Preface ^N^OST
P E O P L E A R E A W A R E that s k u n k s a n d p o r c u p i n e s have
effective
w a y s to repel their enemies. W h a t they don't realize, and science is just n o w l e a r n i n g , is that plants also have defense systems.
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T h e o p h r a s t u s ( 2 8 5 B.C.) a n d , later, P l i n y r e c o g n i z e d the existence interference
among
plants and noted
its s i g n i f i c a n c e
of
in agriculture.
H o w e v e r , i n v o l v e m e n t o f p l a n t - p r o d u c e d c h e m i c a l s i n p l a n t - p l a n t interactions was first suggested by the Swiss botanist M . A . - P . de C a n d o l e i n 1832. In 1937, H a n s M o l i s c h c o i n e d the term allelopathy to i n c l u d e both h a r m f u l a n d b e n e f i c i a l b i o c h e m i c a l interactions between a l l types o f plants a n d interactions i n v o l v i n g m i c r o o r g a n i s m s . T h i s definition was later adopted by R i c e i n 1983 and is currently accepted. We w o u l d l i k e to i n c l u d e the p l a n t insect a n d the p l a n t - h i g h e r a n i m a l interactions i n the terms allelopathy a n d a l l e l o c h e m i c a l s for this book. The
nature o f a l l e l o c h e m i c a l s ; the m e c h a n i s m s a n d rates o f
their
e m i s s i o n f r o m the aggressive plant; their fate i n the soil; and their uptake, translocation, and mode
of
a c t i o n w i t h i n the
receptive plant are
all
processes that s h o u l d be studied. These processes w i l l be discussed i n the p l a n t - p l a n t , p l a n t - m i c r o o r g a n i s m , p l a n t - i n s e c t , a n d p l a n t - a n i m a l sections o f this book. In d e s c r i b i n g the allelopathic p h e n o m e n o n , understanding h o w the aggressive plant (the donor) avoids autotoxicity is also essential. In
indigenous
plant c o m m u n i t i e s , a l l e l o p a t h y
may
determine
the
d i s t r i b u t i o n patterns o f plants i n r e l a t i o n to their neighbors, whereas i n agriculture and forestry allelopathy m a y affect yields. F o r example, weeds w i t h allelopathic potential or crops that produce autotoxic aftereffects m a y reduce yields; conversely, u s i n g crops w i t h the a l l e l o p a t h i c p o t e n t i a l to decimate weeds m a y i m p r o v e yields. Agricultural Implications Incorporating allelopathy into a g r i c u l t u r a l management m a y reduce the use o f herbicides, fungicides, a n d insecticides; cause less p o l l u t i o n ; d i m i n i s h autotoxic hazards; etc. P l a n t s a n d soil w i t h their a l l e l o c h e m i c a l s or those a l l e l o c h e m i c a l s p r o d u c e d by associated m i c r o o r g a n i s m s , insects, or higher a n i m a l s c o u l d provide new strategies for m a i n t a i n i n g and increasing forest and a g r i c u l t u r a l p r o d u c t i o n i n the future. If the c h e m i c a l s are a l l e l o p a t h i c , they l e n d themselves
to b e c o m e
starting materials for the synthesis o f herbicides, pesticides, a n d fungicides xi
Waller; Allelochemicals: Role in Agriculture and Forestry ACS Symposium Series; American Chemical Society: Washington, DC, 1987.
that are not based o n p e t r o l e u m c o m p o u n d s , w h i c h are a p u b l i c health concern. We try to be responsive to the needs o f the p u b l i c . T h e r e must be an interactive w o r k i n g group c o m p o s e d o f foresters, entomologists, botanists, agronomists, biochemists, plant pathologists, a n d a n i m a l scientists to solve these research p r o b l e m s . O r g a n i z i n g this g r o u p w o u l d create c o o r d i n a t i o n problems as w e l l as funding problems. In spite o f these obstacles, the n u m b e r s o f scientists w o r k i n g w i t h allelopathy i n its v a r i o u s forms are increasing. Acknowledgments
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We thank e a c h o f the p a r t i c i p a n t s , b o t h domestic a n d f r o m a b r o a d , for sharing w i t h us the results obtained i n their studies o n a l l e l o c h e m i c a l s . We also w o u l d l i k e to thank the A m e r i c a n C h e m i c a l S o c i e t y for h o l d i n g the s y m p o s i u m upon w h i c h this b o o k is based because this is the third time they have honored this subject i n the past year a n d a half. GEORGE R.
WALLER
Department of Biochemistry Oklahoma Agricultural Experiment Station Oklahoma State University Stillwater, O K 74078 October 1985
xii
Waller; Allelochemicals: Role in Agriculture and Forestry ACS Symposium Series; American Chemical Society: Washington, DC, 1987.
Introduction .ALLELOCHEMICALS
have
already
been
shown
to i m p o s e
numerous
i m p a c t s i n c u l t i v a t e d a n d natural ecosystems. A l t h o u g h their influences were observed at least as far b a c k as the time o f Theophrastus ( 2 8 5 B.C.), the major progress i n this science has o c c u r r e d d u r i n g the past 2 5 years.
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O n l y d u r i n g that p e r i o d has the science gained credence a m o n g scientists of m a n y disciplines. T h e p h e n o m e n o n o f allelopathy m a y be unique i n that it p r o b a b l y
involves
more
scientific d i s c i p l i n e s than a n y other
single
phenomenon. T h e diversity o f disciplines and w i d e g e o g r a p h i c a l area represented i n this b o o k
are i n d i c a t o r s o f the w o r l d w i d e
importance
o f allelopathy.
A l l e l o p a t h y i m p a c t s v i r t u a l l y a l l the plant science and pestology disciplines as w e l l as m i c r o b i o l o g y and natural products chemistry. O n e o f m y greatest pleasures has been to see the disciplines c o m e together to create the c r i t i c a l mass necessary to study this science. F o u r recent i n t e r n a t i o n a l s y m p o s i a have fostered this i n t e r d i s c i p l i n a r y effort. N u m e r o u s research teams have gelled as a result o f these meetings. E l r o y Rice's fine b o o k has also served as a n i m p o r t a n t focus for this science. T h e science has n o w clearly entered its l o g a r i t h m i c phase o f growth. Challenge to All Disciplines A l l e l o p a t h i c interactions are c o m p l e x . I ' m aware o f no case where one c h e m i c a l has been u n e q u i v o c a l l y p r o v e n to e x p l a i n the entire situation. A l m o s t a l l a l l e l o p a t h i c interactions i n v o l v e not o n l y products o f higher plants but also those o f m i c r o b e s , either as enhancers o r detoxifiers. A l l cases require c h e m i c a l c h a r a c t e r i z a t i o n w o r k f o l l o w e d b y intensive studies by plant physiologists. S e l d o m can a l l the w o r k be a c c o m p l i s h e d w i t h i n one group. S i m p l y , this means w e must w o r k together. We should encourage that the term allelopathy be used i n its broadest sense (as intended b y H a n s M o l i s c h ) . A l l e l o p a t h y w o u l d l o g i c a l l y i n c l u d e the c h e m i c a l s p r o d u c e d b y m i c r o b i a l plants (Actinomycetes,
algae, fungi,
etc.) and those that enhance g r o w t h as w e l l as inhibit growth. We must refine o u r methods to prove allelopathy. M e r e l y g r i n d i n g up a plant and o b t a i n i n g a p h y t o t o x i n is not p r o o f o f allelopathy. W e urge that protocols
s i m i l a r to K o c h ' s postulates be f o l l o w e d
to d e v e l o p
proofs.
I m p r o v e d techniques are needed i n m a n y phases o f the w o r k . F o r example, we must be careful not to produce c h e m i c a l artifacts d u r i n g our extractions and separations. W e must f i n d better ways o f c o l l e c t i n g a l l e l o c h e m i c a l s xiii
Waller; Allelochemicals: Role in Agriculture and Forestry ACS Symposium Series; American Chemical Society: Washington, DC, 1987.
f r o m the rhizosphere. We have not yet identified p r o b a b l y 2 5 % o f the a l l e l o c h e m i c a l s p r o d u c e d by higher plants and microbes. E v e n i f we prove that allelopathy is i n v o l v e d i n plant interference, we should not forget that it is but one m e c h a n i s m that influences the eventual outcome i n plant c o m m u n i t i e s .
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Challenge to Crop and Forest Scientists T h e a p p l i e d aspects o f allelopathy should provide excitement for a g r i c u l tural scientists. A l l e l o c h e m i c a l s pose b o t h a p r o b l e m and an opportunity. A l l e l o c h e m i c a l s undoubtedly cost w o r l d agriculture b i l l i o n s o f dollars a n n u a l l y ; h o w e v e r , by g a i n i n g an understanding o f these natural m e c h a nisms, we c o u l d put them to w o r k to benefit agriculture. S e l d o m are plant rotations, tillage systems, c u l t i v a r selections, or p l a n t i n g c o n f i g u r a t i o n s planned w i t h the idea o f r e d u c i n g adverse allelopathic effects, m u c h less to exploit beneficial impacts. We don't even k n o w the best way to design our h o m e vegetable gardens. In recent years, A m e r i c a n farmers have been c h a l l e n g e d to p r o d u c e crops w i t h a profit m a r g i n . A l t h o u g h higher c o m m o d i t y prices and higher yields c a n enhance p r o f i t a b i l i t y , reduced input into p r o d u c t i o n w i l l also produce s i m i l a r results. W h e r e v e r possible, we should g a i n an understandi n g o f n a t u r a l m e c h a n i s m s a n d try to put them to w o r k i n a g r i c u l t u r a l p r o d u c t i o n systems. T h i s m a y a l l o w us to reduce some costly fuel and c h e m i c a l expenditures. L i t t l e is k n o w n about the potential to exploit m u t u a l i s m i n a g r i c u l t u r a l systems. A l m o s t a l l the w o r k to date has concentrated o n s y m b i o t i c nitrogen-fixers a n d m y c o r r h i z a l associations. A v a i l a b i l i t y o f soil nitrogen and phosphorus is a severe p r o b l e m i n m a n y areas o f the w o r l d . A l l e l o c h e m i c a l s m a y i m p a c t the a v a i l a b i l i t y o f these nutrients through effects o n the symbiotic microbes. We have g a i n e d some understanding o f autotoxicity and replant p r o b l e m s , w h i c h are c o m m o n i n p e r e n n i a l c r o p p i n g systems, but m u c h remains to be learned. These problems c a n cause serious e c o n o m i c losses, and m a n y appear to involve allelopathy. P l a n t s and m i c r o b e s w i l l undoubtedly be a r i c h source o f c h e m i c a l s that are b e n e f i c i a l to plant g r o w t h , y i e l d , or quality. S o m e interesting developments are n o w under way i n this r e a l m . I've often wondered w h y we haven't done more to exploit allelopathic plants to manage vegetation on our right-of-way lands. Steve H o r s l e y and others have shown that selected herbaceous species c a n v i r t u a l l y eliminate tree g r o w t h for as l o n g as 8 0 years. We've also done little to exploit a l l e l o p a t h i c turf grasses, a l t h o u g h excellent weed-suppressing types have been reported i n Lolium and Festuca. T h e w o r k o n d w a r f spikerush gives hope that we m i g h t manage aggressive aquatic plants w i t h nonweedy xiv Waller; Allelochemicals: Role in Agriculture and Forestry ACS Symposium Series; American Chemical Society: Washington, DC, 1987.
allelopathic species. A l l these examples c o u l d greatly reduce c h e m i c a l input into systems. Challenge to Plant Physiologists We k n o w very little about the fundamentals o f a l l e l o c h e m i c a l p r o d u c t i o n
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and release. M a n i p u l a t i n g a l l e l o c h e m i c a l s by i m p o s i n g the stress o n the o r g a n i s m w i l l p r o b a b l y be possible. D o plants release c h e m i c a l s as a result o f exposure to an alien species? has been done regarding defense to insect attack, but v i r t u a l l y on p l a n t - p l a n t responses has been done.
appropriate produce or M u c h work no research
T h e l i m i t e d w o r k o n m o d e o f action o f a l l e l o c h e m i c a l s suggests that they affect a variety o f sites a n d b i o c h e m i c a l processes, m a n y o f w h i c h are s i m i l a r to those affected by synthetic herbicides. M a n y n o v e l sites a n d m e c h a n i s m s probably r e m a i n to be discovered. P r o o f o f allelopathy c o u l d be strengthened i f more research was done to document uptake a n d fate o f a l l e l o c h e m i c a l s i n the recipient or suscept plant. We need to determine relative toxicities (selectivity) o f a l l e l o c h e m icals on the target species. W h a t m i g h t be the o u t c o m e o f a 3 0 % g r o w t h reduction d u r i n g only 2 weeks o f a plant's life cycle? P l a n t physiologists c a n contribute i m m e n s e l y i n the technology o f bioassay. Several i n vitro systems c o u l d prove useful w h e n more is k n o w n about the m o d e o f a c t i o n o f the c o m p o u n d s . These types o f assays m a y prove extremely useful i n m o n i t o r i n g t o x i c i t y t h r o u g h fractionations o f extracts or exudates. Challenge to Plant Ecologists A l t h o u g h ecologists have r e c o g n i z e d several possible m e c h a n i s m s for plant interference, they have s e l d o m determined the relative i m p a c t s o f v a r i o u s m e c h a n i s m s at different life stages or under different e n v i r o n m e n t a l conditions. A l l e l o c h e m i c a l s m a y be especially i m p o r t a n t for some species and at some stages o f g r o w t h , but have little i m p a c t on others. T h e y might be i m p o r t a n t under wet (anaerobic) environments a n d absent under dry conditions. A l t h o u g h some h i g h l y respected plant ecologists say it is virtually impossible to separate interference mechanisms i n the field, I say instead that we must be m o r e creative i n our a p p r o a c h to that p r o b l e m . Several years ago, C . H . M u l l e r made important progress o n this p r o b l e m . H i s papers c a n teach a l l o f us a lesson. P l a n t ecologists a n d a g r i c u l t u r a l scientists have s e l d o m agreed o n anything. It is i r o n i c that one general area o f agreement involves the notion that w h e n plants do not perform w e l l together it is because o f competition. I contend that this notion is false. In m y view, interference is the o u t c o m e and c o m p e t i t i o n for resources is but one m e c h a n i s m . A l l e l o p a t h y is another
xv Waller; Allelochemicals: Role in Agriculture and Forestry ACS Symposium Series; American Chemical Society: Washington, DC, 1987.
i m p o r t a n t m e c h a n i s m that produces interference. T h i s has been stated before by others, but I feel it needs repeating. M o r e needs to be learned about plant succession and w h y it proceeds as it does i n a n u m b e r o f different environments. C o n s i d e r a b l e evidence exists that a l l e l o c h e m i c a l s m a y have i m p a c t i n this area. We also need a better understanding o f m u t u a l i s m . U n d o u b t e d l y , m a n y mutualistic associations exist o f w h i c h we are not aware. F o r e x a m p l e , might associated microbes produce c h e m i c a l s that help plants defend their space?
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Challenge to Microbiologists S o m e o f the m o r e i m p o r t a n t a l l e l o c h e m i c a l interactions i n v o l v e soil microbes. T h e y m a y be either donors or recipients. M i c r o b i o l o g i s t s should m a k e an effort to identify soil organisms that produce phytotoxins because they m a y damage crops i n the field or prove useful as b i o c o n t r o l agents or sources o f useful chemicals. We s h o u l d also learn w h i c h o r g a n i s m s and a l l e l o c h e m i c a l s adversely affect the m i c r o b i a l symbionts. S o m e have already been shown to suppress g r o w t h o f b a c t e r i a l nitrogen fixers a n d nitrifiers as w e l l as m y c o r r h i z a l fungi. C o m p o u n d s that inhibit n i t r i f i c a t i o n c o u l d prove to be i m p o r t a n t agriculturally. W e e d seed longevity is attributed, at least i n part, to inhibitors that protect the seed f r o m decay by microbes. O n e o f the reasons weeds pose such a serious p r o b l e m is because their seeds can persist for decades. T h i s p r o b l e m m i g h t be a t t a c k e d by either destroying the inhibitors or by developing strains o f microbes that can destroy the seeds. Challenge to Pestologists We s h o u l d determine w h i c h plant pests i n f l i c t their d a m a g e through production o f phytotoxins. It n o w appears that several pathogenic fungi m a y do this. N u m e r o u s w e e d species m a y impose interference on crop g r o w t h , at least i n part t h r o u g h a l l e l o c h e m i c a l s . M o r e than 7 0 species have n o w been alleged to have allelopathic potential. Perhaps the most e x c i t i n g concept is to use the natural p r o d u c t as a pest-regulating or pest-inhibiting c o m p o u n d . T h i s approach might w o r k on vertebrate pests as w e l l as insects, nematodes, plant pathogens, and weeds. O n e o f the most e x c i t i n g new n e m a t o c i d a l and m i t i c i d a l c o m p o u n d s is a v e r m e c t i n , a c o m p l e x natural product p r o d u c e d by a Streptomyces. A n exciting new herbicide w i t h glyphosate-like activity has also recently been discovered i n a Streptomyces culture. I a m confident that the pesticidep r o d u c i n g factory o f the future w i l l be a biosynthetic unit. M a n y o f our useful c o m p o u n d s w i l l be p r o d u c e d by actinomycetes, bacteria, or fungi using plant products as substrates. T h i s i n itself c o u l d produce another xvi Waller; Allelochemicals: Role in Agriculture and Forestry ACS Symposium Series; American Chemical Society: Washington, DC, 1987.
major m a r k e t for a g r i c u l t u r a l products. T h e c o m p o u n d s p r o d u c e d i n this manner might also pose less environmental hazard. A n obvious place for intensive w o r k on allelopathy is i n the w e e d science area. H e r e , plant interference is either our p r o b l e m or o u r opportunity. We should be clever enough to exploit allelopathy as a w e e d suppression strategy. T h i s c o u l d be a c c o m p l i s h e d w i t h crops that release a l l e l o c h e m i c a l s through exudation or by crop residues placed into sequential c r o p p i n g systems. M y research team and others have already developed some p r o m i s i n g leads i n this area.
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Challenge to Natural Product Chemists T h i s aspect has been the r a t e - l i m i t i n g step i n m a n y studies o f allelopathy. A l t h o u g h a l l signs m a y point to allelopathy, p r o o f requires positive i d e n t i f i c a t i o n o f the a l l e l o c h e m i c a l s . N o t m a n y p l a n t scientists c a n a c c o m p l i s h this, and some s i m p l y go l o o k i n g for the same o l d c o m p o u n d s because they can buy standards f r o m the c h e m i c a l supply house. W h a t is needed is a cooperative effort w i t h plant physiologists and chemists w o r k i n g side-by-side on fractionation and bioassay. We need to isolate and identify the m o r e active c o m p o u n d s even i f they are present i n s m a l l quantities. We must be careful not to isolate c h e m i c a l s that prove to be artifacts. O u r i s o l a t i o n techniques s h o u l d begin w i t h steps that m i g h t be expected to operate i n nature. U s u a l l y , water w i l l be the appropriate solvent. We should perform isolation i n the absence and presence of microbes to see if they add new toxins. C h e m i s t s s h o u l d h e l p d e v e l o p better m e t h o d o l o g y for i s o l a t i n g c o m p o u n d s f r o m the environment, p a r t i c u l a r l y the soil environment. We need more breakthroughs a l o n g the line o f the trapping resin developed by Tang and Young. C h e m i s t s should continually develop i m p r o v e d separation and spectral analyses systems. T h e instruments n o w available are extremely powerful but, because o f cost, are available to only a few laboratories. W h e n n o v e l c h e m i c a l s are c h a r a c t e r i z e d , chemists s h o u l d synthesize s i m i l a r structures to search for useful analogs. C h e m i s t s should also consider more plant c o m p o u n d s as potential intermediates or even starting points i n production o f other useful products. T h e r e appears to still be a shortage o f natural product chemists. If m o r e n a t u r a l product chemists were available for postdoctoral positions, their appetites c o u l d be whetted for allelopathic research. Acknowledgments I must thank several colleagues w h o have contributed a great deal to m y success. I w i s h to first thank m y department c h a i r m a n , J a c k K e l l y , w h o has most i m p o r t a n t l y g i v e n me the f r e e d o m to pursue m y research on xvii Waller; Allelochemicals: Role in Agriculture and Forestry ACS Symposium Series; American Chemical Society: Washington, DC, 1987.
allelopathy. I w i s h to especially thank the allelopathy graduate
students
Jane Barnes, Joe D e F r a n k , R o n L o c k e r m a n , Tracy Sterling, A n n e H a r t u n g , and L e s l i e Weston; a n d postdoctorates
R o d Heisey, F r e d L e h l e , a n d Saroj
M i s h r a for a l l their contributions. I p a r t i c u l a r l y appreciate the technical help o f B i l l C h a s e a n d C u r t W h i t e n a c k a n d the fine secretarial assistance o f Jackie
Schartzer.
In a d d i t i o n , I w i s h to thank
Bill
Duke
of Cornell
U n i v e r s i t y a n d the entire W e e d Science Staff at the U n i v e r s i t y o f C a l i f o r n i a ( D a v i s ) for the i n v i g o r a t i o n they s u p p l i e d d u r i n g m y s a b b a t i c a l leaves. F i n a l l y , I must thank Stan R i e s for t e a c h i n g m e some i m p o r t a n t
lessons
about intensity a n d creativity. T h i s i n t r o d u c t i o n w a s o r i g i n a l l y presented
as the 1985 S t e r l i n g B .
H e n d r i c k s M e m o r i a l L e c t u r e d u r i n g the 190th A m e r i c a n C h e m i c a l Society National Meeting in Chicago.
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ALAN R. PUTNAM
Department of Horticulture and Pesticide Research Center Michigan State University East Lansing, M I 48824
xviii
Waller; Allelochemicals: Role in Agriculture and Forestry ACS Symposium Series; American Chemical Society: Washington, DC, 1987.
