsequent s tud ies have suppor ted th i s hypothes is . Youngleaves o f t he CA M p lan tCotyledon orbiculatad id no t deve lop dense ep ide rma l wax un t il 21 -24 days of deve lopment , a f te r which leaves re flec ted c lose to 60 of inc ident l igh t (F ig . 1 )(Barker e t a l . , 1997). Pr ior to day 24 , xan thophyl l -cyc le p igments p er un i t ch lorophy l l were a tthe i r h ighes t (da ta not shown) . Low ref lec tance ( ind ica tive of l igh t a ttenuation) was assoc ia tedwi th h igh leve ls of fo l ia r an thocyanin (F ig . 1 ). Thus , photopro tec t ive s t ra teg ies of deve loping


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p h y l l s, a n t io x i d a n t s , a n d e p i d e r m a l w a x e s . T h e s e l i m i t a ti o n s m a y b e o v e r c o m e t h r o u g h t h e u s eo f m u t a n t s t h a t ar e u n a b l e t o s y n t h e s i z e a n t h o c y a n i n . Wo r k o n g e n e s t h a t s i g n a l a n t h o c y a n i na c c u m u l a t i o n h a s l a r g el y b e e n l a c k in g , p a r t i c u la r l y i n t h e c o n t e x t o f e c o p h y s i o l o g i c a l i n v e s t i-g a t io n s . T h u s , a n a l o g o u s t o s t u d ie s o f t h e x a n t h o p h y l l c y c le a n d p h o t o p r o t e c t i o n i n m u t a n t s , i t

m a y b e p o s s i b l e to u n e q u i v o c a l l y d e m o n s t r a t e t h a t t h e e c o p h y s i o l o g i c a l r o le o f a n t h o c y a n i n isp h o t o p r o t e c t i o n .

V I . A c k n o w l e d g m e n t s

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