Plants Wetlands

8/6/2019 Plants Wetlands

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T H E B O T A N I C A L R E V I E WV OL . 6 6 J U L Y - S E P T E M B E R0 0 0 N o . 3

B i o a c t iv e C h e m i c a ls a n d B i o l o g i c a l -B i o c h e m i c a l A c t iv i ti es a n dT h e i r F u n c t i o n s in R h i z o s p h e r e s o f W e t la n d P l a n ts

AMIR NEORIIsrael Ocean ographic & Limn ological ResearchNational Center fo r M aricultureP.O. Box 1212

Eilat 88112, IsraelK. RAMESH REDDY

Soil and Water Science DepartmentUniversity o f FloridaGainesville, FL 32611, U.S.A.HANA ~I~KOVA-KON~ALOVA

Section o f Plant EcologyInstitute o f BotanyAcadem y o f Sciences o f the Czech RepublicTrebon, Czech Republic

AND

MOSHE AGAMIPlan t Sciences DepartmentFaculty o f Li fe SciencesTel Av iv UniversityTel Av iv 69978, Israel

I .II.

Ill.Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 351Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 351Biological Activities of Chemicals from Wetland Plants . . . . . . . . . . . . . . . . . . . . . . 353A. Poisons . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 354B. Pest-Control Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 354

I. Anaerobic Metabolites . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3552. Alkaloids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3553. Phenolics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 355

Copies o f this issue [66(3)] may be purchased from the NYBG Press,The New York Botanical Garden, Bronx, NY 10458-5125, U.S.A.Please inquire as to prices.

The Botanical Review66(3): 350-378, July-September 0 0 09 200 0 The N ew York Botanical Garden 350


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BIOACTIVE CHEM ICALS IN RHIZOSPHERES OF WETLA ND PLANTS 351

4. T erpen oid s and S teroids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3565. O ther C hem icals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 357C. Biogeochemical Func tions in the Wet land Rh izosphere . . . . . . . . . . . . . . . . . . . 3571. E xtra ce llu la r E nz ym atic A ctiv ity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3572 . G ro wth R eg ula to rs (H orm on es) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3583. P hytosiderophores . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3594 . H e av y- M eta l B in de rs a nd P hy to ch ela tin s . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 595. A llelopathy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 360IV . M ed ic in al P ro pe rtie s o f W e tla nd P la nts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 62A . W e tla nd P la nts in T ra ditio na l M e dic in e . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 36 2B. Chemica ls f rom Wet land P lan ts in Modem Med ic ine . . . . . . . . . . . . . . . . . . . . . 363V . D iscussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 363V I. C onclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 365V II. A cknow ledgm ents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 366

V III. L iterature C ited . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 366IX . T ab le s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 374I . A b s t r a c t

W etland so i l s p rovide anox ia- to leran t p lan ts wi th access to am ple l igh t, w ater , and nut r i -en ts . In tense com pet i t ion , involv ing chemical s t ra teg ies , ensues am ong the p lan ts . The roo tso f we t land p lan ts are pr im e targets for roo t -eat ing pests, and the wet land rh izosp here i s anidea l env i ronmen t fo r m any o ther o rgan i sms and com mun i t i es because i t p rov ides wate r, ox y -gen , o rg anic food , and physic al p ro tect ion . Conse quent ly , the rh izosphere o f we t land p lan ts isdense ly popu la t ed by m any spec ia li zed o rgan i sms , w h ich cons iderab ly in fluence i ts b iogeo -chemical funct ion ing . The roo ts pro tect themselves against pes ts and cont ro l thei r rh izo-sphere organisms by b ioact ive chemicals , which of ten also have medicinal p roper t ies .An aerob ic metabol i tes , a lkalo ids , phenol ics , terpenoids , and s tero ids are b ioact ive che micalsabund ant in roo ts and rh izospheres in wetlands. Bioact iv i t ies include al le lopathy , g row thregulat ion , ex t raorganism al enzym at ic activi ties , metal man ipulat ion by phytosiderop horesand phytochelat ines , var ious pest -cont ro l ef fects , and poisoning . Complex b io logical -b io-chem ical in teract ions am ong roots , rh izosphere organism s, and the rh izosphere so lu t ion de-t e rmine the overa l l b iogeochem iea l p rocesses i n t he wet l and rh i zosphere and in t he vege ta t edwet lands . To co mp rehe nd how w et lands real ly funct ion , it is necessa ry to unders tand these in-teract ions . Suc h unde rs tanding requi res fur ther research .

I I . I n t r o d u c t i o nThe rh izosph ere i s the vo lum e of so il surrounding the p lan t roo t and in teract ing wi th i t

(Cur l & T ruelove , 1986) . So m e cr it ical features d is t inguish the rh izospheres o f we t land p lan tsf rom those o f ter res tr ia l p lan ts . Th e ma in d i f ference i s the w ater that surrounds the roo ts inw et land p lan ts , as op pose d to the ai r spaces around the roo ts of ter res tr ia l p lan ts . Becau se o fthe s low rate a t whic h gases d i f fuse th rough wa ter , rh izospheres o f we t land p lan ts are of tenl imi ted in oxygen , suppl ied there a lmost exclusively by the p lan t roo t i t sel f (e .g . , Br ix &Sehierup , 1990; A rms trong et a l. , 1992). On the o ther hand , being f looded ma kes the rh izo-spheres o f wet l and p l an ts more access ib l e t o wate r -ca rr i ed chemica l s and o rgan i sms f rom thebu lk soil tha n are terrestrial rhizosp heres .

Floo ded an aerob ic so i l s are considered host i le to p lan ts (e .g ., M i tsch & G ossel ink , 1993) .A cco rd ing to th is v iew , p lan ts in f looded so i l s are constan t ly s tressed. Th ey surv ive on ly i fthey c an co unterac t the suffocat ion of thei r roo ts . Usual ly , thei r defenses invo lve roo t aerat ion


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352 THE BOTANICAL REVIEW

and detoxification o f anaerobic metabolites (reviewed extensively in Crawford, 19 87; Blom ,1990; Gopal & M asing, 1990; Crawford & Braendle, 1996). Y et it is apparent that for thoseplants that can p rotec t their roots from ano xia and its resulting toxins, the w etland soil is ave ry suitable environm ent. T he floo ded soil, cleared o f its taller vegetation b y the anoxia, pro-vides the plant with its mo st basic and essential requiremen ts: access to light fro m above, wa-ter and nutrients from below, and room to expand.In the hostile anaerobic bulk soil the rhizospheres o f wetland plants create ox idized oasesfor various benign and pest microorganisms (e.g., Lee & Baker, 197 3; Meyers, 197 4) andsmall animals (e.g., Prejs, 1977; Osenga & Coull, 1983). Some o f them could be expe cted toquick ly consume the roots, y et this often happens on ly after the plant dies (of. Verhoeven,1986). Life in such a demanding en vironment has required the development o f a large array o finteresting, and often unique, defensive and aggressive chemical and biological-chemicalproce sses in the flooded rhizosphere and around it, to aid in plant-p est and plan t-plant co m-petition.Pest-control chemicals in the root m ay slow its consumption b y pests. Th ese chemicalscan hav e also medicinal p roperties, which h ave not always been scientifically studied. H ow -ever, healers in traditional cu ltures ma y hav e used such med icinal properties.Thanks to the pro xim ity in the rhizosphere o f anaerobic and aerobic zones, and o f steepgradients in ox yge n (e.g., A ndersen & Kristensen, 198 8) and nutrients (e.g., Bo ttom ley &Ba yly, 1984) perpendicular to the rhizoplane---the external surface o f the ro ot --t he m ost in-teresting and significant biogeochem ical processes o f the flood ed soil, and the densest mic ro-bial populations, oc cur there (see Ogan, 19 82 , and Laanbroek, 1990; the earl y literature onthis subject is w ell reviewed in Makulova, 1970; Ulehlova, 1976). Furthermore, the total sur-face area o f the anaerobic-aerobic plane around the rhizospheres in dens ely vegetated w et-lands can be m uch larger than the area o f the horizontal sediment-w ater or anaerobic-aerobicinterfaces (e.g., Sm ith et al., 19 79; Francour & Semrou d, 19 92). Thus it is likely that the pro-cesses occurring in the rhizosphere have quantitatively more influence on the total biogeo-chemical processes in the wetland than does the horizontal sediment-water interface,although the latter is mor e conveniently studied. The re has therefore been a rising recogn itionthat understanding w etland biogeoehemistry requires understanding ofrhi zo sp he re processes(e.g., Doy le & O tte, 1997; Havens, 1997; Hsieh & Y ang, 1997).Y et there is a shortage o f data on these multidisciplinary issues; wetland processes andfunctions hav e typ ically been studied b y specialists. For instance, soil biogeochemists havestudied the physical, thermodynam ic, and chemical factors that control biogeochemical pro-cesses in wetland soils (see Mitsch & G osselink, 1993). These scientists have often studiedthe so il-wa ter interfaces o f wetlands with soil cores and slurries bu t have excluded the irroo ted plants. Similarly, microbiologists h ave studied microorganisms and the processes t heymediate, necessarily ofte n in pure cultures or in sediment slurries, bu t without plants. The re-fore, much is know n about the different microbial groups o f flooded soils, their requirements,and the ir activities in cultures (e.g., Laanbroek, 1990) bu t not in situ. Th e plants themselveshave often been studied by botanists, plant physiologists, and ecologists, who often hav e notincorporated th e soil and microbial disciplines into the ir research. Frequently, the first stagein preparing a wetland plant fo r an experiment is brushing an d rinsing o ff the soil from theroots. Th eref ore , there is m uch greater understanding o f the physiological adaptations that al-low plants to live in flood ed soils (Blom, 1990; Armstrong et al. , 1991) than o f their chemi-cal-biochemical interactions with rhizosphere organisms and chemicals (Braendle et al.,1996). I t is revealing to n ote that wh en wetland soils were studied with the plants in th em --f orexamp le, in relation to wastewater treatment (see Red dy & Sm ith, 1987)---the plant-soil corn-


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B IO A C T IV E C H E M IC A L S IN R H IZ O S P H E R E S O F W E T L A N D P L A N T S 3 53

p l e x w a s c o n s i d e r e d a " b l a c k b o x . " I n s u f f ic i e n t a tt e n ti o n w a s o f t e n p a i d t o t h e q u a n t i ta t iv ed e t a il s o f t h e c h e m i c a l - b i o c h e m i c a l i n t e r a c ti o n s o f t h e p la n t , i ts r h i z o s p h e r e , a n d t h e m i c r o -b ia l co m m u n i t i e s in an d a ro u n d i t (H a ck n e y , 1 9 8 7 ; d e l a C ru z e t a l. , 1 9 89 ) . T h e o x y g en r e -g im e in w e t l an d rh izo sp h eres ( e .g ., A rm s t ro n g e t a l. , 1 9 9 1 ) an d ro o t ex u d a tes a s su p p l i e r s o fd eg ra d ab le o rg an ic ca rb o n to th e rh i zo sp h ere ( e .g ., Wetze l , 1 9 9 2 ) a re f av o rab le ex cep t io n s ;th a t i s , t h ey a re w e l l s tu d ied w i th r e sp ec t to th e o v era l l eco sy s tem .

T h e r e i s a l s o a g r o w i n g b o d y o f e v i d e n c e t h a t th e o x y g e n p u m p e d t o t h e s o il b y t h e p l a n tsc o n t r o l s m a n y i m p o r t a n t b i o g e o c h e m i c a l a n d b i o l o g i c a l a c t i v i t i e s a n d p r o c e s s e s . F o r i n -s t a n c e , i t w a s r e c e n t l y s u g g e s t e d t h a t t h e o v e r a l l ra t e o f m e t h a n e r e l e a s e t o t h e a t m o s p h e r e i n ap e a t l a n d i s c o n t r o l le d b y t h e s u p p l y o f o x y g e n t o t h e r h iz o s p h e r e o f t h e a q u a ti c m a c r o p h y t eSparganium eurycarpum ( K i n g , 1 99 6) . H o w e v e r , w e b e l i e v e t h a t th e s u b j e c t o f o x y g e n s u p -p ly to w e t l an d rh izo sp h eres i s su f f i c i en t ly d ea l t w i th in th e l i te r a tu re . R o o t -p a th o g en in t e rac -t io n s h av e a l so b een w e l l d o cu m en ted , b u t p r im ar i ly in ag r i cu l tu ra l c ro p s ( r i ce , w a te rh y a c i n t h ). C o m p l e x c h e m i c a l a n d g e n e t ic c o n t r o l s w e r e i n d e e d f o u n d in m a n y s u c h c a s e s(D ix o n & L am b , 1 9 90 ). U n fo r tu n a te ly , n o t en o u g h i s k n o w n a b o u t su ch in t e rac t io n s in n a tu -r a l w e t l a n d s . A s t u d y o f i r o n o x i d e d e p o s i t io n o n r o o t s o f r i c e (Oryza sat&a ; J o h n s o n - G r e e n& C ro w d er , 1 9 9 1) an d a s tu d y o f N -cy c l in g in th e w e t l an d rh izo sp h ere (R ed d y e t a l ., 1 9 8 9) ,w h ere ro o t - rh iz o sp h er e in t e rac t io n s w e re in v es t ig a ted in d e ta i l , i n d eed p ro v id ed in s ig h t in toth e o v era l l i n te rac t io n s in th e rh izo sp h ere . B u t su ch s tu d ies a re sca rce . S o m e o f th e r e sea rcht h a t d i d i n t e g r a t e r h i z o s p h e r e m i c r o b i o l o g i c a l p ro c e s s e s a n d i n te r a c t io n s h a s b e e n r e v i e w e din a se r i e s o f a r t ic l e s b y G u n n i so n an d B ark o (1 9 8 8 a , 1 9 88 b , 1 9 89 ; B a rk o e t a l. , 1 9 9 1 ) an do th e r s (C arp en te r & L o d g e , 1 9 86 ; W aise l & A g am i , 1 9 9 6) .

O b v i o u s l y , i s o l a ti n g t h e c o m p o n e n t s o f a n e c o l o g i c a l s y s t e m i s n e c e s s a r y f o r u n d e r st a n d -i n g h o w t h e y f u n c t i o n . H o w e v e r , th e c o m p l e t e e c o lo g i c a l p i c t u re m a y b e c o m e b l u r re d b ysu ch p rac t i ces . T h ere f o re , t h e ap p l i ca t io n o f ex p er im e n ta l re su l t s t o n a tu ra l sy s t em s i s o f t end i f f i cu l t o r sp ecu la t iv e an d l ead s to u n p leasan t su rp r i ses . F o r in s t an ce , i n a s tu d y o f l acu s t r in es e d i m e n t s K e p k a y ( 1 9 8 5 ) d e s c r i b e d u n e x p e c t e d l y s t ro n g a n d u n e x p l a i n e d i n h i b i ti o n o f m a n -g an ese o x id a t io n an d n i t r i f ica t io n b y ro o t s ( see o th e r ex am p les in B u rd ick e t a l ., 1 9 89 , an d inG a n g a w a n e & K u l k a m i , 1 9 8 5 ) .

T h e g a th e r in g o f in fo rm at io n av a i l ab le o n w e t l an d rh izo sp h eres f ro m as m an y d isc ip lines a sp o ss ib le w i l l a l lo w a m o re co m p reh en s iv e u n d er s t an d in g o f th e fu n c t io n in g o f v eg e ta t ed w e t -l an d s. M o reo v er , p o in tin g o u t rh izo sp h ere p ro cesses an d fu n c t io n s th a t h av e b een d o cu m en tedin n o n w et l an d p lan t s can a id in fo rm u la t in g p lan s fo r r e sea rch o n su ch i ssu es in w e tl an d s. W eh o p e to p o in t o u t i s su es fo r w h ich th e re a re g ap s in th e sc i en t if i c k n o w led g e an d to s tim u la te in -teres t in f i l l ing them. In the p resen t ar tic le , the f i rs t in a ser ies ( two o ther pub l icat ions wi l l de-sc r ib e m ic ro b es an d an im al s o f w e t l an d rh izo sp h eres an d th e i r i n t e rac tio n s w i th th e p lan t ro o tan d i t s en v i ro n m en t ) , w e sy n th es i ze p u b l ish ed ev id en ce o n b io ac t iv e ch em ica l s an d b io lo g ica l -b io ch em ica l ac t iv i ti e s an d th e i r i n f lu en ce o n th e fu n c t io n in g o f w e t lan d s . In sev e ra l cases w eb e l i ev e th a t s im i l a r p h en o m en a a re l i k e ly to b e fo u n d in w e t l an d s i f l o o k ed fo r , so w e h a v e p re -s e n t e d t h e r e l e v a n t i n f o rm a t i o n f r o m n o n w e t la n d e n v i r o nm e n t s . W e t h e n u s e t h e e v i d e n c e t osu g g es t l i n es o f r e sea rch n ecess a ry to in te rp re t t h is in fo rm at io n in th e co n tex t o f th e fu n c t io n -i n g o f a w e t l a n d . W e h o p e t o c o m p l e m e n t p r e v io u s r e v i e w s o n m o r e s p e c i f ic w e t l a n d s u b j ec t s(such as Hoo k , 1984 ; Kozlow sk i , 1984 ; Blom , 1990 ; Arm strong e t ai ., 1991) .

H I . B i o l o g i c a l A c t i v i t i e s o f C h e m i c a l s f r o m W e t l a n d P l a n tsB io ac t iv e p lan t ch em ica l s m o d i fy th e ac t iv i ty o f o rg an i sm s (R in eh ar t e t al ., 1 9 9 0) . P lan t

ch em ica l s th a t i n h ib i t o rg an i sm s th a t d am ag e th e p lan t a re co n s id e red n a tu ra l p es t - co n t ro l


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chemicals. Carpenter and Lodg e (1986) expressed the notion that aquatic plants usually lackgrazing deterrents. H owev er, as w e shall show, this is not true. Even in grasses, not known fortheir bioactive chemicals, genera with widespread wetland species--Panicum and Phalaris-- h av e been reported to contain effective toxins (Cheeke, 1995). Other rhizosphere organ-isms in wetlands also produce bioactive chemicals, which can influence the biological-biochemical functioning o f the rhizosphere. In this section w e shall review the m ost studiedchemical and biological activities that are or can be associated with wetland rhizospheres.

A. POISONST he potential ro le of plant poisons in the defense o f the plants is straightforward. Q uite a

few wetland plants are poisonous to animals, especially in the Nymphaeaceae, Rannuncu-laeeae, and Um biliferae (T able I; Mu enscher, 1975; for a rev iew of toxic plant proteins, seeTu & Miller, 1992). Moreover, mo st of the typically "poisonous" plant families have w etlandmem bers (T able V). The natural role of these poisons is presumably protection o f the wholeplant against grazing an imals, bu t often the roo ts are mo re toxic than is the rest o f the plant(Grainge & A hmed, 19 88 ). Th ere are also reports o f antiplant poison s--natu ral herbi-c id e s- in the roots of several wetland plants (Grainge & A hmed, 1988) .Un fortunately, studies o f plant tox icity and general pest-control activity ofte n do n ot iden-tify the chemicals. For instance, Ceratophyllum plants protect themselves fro m herbivores b yunidentified repellent substances (Bronmark, 1985), and aquatic plants of several gen er a- -Lyonia, for exam ple --pro du ce effective hemolytic piscicides (Bhatt & Farswan, 1992).Plants in the widespread generaXanthium, Scirpus, T ypha, and Phragm itesprod uce unidenti-fied fungicides, bactericides, and larvicides (briefly reviewed by Lak sman, 1987). Typha an dEleocharis also pro du ce selective algieides (Aliotta et al., 1990). Th at aquatic plants ha ve tra-ditionally pro vid ed m an with poisons against fish and other aquatic animals is indicative o fthe prev alence o f poisons in roots o f wetland plants (see Costa-Pierce et al. , 1991).

B. PEST-CONTRO LACTIVITYIt has ofte n be en ob served that certain live plants are not attacked by pests and herbivores.As we discuss below, plants have several mechanisms for achieving pest-control results in

the ir rhizospheres. O ne o f them is pest-control chem icals (another comm on approach inplants is localized hy persensitivity to the pathogens, as described in Sm ith, 1 98 9). Thesechemicals can be antimicrobial, insecticidal, or poisonous, as described abo ve. To influencethe rhizosphere, these chemicals do no t have to be actively exudated. O ften significant releaserates resu lt from ro ot growth, dying roo t cells, and sloughing o ff cells. Furthermore, whenpests attack the ro ot tissue, the dead o r injured tissues release those chem icals at the attackedpoint, thu s loca lly protecting the plant from further damag e (Smith, 1976).M ore than 2,000 plants are know n to have pest-control chemicals (Balandrin et al., 1 985;Grainge & Ahm ed, 1988). Much o f the information on pest-control chemicals in wetland andaquatic plants is from economically important rice. The documented cases regarding resis-tance o ff ic e varieties to insects, for example, include several volatile repellents and phenolicfeed ing deterrents found in all organs o f the plant (reviewed by S mith, 1989). Bu t reports ex-ist for othe r plant sp ecies as well. Exudates o f the aquatic fern Salvinia auriculata inhibitedthe breeding o f the mosquito Anopheles albimanus (Hobb s & Mo lina, 1983), and a petroleumextract from the roo ts of the mangrove plant H eritiera littoralis was a piscicide (M iles et al.,1989). In a mo re complex case, the inhibition o f microbial organic-matter decom position in


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BIOACTIVE CHEMICALS IN RHIZOSPHERES OF WETLA ND PLANTS 355

the rhizosphere o f P i n u s r a d ia ta was attributed to exudates not from the roo t but from its sym-biotic m yco rrhiza (Gadgil & Gadgil, 1975). Th e antibacterial activity of root exudates fromwetland plants is widespread (Gopal & Goel, 1993). The plant genera involved includedNuphar, Sc irpus , Acorus , Juncus , Ir is , Mentha , Phragmites , A lnus , Lemna, Nymphaea ,Carex , V a l l isneria , Po tam oge ton , Typha , and several aquatic angiosperms.

Sm ith (1976) described im portant bioactive chemicals typical o f certain plant families. Theimportant bioactive chemicals o f plant origin are anaerobic metabolites (organic acids, alco-hols), alkaloids, phenolics, terpenoids, steroids, and hydrogen cyanide (HCN ). Intuitively, achemical can h ave m ore than one function or bioactivity in the plant and its environment.

1 . A n a e r o b i c M e t a b o l i te sIn the broad sense, anaerobic metabolites can be inhibitory to plants and various other or-

ganisms. Elevated CO 2 concentrations o r large pH an d ionic shifts created in their rhizosphereor by the ir roots can mak e the plants toxic (see Hook, 1984). A w ell-known example is that o fplants from the Sphagnaceae, which by exchanging ions w ith their surroundings reduce thepI-I until it bec om es detrimental to m ost other plants and to m any microorganisms or animals(Dickinson, 198 3; Mason & Standen, 1983; Speight & B lackith, 1983). How ever, the pHchanges can also depend on the chem ical form o f plant nutrition. Fo r instance, N2 fixation andamm onia up take lead to decreased pH , but nitrate uptake leads to increased pH. T here are alsointeresting interactions amon g roo t exudates, rhizosphere pH, and the uptake o f such micro-nutrients as iron and zinc in wetland ric e (Kirk & Bajita, 1 995).

Plants adapted to waterlogging, such as the willow (Salix alba), mannagrass (Glyceriaaquat ica) , and rice (Oryza sa t iva), exude glycolytic products to the rhizosphere und er water-logged conditions ((~irknvfi, 1978; Hook, 1984; Smith et ai., 1986). Products such as alcoholsand organic acids (lactate, malate) can be toxic to plants, animals, and microorganisms. T heroots o f the wetland plants themselves have some resistance to them. Such m etabolites can berespired in the ro ot itself, w hen o xyg en becomes available, or they can b e transported to aerialparts o f the plant fo r detoxification b y oxidation (Crawford, 1987).

2 . A l k a l o i d sAlkaloids, the most studied---and useful to man--biologically active plant-producedchemicals, e xist in several plant families with wetland o r aquatic species (Table III). Clark etal. (1985) extracted several antibacterial and antifungal alkaloids from tissues of the ye llowpop lar or tulip tree, Liriodendron tulipifera (Magn oliaceae). Alkaloids are also produced by

the roots of Ca ss ia f i s tu la (Sinha et al., 1992). Unfortunately, few of the specific wetlandmem bers o f many o f these families hav e been examined for their alkaloids. F or instance, rootsin species o f the Anno nacea family, which include the wetland tree A n n o n a g la b r a, producetannins and alkaloids (Lewis & Elvin-Lewis, 1977).

3 . P h e n o l i c sPhenolic compounds are widespread in plants, including those fro m wetlands. T hey can berathe r poisonous to microorganisms and aquatic animals (e.g., Green et al., 198 5). M any o fthe docum ented plant-produced p est-control effects are caused by chemicals o f this family.Sarkar et al. (1988) d escribed an effective pest-control and deterrent pheno lic comp ound fro mthe roots o f the wetland plant needle rush, J u n c u s ro e m e r ia nu s . This explains earlier observa-


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356 THE BOTAN ICAL REVIEW

tions o f herbivo res' avoidance o f this plant. Phenolics extracted from Typha roots have beenshow n to be algicides (Aliotta et al., 199 0). Biologically active phenolics hav e also been ex-tracted and identified from roots o f the widespread Nu phar variegatum (Nishizawa et al.,1990), U rtica dioica (Kraus & Spiteller, 19 90 ), and M yriophyllum verticillatum (Aliotta eta l. , 19 92) . Some of the most com mon wetland p la n ts l t he genera Phragmites, Asclepias,Phalaris, Spartina, Sphagnum, and Eupho rbia--have been shown to release phenolics tothe ir rhizospheres (cf. Dickinson, 1983). Various plant genera that contain wetland specieshav e been suggested to inhibit with phenolic compounds nitrifying ba cteria--co m petitors foroxy gen and am m on ia--in th eir rhizosphere (reviewed briefly in Cooper, 19 86 ; see alsoHe dges & Messens, 1990).

Because phen olic com pound s are intermed iaries in the pathways o f several impo rtant bio-chemical processes, some plants and soil microbes can metabolize external phenols as well.Brummet and O'Keefe (1982), following an earlier report by Wolverton and McKown(1976), o bserved in w ater hyacinth ro ots the uptake and translocation o f externally adminis-tered phenolic com pound s to the aboveground parts for metabolism. T his activity could be in-duced, and preexposure o f the plants to 25 -100 rag/1 o f phenol doubled their tolerance for thechemical, to u p to 400 rag/1. Potential targets of pla nt-b ioac tive chemicals, soil microbes ha vebee n shown to consume phenolic com pounds, thus protecting themselves, neighboring organ-isms, and plant roots (Gunnison & Barko, 1988a).Betalains are pigmented nitrogenous phenols found o nly in the plants o f the order Cen-trospermae (Smith, 1976). Th ey give these plants, such as red beets, their typical co lor and arealso effec tive insect repellents. Several families in this ord er hav e genera of wetland plants,such as the Aizoaceae (Sesuvium), Polygonaceae (Rum ex, Polygonum, Brunnichia), Cheno-podiaceae (Halimione, C henopodium, Atriplex, Salicornia, Suaeda), Amaranthaceae (Ama-ranthus, Ac nida ), and Po rtulacaceae (Montia).Phenolic comp ounds in the rhizosphere can also be of microbial origin. Certain soil micro-organisms release phenolics, perhaps in self-defense (cf. Dickinson, 1983; Laksman, 1987;Gunnison & Barko, 1988a, 1989; Lyn n & Chang, 1990). Once in the rhizosphere, such potentchemicals can interfere with any biological activity around and in the roots. M icrobial phe-no lics have bee n imp licated in affecting rhizosphere processes, such as plant-microbe h ost-symb iont recognition and specificity (Ly nn & Ch ang, 1990). Y et there is little specific infor-mation on phenolic compounds in wetland plants and on their role in the functioning o f therhizosphere.

4. Terpenoids an d SteroidsTerpenoids and steroids, including the carotenes, rubber, and several plant hormones, are

com m on plant chemicals, w hich are potent in several bioactivities, in particular antifungalroles (Smith, 1976). Man y of these chemicals are grazing repellent, causing a bitter taste andbad physiological reactions in animals and insects. Some terpenoids are water soluble andbind w ell to soil, thus m aintaining their activity there for a long time. Som e o f them h ave beenassociated w ith allelopathy in the wide sense. Cineole an d camph or, in particular, are inhibi-tors o f seed germination. In waterlogged soils, terpenoids and steroids deactivate free soil en-zym es (Wetzel, 1991).Terpenoids ha ve been found in the roots o f wetland plants, such as Urtica dioica, whosecom m on name "stinging ne ttle" perhaps reflects the effec t o f the chemicals (Kraus & Spi-teller, 199 l).


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BIOAC TIVE CHEM ICALS IN R_HIZOSPHERES OF W ETLAN D PLAN TS 357

5. Other ChemicalsM a n y b i o a e t i v e c h e m i c a l s a r e l e s s w i d e s p re a d . B e t a - e c d y s o n e , f o r i n st a n c e , i s a n i n s e c t

f eed in g d e te r r en t th a t e f f ec t iv e ly in h ib i ts i n sec t d ev e lo p m en t (S m i th , 1 9 7 6 ). I t h as b een fo u n do n l y i n th e T a x a c e a e a n d P o d o c a r p a c e a e o f t h e g y m n o s p e r m s , s o m e o f w h i c h i n h a b it w e t -l a n d s . R h i z o m e s o f Urtica dioica p ro d u ce an an t i fu n g a l l ec t in (B ro ek a er t e t a l. , 1 9 8 9) . T h ep l a n t s f r o m s e v e r a l f a m i l i e s th a t i n c l u d e w e t l a n d s p e c i e s p r o d u c e n o n p r o t e i n a m i n o a c i d s ,sh o w n to in h ib i t o r k i l l i n sec t s an d m ic ro b e s (S m i th , 1 9 7 6 ). P lan t s f ro m th e f am i ly A n n o n a -c e a e , w h i c h i n c l u d e s th e w e t l a n d t re e Annona glabra, p r o d u c e d e r i v a t i v e s o f f a t t y a c id s w i thp o t e n t b i o l o g i c a l a c t iv i ti e s , s o m e o f w h i c h h a v e m e d i c i n a l u se s. D o c u m e n t e d b i o a c ti v i ti e s o fth i s so u rce a re cy to to x ic , an t i tu m o r , an t im a la r ia l , an t im ic ro b ia l , im m u n o su p p ressan t , an -t i f eed an t , an d p e s t i c id a l ( e l . R u p p rec h t e t al ., 1 9 90 ). L o n g -ch a in f a t ty ac id s a re b io lo g ica l lyac t iv e ch em ica l s ch a rac te r i s t i c o f aq u a t ic p l an t s (G o p a l & G o e l , 1 9 9 3) , an d th ey h av e b eenim p l i ca ted in a l l e lo p a th ic in t e rac t io n s o f Polygonum, Eleocharis, Potamogeton, Najas, Tha-lassia, Ruppia, and Typha. E l e m e n t a l s u l f u r r e le a s e h a s b e e n a l s o r e p o r t e d b y s e v e r a l a q u a t i cp lan t s , i n c lu d in g Ceratophyllum demersum (G o p a l & G o e l , 1 9 9 3) .

S o m e p l a n t s p r o d u c e p h y t o a l e x i n e s a nd H C N t o f i g h t t h e i n v a d e rs ( L y n c h , 1 9 9 0; I s a a c ,1 99 2) . T a b l e I V p r e s e n t s t h e f a m i l ie s i n w h i c h H C N w a s b e e n s h o w n t o b e p r o d u c e d a n d t h et y p i c a l w e t l a n d g e n e r a b e l o n g i n g t o th e s e f a m i l ie s . A p p a r e n t l y , s o m e o f t h e m o s t c o m m o nw e t l an d p lan t s b e lo n g to su ch f am i l ie s . I t s eem s r easo n ab le to su g g es t fu r th e r in v es t ig a t io n so n th e ro l e o f H C N in rh izo sp h ere fu n c t io n in g in th ese p lan ts .

A g r icu l tu ra l ly im p o r tan t p l an t -p ro d u ced in sec t i c id es a re a l so fo u n d in w e t l an d p lan ts , g o -t en o n e , a p o ten t an d u se fu l p es t i c id e , is fo u n d in ro o t s o f th e g en u s Pieris ( E r i c a c e a e ; G r a i n g e& A h m ed , 1 9 88 ) , w h ich in c lu d es th e w e t l an d p lan t f e t t e r b u sh (Pierisfloribunda). P y re th r in sa re a l so ag r i cu l tu ra l ly im p o r tan t in sec t i c id es th a t occu r i n p l an t s o f th e Pyrethrum g e n u s ,w h i c h c o n t a i n s w e t l a n d s p e c i e s .

c . B IO G E O C H E MIC A LFUNCTIONS 1N THE WETLA ND RHIZOSPHERE1. Extracellular Enzym atic Activity

T h e r h i z o s p h e r e o f th e w e t l a n d p l a n t c a n b e c o n s i d e r e d a " s o u p " o f e x t r a c e l l u l a r e n z y m e s .A l t h o u g h s o m e e n z y m e s a r e a c t iv e l y s e cr e t e d , m a n y o f t h e m s i m p l y e x u d e f r o m c e l l s th a t a r eb r o k e n i n t h e n a t u r a l p r o c e s s o f r o o t g r o w t h a n d t h e e m e r g e n c e o f a d v e n ti t io u s r o o ts . F r e e e n -zy m es a re im p o r tan t in th e aq u a t i c en v i ro n m en t , e sp ec ia l ly th e rh i zo sp h ere ( Jan d era e t a l . ,1 9 89 ; W etze l , 1 9 91 , 1 9 9 2) . T h ey can b e o f p l an t , m ic ro b ia l , o r an im al o r ig in , an d th ey h av ed i f f e r e n t f u n c ti o n s . T h e i r a c t i v i ty c a n b e p r e s e r v e d f o r s o m e t i m e . T o t h a n d Z l i n s z k y ( 1 9 8 9 )s h o w e d t h a t u p o n t h e d e a t h o f t h e o r g a n i sm , t h e e n z y m e s o f t h e e l e c t ro n - t r a n sp o r t sy s t e m s o fm a n y f l o o d e d - s o i l o r g a n i sm s c a n k e e p f u n c t io n i n g a n d e n h a n c i n g t he b r e a k i n g d o w n o f o r -g a n i c m a t t e r f o r w e e k s . L i v e r o o t s o f a x e n i c a l l y c u l tu r e d p la n t s r e l e a s e d p h o s p h a ta s e s , i n v e r -t a ses , p ro teases , an d p e ro x id ases , a l l o f w h ich co u ld p a r t i c ip a te in th e b io g eo ch em ica l cy c l in go f c o m p o u n d s ( c f . W e t z e l , 1 99 1) . A m m e r m a n ( 1 9 9 1 ) a n d C o t n e r a n d W e t z e l (1 9 9 1 ) r e -v i e w e d d i f f e r e n t s y s t e m s o f e x t r a c e ll u l a r e n z y m e s t h a t p e r f o r m i m p o r t a n t fu n c t i o n s i n t h e r e -g e n e r a t i o n a n d m e t a b o l i s m o f p h o s p h o r u s i n th e a q u a t ic e n v i r o n m e n t . A p p a r e n t l y ,ex t r aee l lu l a r en zy m es can a l so ca r ry o u t s ig n i f i can t r a t e s o f n i t r i f ica t io n in f lo o d ed so i l s (v anC lee m p u t & P a t r i ck , 1 9 7 4 ). R h izo sp h ere m ic ro b e s , p a r t i cu la r ly p a th o g en s , p ro d u c e p ec t in o -ly t i c en zy m es an d cu t in ase w i th a sp ec i f i c ro l e : to p en e t r a t e th e ro o t . S o m e ro o t s , in tu rn , p ro -d u c e g l u c a n a s e t o d a m a g e t h e w a l ls o f f u n g a l p a t h o ge n s .


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Enzym atic activity is higher in the rhizosphere o f terrestrial plants than elsewhere in thesoil (Jandera et al., 1989; Lynch , 1990). In flooded soils enzymes are often inhibited b y com-plexation to humic and fulvic substances (Wetzel, 1991, 1992). Tannins in particular bindproteins into indigestible and often inactive comp lexes (Mandava, 1985; W etzel, 19 91). Th ein situ function o f extracellular enzym es is responsive to environmental conditions, such asred ox potential o r pH (B enner et al., 198 9). Enzym es in flooded organic soils, even if inactiveund er anaerobic conditions, accelerate th e breakdown of nonhumified organic m atter uponoxidation (M athur & Farnham , 1985). Th e activities o f peat enzym es, either intracellular orext race llula r--ce llula ses , proteases, and polyphenolox idases---indeed increased dramati-cally upon soil oxygenation (Lahdesmaki & Piispanen, 1990). Such activity led to the quickrelease o f various nu trients, especially am ino acids and amm onia, to the interstitial waters.Because ro ots o f wetland plants m odify the pH and increase the red ox potential in the ir rhizo-sphere, it appears that the y influence extracellular enz ym e activity there. Th e evidence o f ac-tive free en zym es in wetland rhizospheres is particularly intriguing in another sense. As w eobserved above, free enzymes m ay be inactivated and preserved by tannins and other chemi-cals in the bulk anaerobic soil, and reactivation can o ccu r upon oxidation. Th is raises the pos-sibility that the wetland plant, upon oxygenation o f new dom ains by its expanding roo tsystem, practically "releases" bound enzymes, thus enhancing the breakdown of organic mat-ter and sup plying i tse lf w ith remineralized nu trients.

2. Growth Regulators (Hormones)Plant-growth regulators found in the so il are produced n ot on ly by plants bu t by other or-ganisms as well. Plant hormones can influence various physiological processes in plants ev enwh en adm inistered through the water. I f a hormone released by one plant interferes w ith thenormal growth o f another, it can be interpreted as allelopathy (see below). S olutions o f planthormones, even in low concentrations (0.01 mg/l of abscisic acid), wh en applied to water hya -cinth, caused significant changes in its metabolism (D 'An ge lo & Reddy , 1987). Earlier suchobservations led to th e use o f the floating Lemna in plant-hormone bioassays. The effects ofauxins, gibberellins, cytok inins, abscisie acid, ethylene, and salicylic acid on Lemna were re-viewed b y Cleland et al. (1982) and b y Mitsch and G osselink (1993). Laksman (1987) re-view ed reports that Typha and Eleocharis produced and released plant-growth-stimulatinghormones. Th ere are also m any such reports for the water hyacinth (e.g., Si ca r& Chakra-

verty, 1968).Ethylene, an im portant plant-growth hormo ne that is produced m icrobially and b y roo ts infloo ded soils (How arth et al., 1 988), also influences other rhizosphere processes, such as theinhibition o f amm onia oxidation (Porter, 1992 ). Although ethylene is produced m icrobially inflooded soils from phenolic acids, it is also bacterially oxidized there (Gunnison & Barko,1988a). Ethylene is qu ickl y degraded in flooded rice rhizospheres (Yoshida & Suzuk i, 1 975;Arm strong, 1979). Other hormones, su ch as salicylic acid (SA), are also released to the rhizo-sphere fro m the root. Neori, Kane, and Raskin (unpu blished) found that SA release fro m theseedling roots of several tissue-cultured aquatic plants (Orontium, Pontederia, and Sagit-taria) reached tens of mieromoles 1 I and 1% o f plant dry weight w ithin 3--4 weeks. SA, atconcentrations as low as 10 microm oles 1 I, significantly inhibited potassium uptake in rootso f terrestrial plants (Putnam , 1985) and is like ly to do the same in wetland plants.Soil microbes also pro duc e and mo dify other plant hormones to control the ir environment.Azospirillum brasilense, a nitrogen fixer in the rhizosphere o f various grass spe cie s--in par-ticular, w etland ric e-- rel ea se d indole lactic acid, gibberellin, and other hormo nes.


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BIOACTIVE CHEMICALS IN RHIZOSPHERES OF WETLA ND PLANTS 359

3 . P h y t o s i d e r o p h o r e sInsoluble ferric iron (Fe3+) often con centrates as a precipitate in the rhizospheres o f w et-

land plants (Johnson-G reen & Crow der, 1 99 1), where it diffuses as soluble ferrous iron(F e2+) fro m bu lk anaerobic soil. Phytosiderophores are nonproteinogenic amino-acid roo texudates that co m plex and dissolve ferric iron. In the Graminae, which include m any wet-land species, these molecules com plex the ferric iron and are taken up b y the roo t via a highlyspe cific uptake system (M arschner et al., 1986). O ther plants, lacking such an uptake system,can then b ecom e iron deficien t in a phenomenon that appears like allelopathy when the sid-erop hore released by a plant inhibits growth o f another plant. Phosphate precipitated withferric iron bec om es available for plant uptake b y the siderophore activity. T he process is notsensitive to high pH or bicarbonates, and this gives grasses an advantage o ve r oth er plants insoils with such co nditions. This pro bab ly explains wh y the resistance o f several rice varietiesto alkaline iron deficiency , or "lime ch lor os is" --a typical disease o f paddy-rice seedlings inalkaline so ils--c orre lated with the ir ability to release phytosiderophores (Marschner et al.,1986). Tagaki et al. (1984) show ed that rice released to the soil solution mug ineic and aven icacids, tw o nonproteigenic amino acids that effective lychelate ferric iron. Mori e t al. (1991)showed that deo xym ugin eic acid is produced in the rice root, secreted to the rhizosphere,chelates fe rric iron, and transports it into the cells via a specialized transporter o f de ox ymugineie acid-Fe3+. If the seedlings w ere not allowed sufficient time to p roduce this phy to-siderophore, they suffered ehlorosis and could not develop properly. Certain phytosidero-phores can also aid in the uptake of other metals, such as copper, manganese, and zinc(Romheld, 1991).Most bacteria need bioavailable iron at concentrations much greater than higher plantsneed (1 mic rom olar for bacteria, versus 1 nanomolar fo r plants; see Hem ming, 1986). Flood-ing and the solubilization of iron following anaerobiosis therefore stimulate the activity ofsome iron-limited soil bacteria. How ever, in the oxidized rhizosphere the bacteria ma y stillnee d siderophores to ob tain their iron. Mycorrhiza and other fungi also produce sideroph oresfor this reason. Ly nch (1990) described several studies of the com plex role of microbiallyproduced siderophores and other ionophores in plant nutrition under flooded conditions.Hyd roxamate siderophores exist in certain so ils at levels that significantly affect the bioavail-ability o f iron (Hemm ing, 1986). Som e siderophores found in nonflooded soils are producedby microbes, such as the fluorescent Pseudom onas syringae, P. f luorescens, and P. aerugi-nosa. These fluorescent pseudomonades also inhibit plant pathogens (Hemming, 1986).Th ere is no reason fo r the situation to be different in wetland plants. Indeed, Pseudomonas sp .was also described from the rhizoplane o f rice (Asanum a et al., 1980), where it inhibited fun-gal pathogens (L ee et al., 1990).

4 . H e a v y - M e t a l B i n d e r s a n d P h y t o c h e l a ti n sPlant ro ots exude a variety of organic chemicals, such as organic acids, with strong bind-

ing capacities fo r he av y metals (Sm ith et al., 1 982; van Steveninck e t al., 19 87, 1990 ). Thesechemicals p rote ct all the organisms that share the rhizosphere fro m heavy=metal ox icity. Theresult seems to be that rhizoplane microbes are m ore sensitive to heavy=metal ox icity han arerhizosphere microbes (Smith e t al., 1 98 2). Several aquatic and wetland plants, especiallyfloating on es such as Azzola and the water hyacinth, have been sho wn to have m etal=bindingpeptides (Zolotukhina et al., 1989), to absorb heavy metals from the water, to accumulatethem in their roots and upper parts (W olverton & McD onald, 1978; Sela et al. , 1988), and to


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have some resistance to their toxicity (Nir et al. , 1990). Similar observations have b een re-ported for the emergent macrophyte Sparganium androcladum (Balch & Jones, 1991).

Phytochelatins m ay be th e principal heavy-metal complexing peptides of higher plants(Grill et al., 1985; Steffens, 1990). T he y are metallothionein-like in function but dif fer in theirchemical structure and compo sition (L-cystein, L-glutamate, and glycine at a ratio o f 4:4:1).Th e synthesis o f these peptides can be induced by copper, mercury, lead, and zinc. Th eirchemical formula seems similar for all metals and for all plants examined. Phytochelatinshav e been reported f rom several aquatic and wetland plants as well. Salt et al. (I 989) and Ro b-inson and Thurman (1986) found such copper-binding peptides in M imulus guttatus, and wa-ter hyacinth co ntained peptides that bound cad mium (Fujita & Kaw anishi, 1 98 6; Fujita &Nakano, 1988).

Oth er organic com pounds o f plant origin also bind hea vy metals in the aquatic environ-ment. W etzel (1991) discussed the role o f plant-derived humic substances in detoxifyinghea vy metals in w etland and aquatic environments. Thurman and Rankin (1982) reported onthe role o f organic acids in zinc tolerance b y Descha mpsia caespitosa. Neori, Bitton, Kane,and Clark (un published) ha ve observed significant detoxification o f cop per by as-yet-unidentified ro ot exudates from axenic arrowhead (Sagittaria sp.) seedlings.

Chelating substances m ay have oth er effec ts in the rhizosphere, which deserve further re-search. The chelating chem ical EDT A is toxic to plants because it comp lexes essential metalsand makes them unavailable (Karataglis, 1978).

5 . A l l e lopa thyAllelopathy is the inhibition o f one plant species through chemical means b y another plant(Szczepanski, 1977; Rice, 1984; Friedman & W aller, 1985; Putnam, 1985). Th e issue o fall e-lop athy m ay be con troversial, particularly with aquatic plants (of. Inderjit & d e Moral, 1997).

Ho w ever, the authors o f tw o excellent reviews h ave evaluated and discussed it in detail andhav e shown th e ecological relevance o f allelopathy in wetlands (G opal & G oel, 1993; Hoots-roans & Blindow, 1994). In the present discussion, w e have tried to avoid semantics and con-sider allel op ath y in its widest functional con notation, including eve n plant-inhibitingchemicals p roduced by microbial mod ification o f the plant exudates or released from decay-ing plants.Ailelopathy b etween w etland plants has been observed often, bo th experimentally an d inthe field (e.g., Cheng & R iemer, 1988; see the comprehensive review in Gopal & Goel, 1993).In a recent study, Hizkiahoo-Shak (1996) reported on numerous experimental instances ofspecific apparent allelopathic interactions amon g aquatic macrophy tes. Som e o f the mo stwidespread wetland p lants have been reported to be involved in allelopathic interactions. A c-cording to Elakovich and Woo ten (1987b, 1989), Gopal and G oel (1993), and Szczepanski(1977), allelopathic chem icals and interactions occ ur in man y wetland gen era, including thewidespread Acer, Ca rex, Cyperus, Eleocharis, Hydrilla, M yriophyllum, Panicum , Peltandra,Phragm ites, Potamo geton, Polygon um, Sagittaria, Sm ilax, and Typha (Table I). Ag ami andW aisel 0 9 8 5 ) described specific allelopathic bilateral inhibition of growth between Najasmarina and Myriophyl lum spicatum. Th ey also reviewed o ther such cases involving Cerato-phyllum, Hyd rilla, Typha, and Vallisneria.Plants o f the generaAm brosia, Peltandra, Bidens,and Typha we re shown to produce plant-growth inhibitors (Thompson, 19 85; briefly re-view ed in Laksman, 1987). Plants in the genera Cyperus, D igitaria, and Euphorbia , all ofwhich include aquatic species, show widespread allelopathic activity (Elmore, 1985). Thewater shield (Brasenia schreberi) produced strongly allelopathic chemicals (Elakovich &


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B IO A C T IV E C H E M IC A L S IN R H IZ O S P H E R E S O F W E T L A N D P L A N T S 3 61

W o o ten , 1 9 87 a). B o th i t an d th e sp ik e ru sh (Eleocharis sp p . ) o f t en k eep o th e r p l an t s an d a lg aeo u t o f t h e i r n e i g h b o r h o o d . Eleocharis coloradoensis s h o w e d e f f e c t i v e a ll e l o p a th y t o w a r d P o -tamogeton sp. a n d E l o d e a sp . (F ran k & D ech o re tz , 1 9 8 0 ). I t is t h e re fo re o b v io u s th a t a l l e lo p a -t h y i s a d r i v i n g f o r c e i n t h e c r e a t io n o f a w e t l a n d p l an t c o m m u n i t y .U n f o r t u n a t e l y , t h e c h e m i c a l s i n v o l v e d h a v e n o t b e e n i d e n ti f ie d i n m a n y f u n c t io n a l s t u di e sa n d o b s e r v a t i o n s o f a ll e l o p a th y b e tw e e n w e t l a n d p l an t s ( G o p a l & G o e l , 1 9 93 ). H o w e v e r ,th e re i s a g ro w in g b o d y o f id en t i f i ed a l l e lo p a th ic ch em ica l s f ro m w et l an d p lan t s an d th e i rro o t s ( c f . G o p a l & G o e l , 1 9 9 3 ) . A l l e lo p a th ic ch em ica l s b e lo n g to sev e ra l ch em ica l g ro u p s ,p a r t i cu la r ly p h en o l i c s (H ag lan d & W i l li am s , 1 9 85 ) , o rg an ic ac id s (R ao & M ik k e l sen , 1 9 7 7) ,p l a n t h o r m o n e s a n d m e t a b o l i t e s o f p l a n t- a r o m a t ic a m i n o a c id s ( G u n n i s o n & B a r k o , 1 9 8 8 a ,1989), a lkalo ids , f lavon id s , terpen o ids , s tero ids (Mc Clure , 1970) , long-c hain fa t ty acids , a lo -m o n es , an d e l em e n ta l su l fu r ( c f . G o p a l & G o e l , 1 9 93 ).Eleocharis i s p e r h a p s t h e m o s t s t u d i e d w e t l a n d g e n u s c o n c e r n i n g c h e m i c a l s a n d m e c h a -n i sm s in v o lv ed w i th i t s a l l e lo p a th ic cap ab i l i t y (E lak o v ich & Wo o ten , 1 9 8 7 b ) . A n d er so n(1 9 8 5 ) an d S tev en s an d Mer r i l l (1 9 8 0 ) r ep o r t ed o n d ih y d ro ac t in o d io l id e (D A D ) f ro m Eleo-charis sp . an d o n th e in h ib i to ry e f f ec t s o f th is co m p o u n d o n o th e r aq u a t i c p l an ts , su ch as Pota-mogeton nodos . The a l l e lo p a th ic ch em ica l s a re r e l eased e i th e r ac t iv e ly to th e rh i zo sp h ere inso lu b le o r v o la t i l e fo rm s o r o n ly a s ce l l s d i e , slo u g h off , o r a re a t t ack ed b y p a th o g en s (P u t -nam, 1985) .

S e v e r a l b i o a c t i v e c h e m i c a l s p r o d u c e d b y p l a n ts a n d s o i l m i c r o b e s p e r s i s t l o n g e r in a n a e r o -b ic so i l s t h an in ae ra t ed o n es . F o r in s t an ce , h u m ic an d fu lv ic ac id s , an ae ro b ic m e tab o l i t e s th a tp e r s i s t i n w e t l an d so i l s an d r i ce p ad d ies , i n h ib it ed g ro w th o f o th e r p lan t s th ro u g h in h ib i tio n o fn o d u l a t i o n ( H a g l a n d & W i ll ia m s , 1 98 5) . B e c a u s e t h e s a m e p r o c e s s m a y o c c u r w i th o t h e r a l le -lo p a th ic ch em ica l s , a l l e lo p a th y m a y b e m o re e f f ec t iv e in w e t l an d s th an in t e r re s t r i a l eco sy s -t em s ( c f . G u n n i so n & B ark o , 1 9 88 a), ev en th o u g h th e ro o t - to - sh o o t r a t io in aq u a t ic p l an t s i sm u ch lo w er th an i s t h a t o f t e r r e s t ri a l p lan ts ,

T h e ex a c t m e ch an i sm o f a l le lo p a th ic in h ib i t io n in th e so i l is u su a l ly n o t id en t i f ied u n e-q u i v o c a l l y , b u t s e e d l in g s o f s w e e t g u m (Liquidamb ar styraciflua) h a d t h e i r m i n e r a l c o m p o s i -t i o n s c h a n g e d u p o n e x p o s u r e t o r h iz o s p h e r e e x u d a t e s o f t he f e s c u e Festuca arundinacea( W a l t e rs & G i l m o r e , 1 9 76 ). D A D f r o m Eleocharis sp ., m en t io n ed a b o v e , a t co n cen t ra t io n sab o v e 5 m g / l , i n h ib i t ed seed g e rm in a t io n an d seed l in g g ro w th in o th e r aq u a ti c p l an t sp ec ies(A sh to n e t a l ., 1985).

A l l e l o c h e m i c a l s o f t e n h a v e m e d i c i n a l p r o p e r ti e s . M e m b e r s o f t h e A s t e r a c e a e f a m i l y , i n-c l u d i n g s u c h w e t l a n d g e n e r a a s Baccha ris , Bidens, Callilepsis , Erigeron, Fra nseria, a n d P a r -thenium, o f t e n p r o d u c e a n e f f e c t i v e a i l e lo c h e m i c a l , s e s q u i te r p e n e l a c t o n e ( S t e v e n s & M e r ri ll ,1 9 85 ) . In a case d i scu ssed in th e sec t io n o n ch em ica l s w i th m ed ic in a l p ro p er t i e s , a m ac ro cy c-l ic t r i c h o t h e c e n e m y c o t o x i n w i t h a p h y t o t o x i c a c t iv i t y is p r o d u c e d b y t h e r h i z o s p h e r e f u n g u sMyrothecium spp. Baccharis megapotamica, w h ich i s n o t sen s i t iv e to th e to x in , s l ig h t ly m e-t ab o l i zes th e ch em ica l , m ak in g i t m o re p h y to to x ic an d a lso , i n c id en ta lly , an t i can ce ro u s ( Ja r -v i s e t a l ., 1 9 85 ) . N ico l l i e r e t a l . (1 9 8 5 ) fo u n d p h y to to x ic ch em ica l s in p lan t s o f th e w e t l an dg e n e r a Erigeron, Euphorbia, Polygonum, and Smilax . T h e i r a l l el o pa t hi c c o m p o u n d s - - c o u -m a t i n , o - e o u m a r i c a c id , a n d m e l il o t ic a c i d - - a r e a l s o a n ti b a ct e ri a l.M a c r o p h y t e - a l g a l a n t a g o n i s m i s w i d e s p re a d a n d h a s o f t e n b e e n s h o w n t o b e c h e m i c a l l yb a s e d . V a n A l l e r e t a l. ( 1 9 8 5 ) re p o r t e d o n t h e i n h ib i ti o n o f a l g a e - - a n d z o o p l a n k t o n - - b yc h e m i c a l s e x t r a c t e d f r o m Potam ogetonfoliosus and Anach aris canad ensis . O x y g e n a t e d f a t tya c i d s p r e s e n t i n w a t e r e x t r a c t s o f Eleocharis microcarpa s t r o n g ly i n h ib i te d m a n y b l o o m -f o r m i n g a l g a l s p e c i e s, e s p e c i a l ly c y a n o b a c t e ri a . S i m i l a r c o m p o u n d s w e r e a l s o f o u n d i n e x -t r a c ts f r o m o t h e r a q u a t ic s p e c i e s o f t h e g e n e r a Potamogeton, Najas, Thalassia, Ruppia, n u -


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m e r o u s a l g a e , a n d w a t e r f r o m s e v e r a l n a t u r a l p o n d s , e s p e c i a l l y o n e w i t h d e n s e s t a n d s o fEleocharis microcarpa.

A p p a r e n t l y , a l l e l o p a t h i c c h e m i c a l s a r e r e l e a s e d t o t h e e n v i r o n m e n t u n d e r n a t u r a l c o n d i -t i o n s . L e o n ( 1 9 9 2 ) e x a m i n e d t h e l i te r a t u r e o n a l le l o p a t h y i n th e m a r s h p l a n t s Spartina patens,Distichlis spicata, Juncus roemerianus, a n d Scirpus olneyi. C h e m i c a l c o m p e t i t i o n in t h e so i l,b e t w e e n t h e u n d e r g r o u n d p a r t s o f t h e p l an t s , w a s c o n s i d e re d p r o m i n e n t i n d e t e rm i n i n g t h ed e n s i t y a n d d i s t r ib u t i o n o f t h e f o u r s p e c ie s . S a x e n a a n d K u l s h r e s h t h a ( 1 9 9 2 ) r e p o r t e d t h a t d e -c o m p o s i n g r o o ts o f Lantana s p . i n h i b i t e d a n d k i l l e d w a t e r h y a c i n t h . T h e l a t t e r w e e d , h o w -e v e r , w a s s h o w n t o b e a b l e t o p r o t e c t i t s e l f f r o m a l l e l o p a t h i c i n t e r fe r e n c e : I t c o u l d e f f e c t i v e l ym e t a b o l i z e c e r t a i n p h e n o l i c c o m p o u n d s w i t h a l l e l o p a t h i c a c t i v i t y , p a r t i c u l a r l y p h e n o l i t s e l f .R a t e s o f u p t o 0 .4 g / l c o u l d b e to l e r a te d a n d m e t a b o l i z e d ( B r u m m e t & O ' K e e f e , 1 98 2) . B e -c a u s e p h e n o l s a r e c o m m o n p r o d u c t s o f p la n t s, i n c lu d i n g w e t l a n d p l a n t s ( H a g l a n d & W i l-l i a m s , 1 9 85 ), t h i s c a p a b i l i t y g i v e s t h e w a t e r h y a c i n t h a n a d v a n t a g e i n a l l e lo p a t h i c c o n f l i c tsa n d m a y p l a y a r o le i n it s c o m p e t i t i v e n e s s . C o n v e r s e l y , s o m e a q u a t i c p l a n t s a r e s e n s i t i v e to a l -l e l o p a t h i c c h e m i c a l s . T h e a q u a t i c p l a n t L e m n a m i n or h a s b e e n e v e n u s e d i n a s s e s s i n g a l l e l o -pa th ic e f fec t s (And erson , 1985 ; E inh e l l ig e t a l. , 1985).

I V . M e d i c i n a l P r o p e r t ie s o f W e t l a n d P l a n t sB e c a u s e w e t l a n d p l a n t s o f t e n c o n t a i n h i g h l y b i o a c t i v e c h e m i c a l s , i t i s n o s u r p r i s e t h a t th e s e

p l a n t s a r e o f t e n o f u s e t o h u m a n k i n d . N u m e r o u s r e p o r t s o n t ra d i t io n a l u s e s o f a q u a t i c p l a n t s a ss o u r c e s o f p o i s o n s a g a i n s t f i s h a n d o t h e r a q u a t i c a n i m a l s a p p e a r i n C o s t a - P i e r c e e t a l. ( 1 9 9 1 ) ,a n d s e v e r a l r e p o r t s o n t h e m e d i c in a l u s e s o f w e t l a n d p l a n t s a p p e a r b e l o w . Y e t m o s t p l a n t s p e -c i e s in t h e w o r l d h a v e n o t b e e n s u r v e y e d i n m o d e m t im e s f o r t h e ir c h e m i c a l o r b i o l o g i c a ll y a c -t i v e c o n s t i tu e n t s ( B a l a n d r i n e t a l. , 1 9 8 5; C o x & B a l i c k , 1 9 9 4 ). S u c h i n f o r m a t i o n o n p l a n t s t h a th a v e b e e n s u r v e y e d c a n b e f o u n d i n t h e l it er a tu r e o f m o d e r n m e d i c i n e a n d o f e t h n o m e d i c i n e ,t h e s c i e n c e t h a t p r e s e r v e s m e d i c a l k n o w l e d g e o f t r a d it i o n a l c u l tu r e s . T h e r e i s s u b s ta n t i a lk n o w l e d g e a b o u t th e m e d i c i n a l p r o p e r t i e s a n d v a l u e o f p la n t s ( T a b l e I I ; T a y l o r , 1 9 4 0 ;M i l l sp a u g h , 1 9 74 ; L e w i s & E l v i n - L e w i s , 1 9 77 ; B a l a n d r i n e t a l. , 1 9 8 5; D u k e , 1 9 86 ; C o x &B a l i c k , 1 9 94 ). B i o a c t i v e p l a n t c h e m i c a l s f r o m w e t l a n d s h a v e b e e n w i d e l y u s e d i n b o t h "p r i m i -t i v e " a n d " m o d e r n " c u l tu r e s . A l a r g e f r a c t i o n o f p l a n t s t ra d i t i o n a l ly c u l t i v a t e d f o r m e d i c i n a lp u r p o s e s c a m e f r o m w e t l a n d s o r h a d c l o s e l y r e l a te d w e t l a n d s p e c i e s (e . g ., S t o c k b e r g e r , 1 9 27 ).

A . WE T L A N D P L A N T S I N T R A D I T I O N A L ME D I C I N ET h e u s e o f w e t l a n d p l a n t s i n m e d i c i n e r e fl e c ts t h e i m p o r t a n c e o f w e t la n d p l a n t c h e m i c a l s

t o h u m a n k i n d . O v e r t h e m i l le n n i a , t r a d i ti o n a l c u l t u r e s h a v e c o l l e c te d m u c h p r a c t i c a l k n o w l -e d g e a b o u t t h e m e d i c i n a l p r o p e r t ie s o f pl a n ts . M u c h o f t h is i n f o r m a t i o n i s n o w b e i n g l o s t , b u tt h e m e d i c i n e s o f se v e r a l p e o p l e s h a v e b e e n d o c u m e n t e d . T h e e x p e r i e n c e o f t h e se p e o p l e s m a yt e a c h u s t o i d e n t i f y p l a n t s w i t h b i o a c t i v e i n g r e d i e n t s t h a t m o d e r n s c i e n t i s t s h a v e n o t y e t d is -c o v e r e d ( C o x & B a l i c k , 1 9 9 4 ) .

N a t i v e A m e r i c a n s u s e d a p p r o x i m a t e l y 2 5 % o f p l a n t s in t h e U n i te d S t a te s a s m e d i c i n e s ,a n d a b o u t 1 0 % o f a l l p l a n t s i n t h e w o r l d h a v e m e d i c i n a l v a l u e ( D u k e , 1 9 86 ). A l t h o u g h n o t a l lo f t h e p l a n t s i n u s e a r e e f fe c t i v e , it h a s b e e n e s t i m a t e d t h a t n e a r l y 4 0 % o f th e p l a n t s u s e d a c t u -a l l y c o n t a i n c h e m i c a l s w i t h t h e d e s i re d m e d i c a l i n f l u e n c e . O n e o f t h e b e s t - k n o w n c a s e s i s t h ew i l l o w , Salix, u s e d b y N a t iv e A m e r i c a n s f o r t h e s a m e p u r p o s e s f o r w h i c h m o d e r n m e d i c in eu s e s i t s a c t i v e c o m p o u n d , s a l i c y l i c a c i d , o r a s p ir i n . T h e r o o t s o f m a n y o t h e r w e t l a n d p l a n t ss e r v e d t o p o i s o n , d i s i n f e c t , p r e v e n t i n f e c ti o n , a n d p r e v e n t i n f l a m m a t i o n .


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W e e n e n e t a l . ( 1 9 9 0 ) e x a m i n e d t h e a n t i m a l a r i a l a c t iv i t y o f r o o t e x t r a c t s f r o m s e v e r a lp l a n t s u s e d i n t r a d it i o n a l T a n z a n i a n m e d i c i n e . O f t h e t h r e e m o s t e f f e c t i v e e x t r a c t s, o n e c a m ef r o m t h e c o m m o n w e t l an d p l a n t Cyperus rotundata. A n o t h e r c o m m o n w e t l a n d p l an t , Acoruscalamus ( s w e e t f l a g ), w a s w i d e l y u s e d f o r m e d i c i n a l p u r p o s e s i n N o r t h A m e r i c a , a s w e l l a s i nI n d i a ( S i v a r a j a n , 1 9 94 ).

O f t h e 5 5 g e n e r a t y p i c a l a n d p r e v a l e n t i n F l o r i d a w e t l a n d s ( R . B e s t , p e rs . c o m m . ) , a t l e a s tt h e f o ll o w i n g 2 6 g e n e r a w e r e m e d i c a l l y u s e d b y N a t i v e A m e r i c a n s ( c o m p i l e d f r o m d a t a i nL e w i s & E l v i n - L e w i s , 1 9 7 7 ; D u k e , 1 9 8 6 ): Acer, Cephalanthus, Comus, Fraxinus, Hyperi-cure , I lex , Lachnanthus, Lem na, Liquidambar, M agnol ia, M yrica , Nu pha r, Nym phaea,Nyssa, Oron tium, Persea, P oligala, Pontederia, Rhexia, Sab atia, Sagit taria, Salix, Sarrace-nia, Saururus, Typha , and Xyris. O n l y n i n e o f th e s e 2 6 g e n e r a d o n o t a p p e a r i n th e l i s ts o fp l a n t s w i t h s c i e n t i f i c a l l y p r o v e d m e d i c a l a c t i v i t y i n T a b l e s I , I I I , I V , a n d V (Liquidambar,Nyssa, Oron tium, Poligala, Pontederia, Rhexia, Saba tia, Saururu s, a n d Xyris).

B . C H E M I C A L S F R O M W E T L A N D PL A N T S I N MO D E R N ME D I C IN EI t is b e y o n d o u r e x p e r t i se t o p r o v i d e a t h o r o u g h r e v i e w o f w e t la n d p l a n ts i n m e d i c in e .

T h e r e f o r e , w e c i te o n l y a f e w c a s e s o f m e d i c a l l y a c ti v e o r u s e fu l c h e m i c a ls f r o m t h e r o o ts o fw e t l a n d p l a n t s t o i l l u s t r a t e o u r p o i n t . L a k s m a n ( 1 9 8 7 ) r e v i e w e d e v i d e n c e f o r t h e m e d i c i n a lp r o p e r t i e s o f c h e m i c a l s f r o m w e t la n d p l a n t s. A n t i tu m o r a c t i v i ty w a s f o u n d i n Spartina alter-nif lora, S. patens, Juncus roem erianus, Sag it taria falcata, a n d Phragmites australis, an dp o l y s a c c h a r i d e s e x t r a c t e d f r o m Typha w e r e s h o w n t o c o a g u l a t e b l o o d . J a r v i s e t a l. ( 1 9 8 5 ) d e -s c r i b e d a n a l l e lo p a t h i c a n d p o i s o n o u s c h e m i c a l o r ig i n a t i n g f r o m r o o t s ofBaccharis megapo-tamica t h a t a l s o h a d a n t i c a n c e r o u s p r o p e r t i e s . T h e c h e m i c a l w a s a m a c r o c y c l i e tr i c h o t h e c e n e ,a m y c o t o x i n w i t h o u t a n t ic a n c e r o u s p r o p e r ti e s , p ro d u c e d b y t h e f u n g u s Myrothecium s p p , A p -p a r e n t l y , t h e f u n g u s l i v e s o n th e p l a n t ro o t s a n d p r o d u c e s t h e n o n a n t i c a n c e r o u s t o x i n , w h i c h i sv e r y p h y t o t o x i c , b u t n o t t o Baccharis . The s p e c i e s B. megapotamica s l i g h t l y m e t a b o l i z e s t h ec h e m i c a l , m a k i n g i t a n t i e a n c e r o u s t o o . T h i s s e e m s l i k e a e a s e o f s y m b i o t i c a s s o c i a t i o n t h a tc o n f e r s o n t h e p l a n t n o t o n l y a m e d i c i n a l v a l u e b u t a l s o , p o s s i b l y , a c h e m i c a l a n t i m i c r o b i a l o ra n t i v i r a l d e f e n s e . O t h e r p l a n t s p e c i e s t h a t h a r b o r th i s f u n g u s p o s s e s s t h e c h e m i c a l i n i ts o r i g i -n a l f o r m , w h i c h i s t o x i c b u t n o t a n t i c a n c e r o u s . Urtica dioica, r e p o r t e d a b o v e t o c o n t a i n q u i te af e w p h e n o l i c a n d t e r p e n o i d c o m p o u n d s , h a s b e e n u s e d t o tr e a t p r o s t a ta h y p e r p l a s i a ( K r a u s &S p i t e l l e r, 1 9 90 ). S e v e r a l c h e m i c a l s t h a t h a d c o n f i r m e d a c t i v i t y a g a i n s t s t a n d a r d a n t i t c a n c e rt e st s o f t h e N a t i o n a l C a n c e r I n s t i tu t e h a v e b e e n e x t ra c t e d f r o m t h e c o m m o n s a l t- m a r s h p l a n tsJuncus roemerianus (need le rush) (Mi les e t a l . , 1981) .

V . D i sc us s io nA p i c t u r e o f th e " t y p i c a l " w e t l a n d p l a n t c a n b e d r a w n f r o m t h e e x t e n s i v e l i te r a t u r e r e -

v i e w e d h e r e . T h i s w e t l a n d p l a n t n o t o n l y i s w e l l a d a p t e d t o i t s h a r s h e n v i r o n m e n t b u t a l s oc o n t r o l s t h e c h e m i c a l a n d b i o l o g i c a l e n v i r o n m e n t o f i t s r h i z o s p h e r e . T o d o s o i t i s i n v o l v e d i na c o m p l e x a r r a y o f c h e m i c a l i n t er a c ti o n s , m o s t o f w h i c h o c c u r a t t h e rh i z o sp h e r e . T h e s e i n -e l u d e e m p l o y i n g a l l e i o p a t h i e c h e m i c a l s i n c o m p e t i t i o n f o r s o i l s p a c e w i t h o t h e r p l a n t s , e m -p l o y i n g p e s t - c o n t r o l c h e m i c a l s f o r th e c o n t r o l o f m i c r o b ia l a n d a n i m a l p e s t s, a n d c h e m i c a li n h i b i ti o n a n d r e s o u r c e c o m p e t i t i o n w i t h m i c r o b i a l c o m p e t i t o r s , s u c h a s n i t r if i e r s. T h e " t y p i -c a l " p l a n t c a n a l s o c h e m i c a l l y e x t r a c t p r e c i p i t a t e d n u t ri e n t s, s u c h a s ir o n a n d p h o s p h a t e , f r o mt h e s o i l, d e t o x i f y h e a v y m e t a l s, a n d d e t o x i f y m e t a b o l i t e s o f a n a e ro b i c m e t a b o l i s m f r o m t h en e i g h b o r i n g b u l k s o i l .


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364 TH E BO TA N I CA L REV I EW

F o r t h e s e a c t i v it ie s t h e w e t l a n d p l a n t u ti li z e s e i t h e r b y - p r o d u c t s o f i ts o w n m e t a b o l i s m o r" m a d e - t o - o r d e r " c h e m i c a l s . T h e w e t l a n d p l a n t i s a l s o a ff e c t e d b y m e t a b o l i t e s a n d c h e m i c a l s ,s u c h a s e n z y m e s , re l e a s e d t o t h e s o il b y i t s d e a d a n d d a m a g e d t is s u e s o r p r o d u c e d i n o r n e a r i t sr h i z o sp h e r e b y o t h e r o r g a n is m s .C o n c e r t e d s c i e n t if ic e f f o r t is r e q u ir e d t o f i ll th e m a n y g a p s i n o u r k n o w l e d g e o f c h e m i c a la n d b i o c h e m i c a l i n te r a c ti o n s i n t h e rh i z o s p h e r e s o f w e t l a n d p l a n t s a n d o f h o w t h e y i n f l u e n c ew e t l a n d f u n c ti o n s . C o n v i n c i n g e v i d e n c e i s s p a rs e o n c h e m i c a l a c ti v it ie s i n s u c h r h i z o s p h e r e s ,p r o b a b l y b e c a u s e m o s t o f t h e a v a i l a b l e in f o r m a t i o n o n b i o a c t iv e c h e m i c a l s h a s b e e n p r o d u c e di n d is c i p l in e s s u c h a s a g r ic u l tu r e , e n t o m o l o g y , to x i c o l o g y , m e d i c i n e , c h e m i s t ry , a n d p h y t o p a -t h o l o g y , n o t ty p i c a l l y in v o l v e d y e t i n w e t l a n d r e s e a rc h . H o w e v e r , w e h a v e f o u n d m a n y " l e a d s "t h a t re q u i r e f u r t h e r in v e s t ig a t io n . S u c h l e a d s e n c o m p a s s o b s c u r e p u b l i c a ti o n s , e v i d e n c e o f b i o -a c t i v e c h e m i c a l s f r o m " u p l a n d " r e l a ti v e s o f w e t l a n d p l a n t s , a n d c h e m i c a l s w h o s e b i o a c t i v i ty i nt h e l a b o r a t o r y h a s n o t b e e n c o n f i r m e d i n s itu . W e a r e a w a r e o f e x a m p l e s i n w h i c h s p e c i e s o f th es a m e g e n e r a d i f fe r c h e m i c a l l y . H o w e v e r , th e p r o b a b i l it y is h ig h e r t h a n r a n d o m t h a t a n u n s tu d -i e d w e t l a n d s p e c i e s h a s b i o a c t i v e c h e m i c a l s i f o t h e r s p e c i e s i n i ts g e n u s , f a m i l y , o r o r d e r a r e a l -r e a d y k n o w n t o h a v e t h e m ( C o x & B a l i c k , 1 9 9 4 ). F o r e x a m p l e , t h e s a lt m a r s h s p e c i e s Suaedamonoica ( C h e n o p o d i a c e a e ) b e l o n g s t o t h e o r d e r C e n t r o s p e r m a e . A s p r e s e n t e d a b o v e , m a n yp l an t s i n th i s o r de r con t a i n b i oac t i ve be t a l a in s . Such a ch em i ca l is t he r e f o r e m or e l i ke l y t o bef o u n d i n t h e r o o t o f th i s s p e c i e s t h a n i n t h e r o o t o f s p e c i e s f r o m o t h e r o r d e r s.

A t a n t a l i z in g q u e s t i o n r e m a i n s : W h a t i s th e r o l e o f e a c h ro o t b i o a c t i v e c h e m i c a l o r p o i s o ni n c o n t r o l l in g r h i z o s p h e r e p e s t s , o n o n e h a n d , a n d i n m o d i f y i n g r h iz o s p h e r e h i o g e o c h e m i c a lp r o c e s s e s , o n t h e o t h e r h a n d ? S p e c i f i c re p o r t s o f a c h e m i c a l b i o a c t i v i t y in a w e t l a n d p l a n t c a np r o b a b l y b e g e n e r a l i z e d : F o r in s t a n c e , i t i s p o s s i b l e t h a t w e t l a n d p l a n t s w i t h p o i s o n o u s a b o v e -g r o u n d p a r t s a ls o h a v e p o i s o n o u s r o o t s.P l a n t h o r m o n e s h a v e b e e n s h o w n h e r e t o e x i st in w e t l a n d s o i l s a n d r h i z o s p h e r e s i n re l a -t i v e l y h ig h c o n c e n t r a t io n s . O b v i o u s l y , a h o r m o n e t h a t a p p e a r s o u t o f t h e n a tu r a l r h y t h m c a nd e t r i m e n t a l l y i n fl u e n c e a p l a n t. B e c a u s e o r g a n i c c o m p o u n d s d e g r a d e s l o w l y in f l o o d e d s o i l s,o n e w o u l d e x p e c t w a t e r - s o l u b l e g r o w t h re g u l a t o r s t o p e r s i s t t h e r e l o n g e r a n d t h u s t o b e m o r ee f f ec t i ve t han t hey a r e in d r y so i l s (c f . G unn i son & B ar ko , 1989). I t is t he r e f o r e i n t r igu i ng t oi m a g i n e w h a t t h e p r o d u c t i o n a n d r e l e a s e o f a h o r m o n e i n to t h e f lo o d e d s o i l, b y e i th e r a p l a n to r a m i c r o o r g a n i s m , d o t o th e p l a n t c o m m u n i t y , t o t h e i n h a b i t a n ts o f i ts rh i z o s p h e r e , a n d t o t h ef u n c t i o n i n g o f a w e t l a n d .

P l a n t a n d m i c r o b i a l s i d e r o p h o r e s a n d p h y t o c h e l a t i n e s o c c u r i n ro o t s o f s e v e r a l w e t l a n dp l a n t s a n d s i g n i f ic a n t l y i n f lu e n c e i r o n m o b i l i z a t i o n a n d h e a v y - m e t a l d e t o x i f l c a t io n i n w e t -l a n d rh i z o s p h e r e s . T h e e v i d e n c e p r o v i d e d h e r e s u g g e s t s t h a t s u c h c h e m i c a l s c a n p r o v i d e t h ep l a n t s t h a t p r o d u c e t h e m w i t h t h e q u a d r u p l e f u n c t io n s o f m e t a l n u tr it io n , m e t a l d e t o x i fi c a t io n ,p e s t c o n t r o l, a n d a l le l o p a t h y .

A l l e l o p a t h y i s d i f fi c u l t a n d c o n t r o v e r s i a l to d e f i n e i n a w a y t h a t s a t is f ie s e v e r y o n e . E v e ns o , w e h a v e r e v i e w e d m a n y d o c u m e n t e d c a s e s o f a p p a r e n t a ll e lo p a t h y i n w e tl a n d p l a n t s a n da l le l o p a th i e c h e m i c a l s i n r o o t s y s t e m s o f w e t la n d p l an t s. T h e e x i s te n c e o f s o m a n y r e p o r t s o na l l e lo p a t h i c c h e m i c a l s a n d t h e i r e f fe c t s in w e t l a n d p l a n t s c o n f i r m s t h a t c o m p e t i t io n f o r s p a c ei n w e t l a n d s i s i n te n s e . T h i s c e r t a in l y d i s a g r e e s w i t h th e n o t i o n ( C r a w f o r d , 1 9 87 ; C r a w f o r d &B r a e n d l e , 1 9 96 ) t h a t w e t l a n d p l a n t s l iv e u n d e r c o n s t a n t a c u t e s t r e s s e s ( " c o m p a r a b l e t o l if e u n -d e r a p r o l o n g e d h e a r t a t t a c k " ; C r a w f o r d , p e r s . c o m m . ) t h a t re s u l t f ro m a n a e r o b i o s i s o f t h es o il . P l a n t s u n d e r s u c h s e v e r e s t r e ss , e a c h o n e f o r i ts e l f, w o u l d h a v e b e e n c o n s t a n t l y t r y i n g t oj u s t s u r v i v e th e e n v i ro n m e n t a l a t ta c k s o n t h e i r p h y s i o l o g y . T h e s u r v i v o r s w o u l d h a v e b e e nf e w a n d f a r b e t w e e n . U n d e r s u c h d i f fi c u l t c o n d i t io n s , p l a n t s a r e n o t a b l e a n d d o n o t h a v e t oc o m p e t e w i t h e a c h o t h e r , s o t h e y d o n o t n e e d a l le l o p a t h y . A c u t e h e a r t p a t i e n t s i n a h o s p i ta l


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B I O A C T IV E C H E MI C A L S I N R H I Z O S P H E R E S O F W E T L A N D P L A N T S 3 65

r a r e l y c o m p e t e w i t h e a c h o t h e r w h e n t h e y a r e f i g h t i n g f o r s u r v i v a l , a n d t h e y l e a v e m a n ye m p t y b e d s b e t w e e n t h e m . T h e c o n t e n t io n t h a t t h e e x i s te n c e o f a n e f f e c t i v e p h y t o t o x i n i n t h er o o t a n d r h i z o s p h e r e o f a p la n t f r o m a d e n s e l y v e g e t a te d , m u l t i s p e c ie s w e t l a n d c a n b e i n c o n -s e q u e n t i a l t o t h e s u c c e s s o f t h is p l a n t i s , i n o u r o p i n i o n , q u e s t i o n a b l e . A t th i s t i m e w e c a n o n l ys p e c u l a t e a b o u t w h e t h e r p l a n t - p l a n t c o m p e t i ti o n f o r s o il s p a c e - - w h i c h i s o f t e n c o m p e t i t io nf o r s u n li g h t, b e c a u s e n u t r i e n ts a n d w a t e r a r e a b u n d a n t i n f l o o d e d s o i l s - - i s f i e rc e r in w e t l a n d st h a n i n d r y - s o i l e n v i r o n m e n t s .

T h e l i m i t e d e v i d e n c e p r e s e n t e d h e r e a b o u t t h e m e d i c i n a l p r o p e r ti e s o f w e t l a n d p l a n ts ,f r o m b o t h e t h n o m e d i c i n e a n d m o d e m m e d i c i n e , s h o u ld b e e x t en d e d . W e a r e n o t q u a l if i ed t oe v a l u a t e t h e v a l i d i t y o f e a c h r e p o r t o n t h e m e d i c a l p o t e n c y o f a w e t l an d p l a n t, s o w e h a v e n o tt r i e d t o r e v i e w s u c h r e p o r t s c o m p r e h e n s i v e l y . I t i s p l a u s i b l e , h o w e v e r , t h a t , u p o n f u r t h e rs t u d y , i n t e r e s ti n g a n d e c o l o g i c a l l y s ig n i f i c a n t c h e m i c a l - b i o l o g i c a l i n t e r a c t io n s w i l l b e f o u n di n r h i z o s p h e r e s o f m e d i c i n a l w e t l a n d p l a n t s . I t i s o n l y l o g i c a l t h a t m e d i c i n a l c h e m i c a l s p er =f o r m f o r t h e p l a n t s t h a t p ro d u c e t h e m t a s k s o t h e r th a n p r o v i d i n g m e d i c in e s . F o r i n s ta n c e , t h ec h e m i c a l s t h a t c a u s e a p a s t e m a d e b y a s h a m a n f r o m Typha r o o t s to c o a g u l a t e h u m a n b l o o dm o s t p r o b a b l y a l s o c o a g u l a t e t h e b l o o d o f r o o t b o r e rs a n d k i l l t h e m .

V I . C o n c l u s i o nT h e i n i t i a l i n f o r m a t i o n c o l l e c t e d a n d s y n t h e s i z e d h e r e c l e a r l y d e m o n s t r a t e s t h e w i d e -

s p r e a d n a t u r e o f b i o a c t i v e c h e m i c a l s a n d c h e m i c a l - b i o l o g i c a l i n t e ra c t io n s i n w e t l an d r h i z o -s p h e r e s . E v a l u a t i o n o f t h e i n f o r m a t i o n i n t h i s r e v i e w a n d e d u c a t e d p r e d i c t io n s a b o u t t h ep o s s i b l e p r e v a l e n c e o f p l a n t b i o a c t i v e c h e m i c a l s i n w e t l a n d r h i z o s p h e re s c a n b e g r e a t l y f a c il i-t a t e d b y t h e s t u d y o f G r a i n g e a n d A h m e d ( 1 9 88 ) , a c o m p r e h e n s i v e c o l le c t io n o f i n f o r m a t i o no n p e s t - c o n t r o l c h e m i c a l s a n d p o i s o n s f r o m p l an t s. F r o m t h e 3 , 4 0 0 p l a n t s t h e y c a t a lo g e d a sc o n t a i n i n g p e s t - c o n t r o l a n d p o i s o n o u s c h e m i c a l s , m a n y - - a t l e a s t 1 7 0 , o r a b o u t 5 %o - - - w e r ew e t l a n d o r a q u a t ic m a c r o p h y t e s . M a n y m o r e c a t a l o g e d p la n t s p e c ie s w e r e n o t a q u a t ic b u t b e -l o n g e d t o g e n e r a t h a t c o n t a i n t y p i c a l a n d w i d e s p r e a d w e t l a n d s p e c i e s . T h e l a t te r s p e c i e s h a dn o t b e e n s t u d ie d w i t h r e s p e c t t o b i o a c ti v e c h e m i c a l s. A t t h e m o m e n t , w e c a n e x t r a p o l a te u s i n gt h e e x i s t i n g d a t a . A l i t tl e o v e r 1 % o f th e w o r l d ' s p l a n t s a r e i n c l u d e d i n t h e c a t a l o g o f G r a i n g ea n d A h m e d ( 1 9 8 8) . H o w e v e r , s t r ik i n g ly , o f t h e 5 5 p l a n t s p e c i e s t h a t a re c o n s i d e r e d m o s t t y p i -c a l o f w e t l a n d s i n t h e w e l l - s tu d i e d r e g i o n o f F l o r i d a (R . B e s t , p e rs . c o m m . ) , 3 6 - - 6 5 % o - - h a v ed o c u m e n t e d p e s t - c o n t ro l c h e m i c a l s ( G r a i n g e & A h m e d , 1 98 8) , a c t i v it y t h a t is p o i s o n o u s t ol a r g e a n i m a l s (M u e n s c h e r , 1 9 75 ; G r a i n g e & A h m e d , 1 9 8 8 ; T u r n e r & S z c z a w i n s k i , 1 9 9 1) ,a n d / o r m e d i c i n a l a c t i o n ( T a y l o r , 1 9 40 ; D u k e , 1 98 6) . F u r t h e rm o r e , 4 7 - - 8 5 % - - - o f t h e 55 p l a n tg e n e r a i n t h a t F l o r i d a g r o u p i n c l u d e s p e c i e s t h a t p o s s e s s a c t i v i t y in a t le a s t o n e c a t e g o r y o fb i o a c t i v i t y . O n a l a r g e r s c a l e , o f t h e 2 7 9 s p e c i e s o f F l o r i d a w e t l a n d p l a n t s t h a t a p p e a r i n th ep o p u l a r m a n u a l WetlandPlant Species o fFlorida (D ress ie r e t a l . , 1987), a t l eas t 26 % -- -40 %o f t h e g e n e r a - - w e r e f o u n d t o h a v e b i o a c t i v it y i n o n e o f th e t h re e c a t e g o ri e s . A s s u m i n g t h a tw e t l a n d p l a n t s i n F l o r i d a a r e n o d i f f e r e n t f r o m t h o s e i n t h e r e s t o f t h e w o r l d i n t h i s r e s p e c t , w ec a n c o n f i d e n t l y p r e d i c t t h a t , u p o n f u r t h e r e x a m i n a t i o n , a t le a s t s i m i l a r p r o p o r t i o n s o f t h ew o r l d ' s c o m m o n w e t l a n d a n d a q u a t i c p l an t s w i ll b e f o u n d to h a v e b i o a c t i v e c h e m i c a ls . I t i sb e y o n d t h e s c o p e o f th i s r e v i e w to a s s e s s w h e t h e r w e t l a n d p l a n t s in F l o r i d a - - o r e l s e -w h e r e - - - h a v e m o r e f r e q u e n t ly b i o a c t i v e c h e m i c a l s t h a n d o u p l a n d p l a n ts i n F l o r i d a - - -o r e l se -w h e r e - - b u t t h e p e r c e n t a g e c o m p a r i s o n w i th t h e G r a i n g e a n d A h m e d c a t a l o g s p e a k s f o r it se lf .I f f o u n d t o b e s o , o n e c o u l d e v e n i n te r p re t s u c h e v i d e n c e t o i m p l y t h a t t h e f a m i l i e s o f t e rr e s -t ri a l p la n t s w i t h t h e g e n e t i c d i s p o s i ti o n t o p r o d u c e d e f e n s i v e c h e m i c a l s w e r e m o r e s u c c e s s f u li n c o l o n i z in g t h e h a r s h b u t c o m p e t i ti v e w e t la n d e n v i r o n m e n t s .


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366 THE BOTAN ICAL REVIEW

It is an ou ts tanding addi t ional f ind ing , f rom on e o f the mos t in tensely s tud ied wet land re-g ions in t he wor ld , t ha t Nat ive A mer icans in F lo r ida u sed as med ic ines mo re than ha l f o f t hemo s t t yp ica l and com m on F lo r ida wet l and p l an ts , 65% o f t hem fo r a sc i en ti f ica l ly p roved rea -son . This suggests that, wi th m ore detai led s tud ies , such a s i tuat ion i s l ikely to be fou nd in theres t o f t he wo r ld ' s we t l ands .

W e conc lude tha t a l a rge f r ac t ion , perhaps more than ha l f, o f t he p lan t s i n t he wo r ld ' s w e t -l ands con ta in various b ioae t ive chemica ls , even though we do no t ye t know ho w m uch each o fthese ch em icals af fects wet land proc esses in quant i ta t ive terms, how the chem icals interact,o r even how fa r f rom the roo t s t hey d i f fu se and have an in f luence . Such d i ff i cul t ques tions ca l lfor novel ideas a nd techniques , such as the procedure ofT ippk ot te r e t al . (1986) fo r so i l th insect ions for b io logical s tud ies and the h igh-reso lu t ion pore-w ater gel sam pler of K ro m et a l.(1994) . W e can co nf ident ly assum e, howe ver , that such chem icals are involved to s ign i f ican tdegre es in pest co nt ro l , a l le lopathy , and o ther chem ical in teract ions wi th in the rh izosphereso f the p lan ts that p roduce them . The se act iv i ties probab ly p lay mo re s ign i f ican t ro les than i scu r ren t ly be l i eved in de t e rmin ing the b ioeco log ica l func t ion ing o f wet lands .

V I I . A c k n o w l e d g m e n t sM ost o f the l iterature on wh ich th is ar ticle i s based w as co l lected and sy nthesized dur ing a

sabba ti ca l ye ar t ha t A . N. spen t a t the D epar tmen t o f So i l and W ater Sc i ences, U n iver s i ty o fF lo r ida . W e thank K aren Bro wn and the Aqua t i c P l an t In fo rmat ion Cen te r , t he Cen te r fo rAquat i c P l an t s , and the s t a f f o f t he Mars ton Sc ience L ib ra ry o f t he Un iver s i ty o f F lo rida fo rthei r a id in assemb l ing the l iterature . A. N. thanks J . D ouc ha and the s ta f fa t the Ac ad em y ofSc iences o f the Czech Repub l i c, In s t it u te o f Microb io logy , Depar tmen t o f Au to t roph ic M i -c roo rgan i sm s a t T rebon , where the man uscr ip t was com ple ted . W e a re espec ia lly g ra te fu l t o J.Kv e t fo r r ev iewing the m anuscr ip t and fo r f ru it fu l d i scuss ions and m any u sefu l sugges t ions ,to N. R ea fo r cr it ical read ing o f an ear ly draf t o f the ar ticle, and to R. Ta dm or for technical a s-s i s tance. T he present ar t ic le owe s m uch also to several anony m ous rev iewers .

V I I I . L i t e r a t u r e C i te dAgam i, M . & Y. W aisel. 1985. Inter relationships between Najas marina and three oth er species ofaquatic macrophytes. Hydrobiologia 126: 169-173.& .1986. The ecophysiology of roots of submerged vascular plants. Physiol. V~g. 24:607-624.Aiiotta, G., M . Della-Greea, P. M onaco, G. Pinto, A. Pollio & L . Previtera. 1990. In vitro algalgrowth inhibition by phytotoxins of ~pha la t i fo l ia L. J. C hem. Ecol. 16: 2637-2646.~ - , A . Mol inaro , P. Monac o, G. Pinto & L. Previtera. 1992. Three biologically active pheny lpro-panoid glucosides from Myriophyllum verticillatum. Phytochemistry 31:109-111.A m m erm an, J . W . 1991. Role of ecto-phosphohydrolases n phosphorus regeneration in estuarine andcoastal ecosystems. Pp. 165-186 in R. J. C hr6st (ed.), M icrobial enzym es in aqu atic environm ents.Springer Verlag, New York.Andersen, F. O . & E. Kristensen. 1988. Oxygen microgradients in the rhizosphere of the mangroveAvicenia marina. M ar. Ecol. Prog. Ser. 44: 201-204.Anderson, W . J . L. 1985. Use of bioassays for allelochemicais in aquatic plants. Pp. 351-370 in A. C.Thom pson (ed.), The chemistry of allelopathy: Biochemical interactions am ong plants. Am ericanChem ical Society, Washington, DC.A rms trong, J. , W . Arm strong & P. M. Beckett . 1992.Phrag raites australis: Venturi- and hum idity-induced pressure flow s enhance rhizome aeration and rhizosphere oxidation. New Phytol. 120:197-207.


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A rm str on g, W . 1979. Aera t ion in h igher p lants ( rev iew). Advan ces Bot . Res . 7 : 225-332.~ , S . H . F . W . J u s t i n , P . M. B e c k e t t & S . L y t h e . 1 9 91 . R o o t a da pt ati on t o s o il w a te rl og gi ng .

Aqu at ic Bot . 39: 57-73 .A s a n n m a , S ., H . T a n a k a & M . Y a t a z a w a . 1 98 0. Pseudomonas cepacia: A characteristic rhizoplane

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