apoplast as the site of response to environmental signals

8/22/2019 Apoplast as the Site of Response to Environmental Signals

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J. Plant Res. 111: 167-177, 1998 Journal of Plant Rese arch@ by The Botanical Society of Japan 1998J P R S y m p o s i u m

poplast as the Si te of Response toEnvironmental SignalsT a k a y u k i H o s o nDep ar tment o f B io logy Facu l ty o f Sc ience Osa ka C i ty Un i vers it y Sum iyosh i - ku Osaka 55 8-8 585 Japan

When the l i fe cyc le of plants is inf luenced by var iousenvironm ental signals th e mechanical propert ies of the cel lwa l l a re great ly changed. The se s igna ls a lso modi fy thelevels and structure of the cel l wal l const ituents and suchmodi f ica t ions are supposed to be the cause of the changesin the wall mechanica l properties . The se chang es in thece l l wa l l th e major comp onen t of the apoplast can berecognized as the response of plants to env i ronmenta ls ignals~ T he ana lysis of the mechanism leading to theresponse suggests that the apoplast is involved not only inthe response but a lso in the p erception and t ransducUon ofenvironmental signals in concert with the receptors ofs igna ls located on the plasma mem brane . Thus the apo-plast plays a principal role in the com mu nicat ion of plantswi th the outer world and enables the plants to adapt them~selves an d surv ive in the env i ronment ful l of s t resses .

Key wo rds: Ap op las t - - Ce ll wa l l m Env i ronmenta l s igna l- - G r a v i t y - - L i g h t - - W a t e r

P la n t s a r e s u b je c t e d t o a g r e a t v a r i e t y o f e n v i r o n m e n t a ls ignals such as l ight , gravi ty, water , and temperature.T h e s e s i g n a l s s t r o n g l y m o d i f y t h e p r o c e s s e s o f g r o w t h a n ddeve lopm ent , by wh ich they con t ro l the l i fe cyc le o f p lan ts .T h e p l a n t c e l l i s e n c l o s e d w i t h t h e a p o p la s t , c o n s i s ti n g o f t h ece l l wa l l and the in te rce llu la r space . Thus , the apop las t i sa f ron t ie r where the p lan t ce l l f i r s t meets d i f fe ren t t ypes o fs igna ls . For the p lan t body , the ou te r ep iderma l ce l l wa l ls e r v e s a s t h e f ro n t ie r b e t we e n t h e o u t e r e n v i r o n m e n t a n d t h eplant i tse l f .

P l a n t s h a v e t h e c a p a c i t y o f r e s p o n d in g t o v a r i o u s e n v i ro n -me nta l s igna ls . Th e seq uen ce o f eve n ts lead ing to the f ina lreac t ion cons is ts o f s igna l pe rcep t ion , t ransdu c t ion t rans-m iss ion) , and response . I t has been sugge s ted tha t theapop las t i s invo lved in the percep t ion o f va r ious s igna ls inc o o p e r a t i o n w i t h t h e p l a s m a m e m b r a n e. So m e s i g n a l s m a yp a s s t h r o u g h t h e a p o p la s t a n d b e p e r c e i v e d i n th e s y m p las t.However , m uch o f t rans fo rmed s igna ls w i ll then be t rans-duce d ba ck to the apop las t . In such a way , in fo rmat iond e r i v e d f r o m t h e e n v i r o n m e n t a l s i g n a l s t e n d s t o a c c u m u la t ein the apop las t . The ap op las t , fina ll y , respon ds to thet ransd uced s igna ls in d ive rse ways . So fa r, the p r inc ipa lr o le o f t h e a p o p la s t a s t h e s i t e o f r e s p o n s e t o e n v i r o n m e n t a ls igna ls has no t been recogn ized c learly . In the p resen t

a r t i c le , we w i l l summar ize the responses o f the apop las t tol igh t , g rav it y , subm ergen ce wate r -logg ing) , wa te r -de f ic ie ncy ,a n d o t h e r s i g n a l s a n d d i s c u s s t h e p o s s i b l e m e c h a n i s m s b ywh i c h s u c h r e s p o n s e s a r e i n d u c e d .

Response of the Apoplast to Env i ronmenta l S igna lsWh e n p l a n t s a r e s u b je c t e d t o v a r i o u s e n v i r o n m e n t a l s i g -

na ls , the mechan ica l p roper t ies o f the ce l l wa l l , the ma jo rc o m p o n e n t o f t h e a p o p la s t , a r e g r e a t ly m o d if ie d . Ch a n g e sin the leve ls and s t ruc tu re o f the ce l l wa l l cons t i tuen ts , wh ichappear to under l ie the mod i f i ca t ion o f the mechan ica l p rop , -er t ies, have also been repor ted.L i g h tL ig h t i s o n e o f t h e m o s t im p o r t a n t e n v i r o n m e n t a l s i g n a l s i nregu la t ing p lan t g rowth and deve lopm ent . W hen e t io la tedseed l ings a re exposed to l igh t , e longa t ion g rowth o f s tems isim m e d ia t e l y in h ib i te d . T h e d e c r e a s e i n t h e c a p a c i t y o f t h ec e l l wa l l t o e x t e n d u p o n l ig h t e x p o s u r e h a s b e e n d e t e c t e d i nd i v e r s e s p e c ie s o f p l a n t s b y v a r i o u s m e t h o d s s u c h a s t h eI ns tr o n t e c h n iq u e M a s u d a et a l . 1970), i n v i t ro s t r e s s - r e l a x a -t i o n M a s u d a e t a l . 1981, M iya mo to e t a l . 1 9 9 2 , T a n et a l . 1992,Parvez et a l . 1996), i n v i vo s t ress - re laxa t ion K ige l andC o s g r o v e 1 9 9 1 ), a n d t h e s t r a i n / s t r e s s m e a s u r e m e n tM iy a m o t o et a l . 1 9 9 2 , T a n e t a / . 1992, Parvez et a l . 1996).

G r o w in g s t e m s a r e c o m p o s e d o f t h i c k , i n e x t e n s i b l e e p i d e r -m i s a n d e x t e n s i b l e i n n e r ti ss u e s, a n d a u x i n i n d u c e s e l o n g a -t i o n o f s t e m s e g m e n t s b y c a u s i n g a l o o s e n in g o f t h e o u t e re p id e rm a l wa l l T a n im o t o a n d M a s u d a 1 9 7 1 , Ku t s c h e r a1989a , Ma sud a 1990 , Hoson 1993) . In pea ep ico ty ls , l igh td e c r e a s e d t h e e x t e n s i b i l i t y o f t h e c e l l wa l l o f i n n e r t i s s u e sM iy a m o t o et a l . 1 9 9 2 ) b u t n o t i n th e e p i d e r m a l wa l l M a s u d a

et a l . 1 9 8 1 ). O n t h e o t h e r h an d , p h y t o c h r o m e m e d ia t e s t h edecre ase in the wa l l ex tens ib i l it y in r i ce co leop t i les Ma sudaet a l . 1970 ) . Bo th b lue and red l igh t a re invo lved in mod i f i-ca t ions o f the m echa n ica l p ropert ies o f the ce l l wa l l in peaep ico ty ls , o f wh ich b lue l igh t e f fec t i s fas t bu t t rans ien t K ige land Cosgrove 1991) .

L igh t causes mod i f i ca t ions o f the leve ls and s t ruc tu re o ft h e c e l l wa l l c o n s t i tu e n t s , wh i c h a p p e a r s t o b e r e l a t e d to t h el igh t - indu ced decre ase in the wa l l ex tens ib i l i ty Tab le 1 ). Inpea ep ico ty ls , l igh t caus ed a th icken in g o f the ce l l wa l l byincreas ing the leve ls o f bo th ce l lu lose and mat r ix po lysac-c h a r i d e s M a s u d a et a l . 1981) . Neu t ra l suga r com pos i t ion o f


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68 T . H o s o n

Table 1. Ch an ge s n the properties of cel l wal l constituents induced by environmen tal signalsChange Signal

Level of cel lulose~Increase

Decrease

Level of matrix polysaccharideeIncreaseDecrease

Composition of matrix polysaccharideModified

Molecular mass of matrix polysaccharideIncreaseDecrease

Breakdow n of m ab'ix polysaccharideStimulatedSuppressed

Level of monophenolIncreaseDecrease

Level of l igninIncreaseDecrease

Profi le of cel l wal l proteinModified

Level of extensinIncreaseDecrease

Level of expansinIncrease

Level of peroxidaseIncrease

Leve l o f /%glucana seIncreaseDecrease

Level of ~-galactos idaseDecrease

Level of xyloglucan hydrolase/endotraneferaseDecrease

Level of endo-xyloglucen transferaseIncreaseDecrease

Light (Masuda e t a l . 1981, Parvez 1997), Hypergravity (Waldron and Brett 1990, Kasah arae t a L 1995, Hoso n e t a l . 1996), A luminum (Hoa e t a l . 1994)Microgravity (Nedukha 1996), Submergence (Zarra and Masuda 1979, Tan e t a L 1 9 9 1 ,Masuda e t a l . 1994a, b, Azuma e t a l . 1996), Water-deficiency (Sakurai e t a l . 1987a, Irakie t a L 1989, Mu5oz e t a l . 1993a, Zhong and I_&uchli 1993, Wakabayash i e t a l . 1997b, c, d)Light (Masuda e t a l . 1 9 8 1 , Parvez 1997), Hypergravity (Waldron and Brett 1990, Kasah arae t a l . 1995, Haso n e t a l . 1996), Aluminum (Hca e t a l . 1994)Submergence (Zarra and Masuda 1979, Tan e t a l . 1991, Masuda e t a l . 1994a, b, Azum a e ta l . 1996), Water-deficiency (Sakurai e t a l . 1987a, Muhoz e t a l . 1993a, W akabayashi e t a l .1997c)Light (Masuda e t a l . 1981), Hyp ergra vity (VValdronand Brett 1990), Subm ergence (Zarra andMasuda 1979, Sauter and Kende 1992, Azuma e t a l . 1996), Water-deficiency (Sakurai e ta l . 1987b, Zwiaz ek 1991, Mufioz e t a l . 1993a, W akabayashi e t a l . 1997c)Light (Miyamoto e t a l . 1997), Water-deficiency (Wakaba yashi e t a l . 1997c)Subm ergence (Revi lla and Zarra 1987)Submergence (Chen e t a l . 1996)Water-deficiency (Zhong and L&uchi 1993), Hig h tempe rature (Labrador e t a l . 1 9 8 7Light (Tan e t a l . 1992, Miyamoto e t a l . 1994, Parvez e t a l . 1997)Submergence (Tan e t a l . 1991, Kutsche ra e t a l . 1993), Water-deficiency (Wakaba yashi e ta l . 1997b, d)Hypergravity (Waldron and Brett 1990, Ho son e t a l . 1996)Microgravity (Cowles e t a l . 1984), Subm ergence (Sauter and Kende 1992), Water-defi-ciency (Zwiazek 1991)Water-deficiency (Bozarth e t a l . 1987, Covarrubias e t a l . 1995)Low temperature (Weiser e t a l . 1990, Goodwin e t a l . 1996)Submergence (Hoson e t a l . 1980), Water-deficiency (Iraki e t a l . 1989)Subm ergence (Ch o and Kende 1997), Water-deficiency (Wu e t a l . 1996)Ligi t (Shinkle e t a l . 1992)Submergence (Chen e t a l . 1996)Light (Chen e t a l . 1998)Water-deficiency (Valero and Labrado r 1996), Low tem perature (Sawicka and Kacperska1994)Light (Mitani e t a l . unpubl ished)Darkness (Braam and Da vis 1990), Low temperature (Pol isensky and Braam 1996), Hightemperature (Braam 1992), Mecha nical stress (Xu e t a l . 1995)Water-deficiency (Pri tchard e t a l . 1993)

a Including changes in the rate of synthesis, b L evels of wal l-b oun d ferul ic and diferulic acids, c Including the expression of genesencoding the proteins.Levels of the cel l w al l consti tuents are expressed pe r organ, per zone, per un it length of organ , per dry weight, or per protein.


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A p o p l a s t R e s p o n d s t o E n v i r o n m e n t a l S i g n a l s ] 6 9t h e m a t r i x p o l y s a c c h a r i d e s wa s a l s o m o d i f i e d b y l i g h t e x p o -s u r e M a s u d a e t a l 1981) . Recent ly , i t wa s found tha t ligh ti n c r e a s e d th e m o le c u la r m a s s o f x y l o g l u c a n s M i y a m o t o e ta l 1 9 9 7 ) . T h e f in d i n g s a re n o te wo r th y , b e c a u s e x y l o g l u c a n sa r e t h e k e y c o m p o n e n t o f t h e c e l l wa l l a r c h i t e c t u re Ha y a s hi1 9 8 9 ) a n d t h e i r m o le c u la r m a s s i s o n e o f m a jo r f a c t o r sd e t e r m in in g t h e wa l l e x t e n s i b il i ty i n d i c o t y l e d o n s M a s u d a1990, Ho son 1991,1993). In re lat ion to th is resul t, i t w asr e p o r t e d t h a t t h e g e n e s u p p o s e d t o e n c o d e a n e n d o - x y l o g -lucan t rans fe rase , wh ich p lays an impo r tan t ro le in ce l l wa l lcons t ruc t ion N ish itan i 1995) , i s up- re gu la te d in express ionfo l lowing exp osure to darkn ess Braam and Dav is 1990).

T h e c o m p o s i t io n o f m a t r i x p o l y s a c c h a r i d e s i s d i f fe r e n tb e t we e n d i c o t y le d o n s a n d G r a m in e a e M c Ne i l e t a l 1984,M asu da 1990, Hoso n 1991,1993). In ma ize co leop t i les , l igh tcaused a la te ra l wa l l th icken ing by inc reas ing the leve ls o fb o t h c e l lu l o s e a n d m a t r i x p o l y s a c c h a r i d e s Pa r ve z e t a l1 9 9 7) , wh e r e a s s u c h a c h a n g e wa s n o t i n d u c e d b y l i g h t inr ice co leop t i les Tan e t a l 1992) . In add i t ion to thesep o l y s a c c h a r i d e s , t h e c e l l wa l l o f G r a m in e a e c o n t a i n s as i g n i f i c a n t a m o u n t o f m o n o p h e n o l s s u c h a s f e r u l i c a c i d s ,wh i c h a r e e s t e r - li n k e d t o t h e m a t r ix p o l y s a c c h a r i d e s Ha r tl e y1 9 7 3 ) . Wa l l - b o u n d f e r u l i c a c i d s u n d e r g o a p e r o x i d a s e -c a t a l y z e d c o u p l i n g t o p r o d u c e d i f e r u l i c a c i d , wh i c h c r o s s -l inks mat r ix po lyse ccha r ides F ry 1986). I t has been reportedtha t l igh t p rominen t ly inc reases the leve ls o f fe ru l i c andd i fe ru l ic ac ids in co leo p t i les o f r ice Tan e t a l 1992) , oa tM i y a m o t o e t a/ . 1994) , and ma ize Parvez e t a l 1997).

S ig n i f ic a n t c o r r e l a t io n s we r e o b s e r v e d b e t we e n t h e i n c r e a s ein fe ru l i c and d i fe ru l i c ac ids and the decrease in the ce l l wa l lextensib i li ty . L ight , howeve r, d id not incre ase the act iv i ty ofperox idase p resen t in the ce l l wa l l o f ma ize co leop t i lesParvez e t a l 1997) , a l though i ts ac t iv i t y inc reased in cuc um -

ber hypo co ty ls upon l igh t i rrad ia t ion Sh ink le e t a l 1992).I n s t e a d , t h e a c t i v i t y o f p h e n y la l a n i n a m m o n ia - l y a s e wa senh ance d up on l igh t ir rad ia tion in ma ize co leop t i les Parveze t a l 1997).G r a v i t y

Pla n t s h a v e e v o l v e d u n d e r t h e c o n s t a n t f o r c e o f g r a v i t ya n d t h u s g r a v i t y a l s o s t r o n g l y i n f l u e n c e s g r o w t h a n d d e v e l -opm ent o f p lan ts , espe c ia l l y tha t o f te rres tr ia l ones . In o rderto c la r i f y the ro le o f g rav i t y in regu la t ion o f p lan t l ife cyc le , i ti s e f fec t ive to rem ove the g rav i ta t iona l fo rce f rom p lan tg r o w t h c o n d i t i o n s a n d o b s e r v e t h e c h a n g e s b r o u g h t a b o u t .Ho we v e r , t h e o p p o r t u n i t y f o r e x p e r im e n t s i n s p a c e , wh i c hprov ides us w i th t rue m ic rograv i ty cond i t ions , i s l im i ted .Moreover , i t i s d i f f i cu l t on ear th to p roduc e a m ic rograv i tye n v i r o n m e n t f o r t h e d u r a t i o n e n o u g h t o i n d u c e o b v i o u scha nge s in g row th and deve lopm ent o f p lan ts . There fo re ,t h e c h a n g e s i n t h e m e c h a n i c a l p r o p e r t i e s o f t h e c e l l wa l lh a v e b e e n a n a l y z e d u n d e r t h e o p p o s i t e h y p e r g r a v i t y c o n d i -t ions , wh ich a re eas i ly p roduced on ear th by cen t r i fuga t ion .I n h y p o c o t y l s o f g a r d e n c r e s s , a c c e le r a t io n a t 1 3 5 g c a u s e da s u p p r e s s i o n o f e l o n g a t i o n g r o w t h a n d a l s o a d e c r e a s e i nt h e c a p a c i t y o f t h e c e l l wa l l t o e x t e n d , a s e x a m in e d b y th es t r e s s r e l a x a t io n m e t h o d a n d t h e s t r a i n / s t r e s s m e a s u r e m e n tM a s u d a e t a l 1 9 9 4 a , Ho s o n e t a / 1996). I t wa s sugg es ted

t h a t s im i la r c h a n g e s o c c u r r e d i n g r a m in e o u s m a i z e s e e d l i n g sHarada e t a l 1997).

There a re severa l repor ts dea l ing w i th mod i f i ca t ions o f ce l lwa l l c o n s t i t u e n t s i n s p a c e Co w le s e t a l 1 9 8 4 , N e d u k h a1 9 9 6 ). T h e y o b s e r v e d t h e d e c r e a s e i n t h e a m o u n t o f c e l l u -lose and l ignin Table 1). Th e results, however, are f rag-m e n t a l a n d n o t c o n c l u s i v e . O n th e o t h e r h a n d , h y p e r g r a v it yinc reased the leve ls o f ce l lu lose Wald ron and Bre t t 1990 ,K a s a h a r a e t a l 1 9 9 5 , Ho s o n e t a/ . 1996) , mat r ix po lysa ccha r -ides Wald ron and B re t t 1990 , Kas ehara e t a l 1995, Hoson e ta l 1996) , and l ign in Wald ron an d B re t t 1990 , Hoso n e t a l1996) in va r ious mater ia ls Tab le 1 ). Ch ange s in sugar com -p o s i t i o n o f m a t r i x p o l y s a c c h a r i d e s a r e a l s o d e t e c t e d i n p e ae p i c o t y l s Wa ld ro n a n d B r e t t 1 9 9 0 ) . Su c h c h a n g e s i n t h el e v e l s a n d c o m p o s i t i o n o f t h e wa l l c o n s t i t u e n t s m a y b ea s s o c ia t e d w i t h m o d i f ic a t i o n s o f t h e m e c h a n i c a l p r op e rt ie so f the ce l l wa l l by hypergrav i ty .

Un d e r m i c r o g r a v i ty c o n d i t io n s s im u la t e d b y a t h r e e - d im e n -s i o n a l c l i n o s t a t , p l a n t o r g a n s s h o w s p o n t a n e o u s c u r v a t u r e sHoson e t a l 1 9 9 2 , Ho s o n e t a l 1 9 9 7 a ) . Wh e n t h e c e l l wa l le x t e n s i b i l i t y o f wh o le o r g a n s wa s m e a s u r e d , n o c h a n g e s

we r e b r o u g h t a b o u t b y t h e c l in o s t a t r o ta t io n M a s u d a e t a l1994a, b ). However , in ma ize shoo ts the conv ex s ide exp an-d ing fas te r exh ib i ted a h igher ex tens ib i l i t y o f the ce l l wa l lt h a n t h e o p p o s i t e s i d e , a n d t h i s a p p e a r e d t o b e a c a u s e o fs u c h a u t o m o r p h i c c u r v a t u r e s Ho s o n 1 9 9 4 , Ho s o n e t a l1 9 9 5 a ) . Ch e m ic a l a n a l y s is o f t h e c e l l wa l l c o n s t i t u e n t s a n dt h e m e a s u r e m e n t o f e n z y m ic a c t i v i t i e s i n t h e c e l l wa l lr e v e a le d t h a t e i th e r th e b r e a k d o wn o r t h e a c c u m u la t i o n o fcer ta in wa l l po lysecc har ides , esp ec ia l l y 1 - - ,3 ) 1 - - ,4 ) -/~-g l u c a n s w h i c h a r e t h e m a jo r p o l y s a c c h a r i d e s d e t e r m in i n gthe mechan ica l p roper t ies o f the ce l l wa l l in GramineaeMa suda 19 90, Sak ura i 1991), wa s invo lved in the s pon tane-

o u s c u r v a t u r e s Ho s o n e t a/. 1995b, 199 7b). Simi lar ly, t hee x t e n s i b i l i t y o f t h e c e l l wa l l o f t h e c o n v e x s i d e wa s h i g h e rt h a n t h a t o f t h e c o n c a v e s i d e i n g r a v i - s t im u la t e d s t e m sSh e n -M iUe r a n d M a s u d a 1 9 7 3 , I wa m i a n d M a s u d a 1 9 7 4 ,

Co s g r o v e 1 9 9 0 , Ba g s h a w a n d C le la n d 1 9 9 0 ) a n d c o r r e s p o n d -ing d i ffe ren t ia l mo d i f i ca t ions o f the ce l l wa l l metabo l ism havebee n repor ted in gravi t ropism Gibe aut e t a/ . 1990 , Ta lbo t ta n d P i c k a r d 1 9 9 4 , M o n t a g u e 1 9 9 5 , Ed e lm a n n a n d S ie v e r s1995).S u b m e r g e n c e

Land p lan ts , in genera l , a re no t ab le to surv ive underwa t e r . Ho we v e r, a g r o u p o f a q u a t i c o r s e m i - a q u a t i c p l a n t ss u c h a s r i c e c a n g r o w u n d e r c o n d i t i o n o f s u b m e r g e n c e f o r along per iod . Ac tua l ly , r ice co leop t i les g row fas te r unde rwa t e r t h a n i n a i r Wa d a 1 9 6 1 , M a s u d a e t a l 1 9 9 8 ) . A i r -b u b b l i n g p a r t i a ll y s u p p r e s s e s c o l e o p t i le g r o w t h u n d e r wa t e rZ a r r a a n d M a s u d a 1 9 7 9 , M a s u d a e t a / 1994a, b ) , sugge s t ing

t h a t t h e s t im u la t io n o f g r o w t h u n d e r wa t e r i s c a u s e d b y b o t hgase ous fac to rs Ish izawa and Esesh i 1984) and m ic rog rav i tye f f e c t d u e t o b u o y a n c y M a s u d a e t a /. 1 9 9 4 a, b) . T h erheo log ica l ana lys is o f the ce l l wa l l p roper t ies o f r i cec o le o p t i l e s s h o we d t h a t t h e e x t e n s i b i l i t y o f t h e c e l l wa l l o fwa t e r - g r o wn c o l e o p t i l e s wa s h i g h e r t h a n t h a t o f a i r - g r o wno n e s Z a rr a a n d M a s u d a 1 9 7 9 , T a n e t a l 1991, Ma sud a e t a l


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] 7 0 T . H o s o n1 9 9 4 a , b , 1 9 9 8 ) . Wh e n r i c e s e e d l i n g s we r e g r o wn u n d e rwate r w i th a i r -bubb l ing , the ce l l wa l l ex tens ib i l i t y was in te r -m e d ia t e b e t we e n u n d e r wa t e r a n d i n a i r ( M a s u d a e t a l .1994a, b).

Su b m e r g e n c e c a u s e s d i v e r s e c h a n g e s i n t h e l e v e l s a n ds t r u c t u r e o f t h e c e l l wa l l c o n s t i t u e n t s o f r i c e c o l e o p t i l e s(Tab le 1 ). Th e leve ls o f ce l lu lose and ma t r ix po lysa ccha r -ides per un i t leng th in wate r -g rown co leop t i les were s ign i f i -c a n t l y l o we r th a n t h o s e i n a i r - g r o wn o n e s ( Z ar ra a n d M a s u d a1979, Tan e t a l . 1 9 9 1, M a s u d a e t a l . 1994a, b) . Th eir levelsi n c o l e o p t i le s g r o wn u n d e r wa t e r w i t h a i r -b u b b l i n g we r ein te rmed ia te (Tan e t a l . 1 9 9 1 , M a s u d a e t a l . 1994a, b ) .M o r e o v e r , t h e r a t e o f a c c u m u la t i o n o f b o t h p o l y s a c c h a r i d e sd e c r e a s e d wh e n r i c e c o l e o p t il e s g r o wn i n a i r we r e s u b m e r -g e d ( Ku t s c h e r a e t a / . 1 9 9 3 ) . T h e s u g a r c o m p o s i t io n a n d th em o le c u la r m a s s o f m a t r ix p o l y s e c c h a r i d e s s u c h a s ( 1 - . 3 ) ( 1 -*4 ) - / ~ - g l u c a n s a n d x y l o g l u c a n s we r e a l s o d i f f e r e n t b e t we e nc o le o p t i le s g r o wn u n d e r wa t e r a n d i n a i r ( Z ar ra a n d M a s u d a1979, Rev i l la and Z ar ra 1987). In re la t ion to th is resu lt , thea c t i v i ti e s o f ( 1 - .3 ) ( 1 - *4 ) - / ~ - g l u c a n - s p e c i f i c g l u c a n a s e s a n da u t o l y s is we r e h i g h e r in wa t e r - g r o wn c o l e o p t i l e s t h a n i n a i r -g r o wn o n e s ( Ch e n e t a / . 1 9 9 6 ) . S i g n i f ic a n t d i ff e r e n c e s we r ea l s o d e t e c t e d b e t we e n a i r - a n d wa t e r - g r o wn r i c e c o l e o p t i l e si n t h e l e v el s o f c e ll wa l l - b o u n d m o n o p h e n o l s a n d g l y c o -p ro te ins , wh ich a re supposed to p lay a ro le in c ross- l ink ingb e t we e n c e l l wa l l p o l y s e c c h a r i d e s a n d m a k e t h e c 6 11 wa l lm e c h a n i c a l l y r ig id . W a t e r - g r o wn r i c e c o l e o p t i l e s c o n t a i n e dlower leve ls o f fe ru l i c and d i fe ru l i c ac ids es te r - l inked tom a t r i x p o l y s e c c h a r i d e s t h a n t h o s e i n a i r ( T a n e t a l . 1991).The i r leve ls in co leop t i les g rown under wate r w i th a i r -bub-b l ing were in te rmed ia te (Tan e t a l . 1991) and those in a i r -g r o wn o n e s we r e d e c r e a s e d b y s u b m e r g e n c e ( Ku t s c h e r a e ta l . 1993 ) . A lso , the leve ls o f two typ es o f ce l l wa l l g lyco-p ro te ins , ex ten s ins and aspa rag ine - l inked ones , were loweri n wa t e r - g r o wn c o l e o p t i l e s t h a n i n a i r - g r o wn o n e s a n dc h a n g e d u p o n t r a n s f e r fr o m w a t e r t o a i r o r t h e r e v e rs et rans fe r (Hoson e t a / . 1980,1983).

Par t ia l submergence induces rap id e longa t ion o f in te r -node s in deep wa ter ri ce . Th is rap id e longa t ion appea rs tob e b r o u g h t a b o u t b y m a in t e n a n c e o f h i g h c e l l wa l l e x t e n -s ib il it y (Ku tsch era and Ke nde 198 8) . Th e ce l l wa l l o f rap id lye l o n g a t i n g i n t e r n o d e s s h o we d t h e l o we r l e v e l s o f c e l l u l o s ea n d m a t r i x p o l y s e c c h a r i d e s ( Az u m a e t a l . 1996) , mod i f iedc o m p o s i t io n o f m a t r i x ( Sa ut e r a n d Ke n d e 1 9 9 2 , Az u m a e t a l .1996) , lower leve l o f l ign in (Sau te r and Ke nde 1992) , anda c c u m u la t i o n o f e x p a n s in s (Ch o a n d Ke n d e 1 9 9 7 ) wh i c h a r ecapab le o f induc ing ex tens ion o f i so la ted and bo i led seg-m e n t s ( M c Q u e e n - M a s o n e t a l . 1 9 9 2 ) . T h e s e c h a n g e s i nce l l wa l l cons t i tuen ts may be invo lved in rap id e longa t ion o ft h e i n te r n o d e s u n d e r c o n d i t io n o f s u b m e r g e n c e . So m eo t h e r a q u a t i c p l a n t s s u c h a s R e g n i l l i d i u m a l s o s h o w r a p ide l o n g a t io n u n d e r wa t er , a n d t h e h i g h c a p a c i t y o f t h e c e l l wa l lt o e x t e n d a p p e a r s t o u n d e rl ie s u c h a s t im u la t io n o f e lo n g a -t i o n (s e e J a c k s o n 1 9 8 5 ) . Ho we v e r, t h e c h e m ic a l b a s i s f o rthe h igh wa l l ex tens ib i l i t y in these p lan ts has no t beenclarif ied.

W a t e r d e f i c i e n c yWh e n p l a n t s a re s u b je c t e d t o wa t e r - d e f i c i e n c y , t h e y s h o wa com plex response . In genera l, g row th o f s tem s andleaves is rap id ly suppressed , wh ereas th a t o f roo ts con t inuese v e n u n d e r s u c h c o n d i ti o n s . T h e c o n t i n u e d g r o w t h o f r o o t sa t low wate r po ten t ia l i s advan tageous to the p lan ts ,because roo ts a re requ i red to reach wate r fo r the i r su rv iva l .Un d e r wa t e r - d e f i c i t c o n d i t io n s , t h e c e l l wa l l o f r o o t s i sma in ta ined in a loosened cond i t ions ( I toh e t a / . 1 9 8 7 , W u e ta /. 1 9 9 6 ) . O n t h e o t h e r h a n d , m e a s u r e m e n t s o f t h e m e c h a n -ica l p roper t ies o f the ce l l wa l l o f wa te r -s t ressed s tems andleaves have p rodu ced co n t rad ic to ry resu l ts . In va r iousm a t e ri al s, t h e d e c r e a s e i n c a p a c i t y o f t h e c e l l wa l l to e x p a n dwa s b r o u g h t a b o u t b y wa t e r - d e f i c i e n c y ( No n am i a n d B o y e r1 9 9 0 , C r a m e r 1 9 9 2 , Ne u m a n n 1 9 9 3 , Ch a z e n a n d Ne u m a n n1 9 9 4) , wh i c h i s s u p p o s e d a s o n e o f c a u s e s o f g r o w t h s u p -press ion . On the con tra ry, there a re a lso repor ts tha t thec e l l wa l l o f s h o o t o r g a n s i s k e p t l o o s e n e d u n d e r wa t e r - d e f i c i tcon d i t ions a s in roo ts (Sakura i and K ura ish i 1988 , Neu man ne t a l . 1 9 8 8 , Ku t s c h e r a 1 9 8 9 b , Wa k a b a y a s h i e t a l . 1997a, b).T h e e f f e c t o f wa t e r s t r e s s o n t h e c e l l wa l l e x t e n s i b i l i t y m a yb e v a r i a b l e f o r s p e c i e s o r o r g a n s a s we l l a s f o r t h e c o n d i t i o n so f wa te r -de f ic ien cy , i .e . d ryness , osm ot ic , o r sa l in i ty . Thus ,a t l e a s t we c a n s a y t h a t u n d e r a c e r t a i n c o n d i t io n , t h e h i ghwa l l e x t e n s i b i li t y o f g ro w in g o r g a n s c a n b e m a in t a i n e d , e v e ni f g r o w t h i s s u p p r e s s e d b y wa t e r - d e f i c i e n c y . Su c h a m e c h -a n i s m a p p e a r s t o c o n t r i b u t e t o r a p id r e c o v e r y o f g r o w t h u p o nre l ie f o f wa te r -de f ic i t s t ress (Sakura i e t a l . 1987a, b , Ku ts -c h e r a 1 9 8 9 b , M u S o z e t a l . 1 9 9 3 b , Wa k a b a y a s h i e t a l . 1997a,b).

Va r i o u s r e s u lt s h a v e b e e n r e p o r te d o n t h e c h a n g e s i n t h eleve ls and s t ruc tu re o f the ce l l wa l l cons t i tuen ts in p lan tssub jec ted to wa te r -de f ic ien cy (Tab le 1 ). In wa te r -s t ress edroo ts , the decrease in the leve l o f ce l lu lose (Zhong andL uch l i 1993), the inh ib it ion o f degrada t ion o f m at r ix po lysa c-char ides (Zhong and I_ uch l i 1993) , and th e inc rease in theleve l o f and suscep t ib i l i t y to expans ins (Wu e t a l . 1 9 9 6 ) h a v eb e e n d e t e c t e d . T h e a c ti v i ty o f e n d o - x y l o g l u c a n tr a n s f e r a s edecre ased upon wate r -de f ic i t s t ress (Pr it chard e t a l . 1993).T h e d e c r e a s e i n t h e l e v e l s o f c e l l wa l l p o l y s e c c h a r i d e s a n dt h e c h a n g e s i n m a t r i x c o m p o s i t i o n d u e t o wa t e r - d e f i c i e n c ywere a lso observed in shoo t o rgans (Sakura i e t a / . 1987a, b,Z w ia z e k 1 9 91 , M u So z e t a / . 1 9 9 3 a, Wa k a b a y a s h i e t a l . 1997b,c , d ). Wa t e r d e f i c i e n c y c a u s e d t h e c h a n g e s i n a c t i v i ti e s o fc e r t a i n c e l l wa l l e n z y m e s a n d a u t o l y s i s ( M u So z e t a l . 1993b,Va le ro a nd Labrado r 1996) o r the p ro f ile o f ce l l wa l l p ro te ins(Bozar th e t a/ . 1987 , Cov ar rub ias e t a / . 1 9 9 5 ) i n L e g u m in o s a es tems. A lso , in wh eat co leop t i les the inc rease in the leve lso f c e l l wa l l - b o u n d f e r u li c a n d d i f e r u li c a c i d s wa s s u b s t a n t i a l -l y r e d u c e d b y o s m o t i c s t r e s s ( Wa k a b a y a s h i e t a / . 1997b, d).I t wa s s u g g e s t e d t h a t t h e d e c r e a s e i n a c t i v i t y o f p h e n y la la n i na m m o n ia - l y a s e wa s i n v o l v e d i n s u c h a r e d u c t i o n ( Wa -k a b a y a s h i e t a l . 1 9 9 7 b ) . T h e d e c r e a s e i n t h e l e v e l s o fc e l l u l o s e a n d s t r u c t u r a l c e l l wa l l g l y c o p r o t e i n s wa s a l s or e po r te d i n c u l t u re d t o b a c c o c e l l s a d a p t e d t o o s m o t i c s t re s s(Iraki e t a l . 1989).Roo ts o f te rres tr ia l p lan ts respon d to d i f fe renc es in mo is -t u r e g r a d ie n t b y g r o w in g t o wa r d s d i r e c t i o n o f g r e a t e r wa t e r


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Apop las t Responds to Env ironmenta l S igna ls ]7 ]potential, which is termed hy drotropism Takah ashi 1997).The differences in the cell wall extensibility between theconvex and the concave sides appeared to be a cause ofthe hydrotropic curvature of pea roots Hirasawa e t a l . 1997).The differential expression of the gene encoding an endo-xyloglucan transferase may be involved in the differences inthe cell wall extensibility of hydrotropically responding rootsTakahashi 1997).O t h e r s i g n a l sExcessive salin ity causes an inhibit ion of plant growth.Salts also influence the mechanical properties of the cellwall and the levels and structure of the wall constituents.These effects of sal in ity are recognized as a kind of osmoticstress as mentioned above. Of other metals or elements,aluminum increased the lev els of cel lu lose and matrixpolysaccharides when it inhibited squash root growth Hoa e tal. 1994). Sil ica is known to accumulate in the cell wall ofGramineae. It showed an effect to m ake the cell wall ofrice coleoptiles and wheat leaves mec hanically rigid unpub -l ished data). Heavy metals such as cadmium and si lver alsoinfluence the m echanical properties of the cell wall Inouheand Tanimoto, personal communication).Plant growth is active within the range of optimal tempera-ture but suppressed at low er or higher tem peratu re. Theincrease in cell wall strength during cold acclimation hasbeen reported in several plant tissues Rajashe kar and Lafta1996). Low temperature also decreased the activ ity of somewall enzymes Sawicka and Kacperska 1994), while i t in-creased the level of extensins Weiser e t a/. 1990, Goodwine t a l . 1996). The gene encoding an endo-xyloglucan trans-ferase wa s up-regulated in expression following cold treat-ment Polisensky and Braam 1996). On the other hand, hightemperature suppressed the degradation of matrix polysac-charides in germinating chic k-pe a stems Labrador e t a l .1987). The expression of the gene encoding an endo-xyloglucan transferase was enhanced by heat shoc k Braam1992).Plants are capable of responding to mechanical st imulisuch as touch, wind, and ra in Biddington 1986, Bra am andDavis 1990). Plant response induced by physical conta ct istermed thigmom orphoge nesis Jaffe 1973). In mech anicallystimulated plan ts, growth of stem s, leav es, and roots isreduced Jaffe 1973, Biddington 1986). Mechanical c ontactalso make s the cell wall mechan ically rigid Jaffe e t a l . 1984).It has been reported that touch and other mechanical s ignalsinduce a set of genes called the touch genes Braam andDav is 1990, Braam e t a l . 1996,1997). One of these genes,T C H 4 is supposed to encode an endo-xyloglucan transfer-ase and appears to play a role in the cell wall reinforcementas the response to mechanical st imuli Xu e t a / . 1995, Braame t a l . 1996,1997).

M e c h a n i s m s e a d in g t o t h e R e s p o n s eThe apoplast responds to various environmental s ignals ind iverse wa ys, as ment ioned ab ove . Before the f ina lresponse is induced, plant must perceive such stimuli, trans-

form the signals, and transduce or transmit them to the siteof reaction. It has been suggested that the apoplast isinvolved not only in the response but also in the perceptionand transduction of environmental signals in concert with theplasma mem brane. The mechanism by which the responseof the apoplast to environmental signals is brought about issum marized in Fig. 1.The mechanoreceptors are supposed to be located on theplasma membrane of plan ts. The nature of mechanorece-ptors has been mainly studied with carnivorous plantsSibaoka 1991) and characean cells Sh imm en 1997).Recently, a wide-spread presence of such receptors inplants is becom ing apparent Cosg rove and Hed rich 1991,Ding and Pickard 1993, Bogre e t a / . 1996). The receptorsact on the perception of mechanical s ignals such as pres-sure and tension, and so, they should be involved in thesensing of gravity. Because buoyancy under water greatlyreduces a tension applied to the plasma m em bran e bygravity, the signal of submergence may also be perceived b ythe mechanoreceptors. On the other hand , wate r-defi-c iency could induce the changes in the osmotic potential ofthe apoplast, thereby affecting the action of these receptors.Moreover, temperature signals also m ight indirectly be se n-sed by these receptors, because h igh or low temperatureinfluences the integrity of the plasma membrane Burke andOrzech 1988, Hughes and Du nn 1996, Nishida and Murata1996). It has been proposed that photoreceptors are locat-ed on the plasma mem brane Short and Briggs 1994, Hager1996, Nishizaki 1996). Phosp horylation of proteins localizedto the plasma m em brane appears to be involved in theperception of l ight s ignals Reymond e t a l . 1992, Kaufman1993, Short and Briggs 1994, Ha ger 1996). Thus, variousenvironmental s ignals can be perceived on the plasmamembrane, the boundary between the apoplast and thesymplast.The signals perceived by receptors on the plasma mem-brane then appear to be transformed as the changes in theactivities of ion channe ls Fig. 1). In som e cases, receptorsthemselves may act as ion channels. The presence ofmechanosensit ive channels in the plant membrane has beenreported in plants Morris 1990, Cosgro ve and H edr ich 1991,Shimmen 1997). Such channels could include stretch-activated type, whose universal presence and principal rolein signal transduction have been studied in detail in animalcells Dun can 1997). A typical example of mechanosen-sitive ion channe ls is calcium channels Cosg rove andHedrich 1991, Ding and Pickard 1993, Polisensky and Braam1996, Shim me n 1997). The receptors of s ignals are alsosupposed to control indirectly the activ ity of other ion chan-nels. Furthermore, the activ ity of the electrogenic protonpump is controlled by environmental s ignals v ia the mem bra-nous receptors Spalding and Cosgrov e 1992, Nishizaki 1996).The changes in the activ it ies of ion channels and protonpumps greatly modify the environment of the apoplast. Ingeneral, the modifications of the cell wall structure aremediated by cell wall enzy m es. The activ ity of theseenzymes in the cell wall i n s i t u is determ ined not only by theirlevels but by the apoplast environment Hoson 1993). Thus,


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172 T. Hoson

Fig. 1.

Environmental s i g n a l sl ~ o h t , . / r a v i t y , w a t e r , e t c . )

/ ~ ~ ch a n n e l s /~/ 9 . ~ ~.Apo p lae t .9 / /A : ) ~ - H+ r envl r~

v~i~iiiiiiiiii:;iiii~" (H o rm o ne ? )~::~:~ G e n e I ~ - -~ - e l l u l o s e -~express,on ~, ~ ~ synthase1 I I C ~ 1 7 6 ' ~i i M components-- ~ :;~ii ii i atrix /~ '~ ~ ~ i ii ii P ro t e i n s |E x o c o s ] j . .. .. .

G o l g i ~ @ / / /

S c h e m a t i c r e p r e s e n t a t io n o f t h e p r o c e s s e s l e a d in g t o t h e r e s p o n s e o f t h e a p o p l a s t t oe n v i r o n m e n t a l s ig n a l s . V a r i o u s e n v i r o n m e n t a l s i g n a l s a r e p e r c e i v e d b y t h e r e c e p t o r s lo c a t e d o nt h e p l a s m a m e m b r a n e o r p re s e n t in t h e s y m p l a s t. T h e s i g n a l s p e r c e i v e d a r e t r a n s fo r m e d a n dt r a n s d u c e d t h r o u g h t h e p l a s m a m e m l ~ ra n e a n d t h r o u g h t h e s y m p l a s t . H o r m o n e s a n d s i g n a ls p e c i f ic g e n e s m a y b e i n v o lv e d i n th e t r a n s d u c t io n o f t h e s ig n a l s . T h e t r a n s d u c e d s i g n a l s th e ni n d u c e t h e c h a n g e s i n th e a c t i v i t ie s o f i on c h a n n e l s a n d p r o t o n p u m p s , t h e r e b y m o d i f y i n g t h ee n v i r o n m e n t o f t h e a p o p l a s t . A t t h e s a m e t im e , t h e s y n t h e t i c a c t i v i t ie s o f t h e c e l l w a l l c o n s t i t u -e n t s a r e c h a n g e d b y t h e tr a n s d u c e d s i g n a l s . T h e c h a n g e s i n th e a p o p l a s t e n v i ro n m e n t a s w e l la s i n t h e l e v e l s a n d s t r u c t u r e o f a p o p l a s t c o m p o n e n t s b r i n g a b o u t t h e m o d i f i c a t i o n s o f t h ea p o p l a s t a c t i v i ty , l e a d i n g t o t h e r e s p o n s e t o t h e s i g n a l s .

the changes in ion concentrations in the apoplast mayinfluence the activity of the cell wall enzymes, resulting in thechanges in the physiological activity of the apoplast. Espe-cially, pH changes greatly affect the activities of the cell wallenzymes, as known as acid growth Hager e t a l 1971). Thispoint will be discussed later.On the other hand, the modif ications o f the activ ities of ionchannels and pro ton pumps shou ld induce the changes inthe osmotic potential of the cells. In maize coleoptiles, lightirradiation caused a rap id increase in the osm otic poten tial,resulting in growth suppression Parvez e t a l 1998). More-over, phosphorylation of receptor proteins present on theplasma membrane induces the signal transduction throughthe protein-kinase cascade in the symplast Kaufman 1993,Short and Briggs 1994, Ha ger 1996). Al so , the changes inconcentration of calc ium ions in the symplast due to themodification of activity of the calcium channels constitutethe m ajo r part of s ign al transduction pathway, in whichcalmodulin may be involved Polisensky and Bra am 1996,Braam e t a l 1996, 1997). Th e transduced signals finally caninduce the expression of signal-specific genes. It has beensuggested tha t horm ones are involved in the signal transduc-tion pathw ay or in the action o f signal-specific genes Fig. 1).The roles of ethylene Jackson 1985, Morgan and Drew 1997)

and abscis ic acid Hugher and D unn 1996, Cowan e t a l 1997,Shinozaki and Yamaguchi-Shinozaki 1997) in mediating thetransduction and response to s ignals are well-known,although contributions of other hormones have also beenshown. Actually, exogenously applied ethylene inducessimilar changes in the levels and structure of the cell wallconstituents to subm ergence in rice coleoptiles Hoson e t a h1990), and abscisic acid to water-deficiency in wh eatcoleopti les Wakabayashi e t a / 1997e).

One of striking results induced by environmental signalstransduced through the plasma membrane and through thesymplast is the changes in synthetic activities of the cell wallconstituents Fig. 1). Ce llul os e is known to be synthesizedby a cellu lose synthase complex located on the plasmamem brane Delmer and Amor 1995). The rate of cellu loseaccum ulation in the apop last is strongly modified by variousenvironm ental signals such as light, gravity, and water Table1). Matrix polysaccharides and the cell wall enzymes aresecreted into the apoplast v ia Golgi stack -trans Go lgi net-work Staehelin and Moore 1995). The activity of exocytosisof G olgi vesic les, important for determining and modify ing themechanical properties of the cell wa ll, is under control o fvarious environmental s ignals through the membranous andthe symplastic signal transduction pathways. At the same


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A p o p l a s t R e s p o n d s t o E n v i r o n m e n ta l S i g n a ls ] 7 3t i m e , s i g n a l - sp e c i f i c g e n e s m a y b e i n vo l ve d i n t h e syn t h e s i so f p ro t e i n co m p o n e n t s o f s i g n a l r e ce p t o r s , i o n ch a n n e l s , a n dp ro t o n p u P h p s , b y wh i ch t h e y m i g h t co n t r o l t h e se n s i t iv i t y o ft h e ce l l s t o e n v i r o n m e n t a l s i g n a l s .Ce l l wa l l l o o se n i n g i n d u ce d b y a u x i n i s m a i n l y b ro u g h ta b o u t b y t h e b r e a k d o w n o f x y l o g l u c a n s i n d i c o t y l e d o n s a n dt h a t o f ( 1 ~ 3 ) ( l ~ 4 ) - / % g l u c a n s i n G r a m i n e a e ( M a s u d a 1 9 9 0 ,Ho s o n 1 9 91 , 1 9 9 3 , S a ku ra i 19 9 1 ). T h e d e g re e o f b re a kd o w no f t h e se m a t r i x p o l ysa cch a r i d e s p l a ys a n i m p o r t a n t r o l e a l soi n r e sp o n se o f t h e a p o p l a s t t o e n v i r o n m e n t a l s i g n a l s (T a b l e1). O u r r e c e n t s t u d i e s s u g g e s t t h a t th e d e c r e a s e i n t h ea c t i v i t y o f b r e a k d o w n o f t h e s e p o l y s a c c h a r i d e s u p o n l i g h ti r r a d i a t i o n i s m e d i a t e d b y t h e ch a n g e s i n t h e a p o p l a s te n v i r o n m e n t a s w e l l a s t h e d e c r e a s e in t h e l e v e l s o f t h e c e l lw a l l e n z y m e s i n v o lv e d i n t h e ir b r e a k d o w n . B y th e l o n g -t e rm l i g h t e xp o su re t o p e a e p i co t y l s , t h e i n v i t r o a c t i v i t y o fx y l o g l u c a n h y d r o l a s e / e n d o t r a n s f e r a s e , o n e o f m a j o r x y l o g -l u c a n - d e g r a d i n g e n z y m e s ( T a b u c h i e t a l . 1 9 9 7 ), wa s d e c l i n e d(unp ub l i she d da ta) . A lso in r i ce co leop t i l es t he act i v i t y o f (1- * 3 ) ( 1 - ~ 4 ) - ,8 - g l u c a n - s p e c i f ic g l u c a n a s e s ( C h e n e t a l . 1996)wa s d e c re a se d b y l i g h t i r r a d i a t i o n (Ch e n e t a l . 1998) .H o w e v e r , th e s h o r t - te r m e x p o s u r e t o l ig h t d o e s n o t i n f l u e n c ethe i r ac t i v i t i es i n v i t r o . R a t h e r, t h e c h a n g e s in t h e a p o p l a s te n v i r o n m e n t , e sp e c i a l l y p H , a p p e a r t o b e i n vo l ve d i n su p -p re ss i o n o f t h e p o l ysa cc h a r i d e b re a kd o w n b y l ig h t. I n t h ep u l v i n u s , b l u e l i g h t i n d u ce d a t r a n s i e n t a l ka l i za t i o n o f t h ea p o p l a s t, w h i c h i s s u p p o s e d t o b e d u e t o t h e i n a c ti v a ti o n o fp r o to n p u m p s o n t h e p l a s m a m e m b r a n e ( O k a z a k i e t a l . 1995).S i m i l a r l y , a n a l ka l i za t i o n o f t h e a p o p l a s t wa s ca u se d b yh yp e rg ra v i t y i n a zu k i b e a n e p i co t y l s (S o g a e t a l . 1 9 9 8 ) . T h ec h a n g e s i n t h e a p o p l a s t p H m a y b e i n d u c e d b y v a r i o u se n v i r o n m e n t a l s i g n a l s i n g ro w i n g o rg a n s , l e a d i n g t o t h em o d i f ica t i o n s o f t h e m e ch a n i ca l p ro p e r t i e s o f t h e ce l l wa l l v i are g u l a t i n g t h e a c t i v i t i e s o f t h e ce l l wa l l e n zym e s .

C o n c l u d i n g R e m a r k sV a r i o u s e n v i r o n m e n t a l s i g n a l s i n d u c e d i v e r s e c h a n g e s i nt h e m e c h a n i c a l a n d t h e c h e m i c a l p r o p e r ti e s o f t h e c e l l w a l l.

In th e p r e s e n t r e v ie w , w e p r o p o s e d t h a t s u c h c h a n g e s in t h ea p o p l a s t s h o u l d b e r e c o g n i z e d a s t h e p o s i t i v e r e s p o n s e o fp l a n t s t o t h e s i g n a ls . T h e a p o p l a s t is in vo l ve d n o t o n l y int h e r e s p o n s e b u t a l s o in t h e p e r c e p t i o n a n d t r a n s d u c t i o n o fe n v i r o n m e n t a l s i g n a ls . T h e i n fo rm a t i o n o n t h e m e ch a n i sml e a d i n g t o t h e r e sp o n se i s l i m i t e d , e ve n i f a ccu m u l a t i n gre ce n t l y . I n o rd e r t o c l a r if y fu r t h e r th e r o l e o f t h e a p o p l a s ta s t h e s i t e o f r e sp o n se t o e n v i r o n m e n t a l s i g n a l s , we sh o u l dc o n t i n u e t o m a k e e f f o r t s t o u n d e r s t a n d t h e p r o c e s s e s o fp e r c e p t i o n a n d t r a n s d u c t i o n o f t h e s i g n a l s a s w e l l a s t h em o d i f i ca t i o n o f t h e ce l l wa l l .

T h e a u t h o r t h a n k s D r. Y . M a s u d a , T e z u k a y a m a C o l l eg e ,Dr . S . Kam isaka , O sak a Ci t y Un iversi ty , Dr . N. Sak ura i , H i ro -sh im a Un ivers it y , Dr . H. Ta kah ash i , To ho ku Un ivers it y , andDr . M . I nouhe, Eh ime Un ivers i t y , f o r t he i r adv ice and prov id ingin fo rmat ion .

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Received Decem ber 30, 1997: Accepted January 20, 1998)

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