Plant-Plant Recognition: Chemistry-Mediating Host Identification in the

C h a p t e r 49

Plant-Plant Recognition: Chemistry-Mediating Host Identification in the Scrophulariaceae Root Parasites Mayland Chang and David G. Lynn

Downloaded by PEPPERDINE UNIV on September 28, 2017 | http://pubs.acs.org Publication Date: January 8, 1987 | doi: 10.1021/bk-1987-0330.ch049

Department of Chemistry, University of Chicago, Chicago, IL 60637

As little as a year ago we r e v i e w e d our understanding of the chemistry mediating host recognition in the p a r a s i t i c angiosperms (8). Although a number of haustoria-inducing factors had been found, i t was clear that the underlying mechanism for this plant-plant interaction was not understood. This paper reviews the identification of 2,6-dimethoxy-p-benzoquinone (2,6-DMBQ) in Sorghum roots as a haustoria-inducing principle for Striga asiatica (Scrophulariaceae). The unique timing events required for Striga parasitism suggest that haustorial induction is mediated through degradation of host root surface components by the parasite's enzymes. Quinones, such as 2,6-DMBQ, would be released and used as recognition signals. This kind of biological recognition may be common to many of the Scrophulariaceae and, in fact, could be a general mechanism for plant-plant interaction.

There are usually a few plants that tend to predominate in a given habitat. While a number of factors contribute to the ecological success of these plants, including their differing ability to use natural resources such as water, light, and nutrients, another more aggressive, chemically based mechanism was proposed in 1832 by DeCandolle (j_). He suggested that plant-produced chemicals may adversely affect neighboring plants. More than a century later, Molisch (2) coined the term allelopathy to include the release of biochemical toxins into the environment by microorganisms and higher plants. A variety of allelochemicals, ranging from simple gases to complex aromatic compounds, have now been identified. Clearly such compounds are playing a significant role in the interaction between plants, and this symposium highlights the potential of allelochemicals in agriculture. 0097-6156/87/0330-0551 $06.00/0 © 1987 American Chemical Society

Waller; Allelochemicals: Role in Agriculture and Forestry ACS Symposium Series; American Chemical Society: Washington, DC, 1987.

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ALLELOCHEMICALS: ROLE IN AGRICULTURE AND FORESTRY

An e x a m p l e o f a s p e c i f i c p l a n t - p l a n t i n t e r a c t i o n i s seen i n p a r a s i t i c angiosperms. These p l a n t s have e v o l v e d t h e c a p a b i l i t y o f e x p r o p r i a t i n g the r e s o u r c e s of o t h e r p l a n t s f o r t h e i r own b e n e f i t . Many p a r a s i t e s e x h i b i t narrow h o s t r a n g e s . As a p r e r e q u i s i t e f o r t h e i r s u c c e s s t h e s e p a r a s i t e s must h a v e d e v e l o p e d methods t o d i s t i n g u i s h between h o s t and non-host p l a n t s . In 1977, A l s a t t e t a l . (3,4) p r o p o s e d t h a t p a r a s i t i c p l a n t s , l i k e herb i v o r o u s i n s e c t s , may use h o s t d e f e n s e c h e m i c a l s as r e c o g n i t i o n cues. T h e r e f o r e , a s t u d y o f t h i s system may not o n l y p r o v i d e some i n s i g h t i n t o the mechanism o f how one p l a n t i s a b l e t o i d e n t i f y n e i g h b o r i n g p l a n t s , but a l s o uncover some a s p e c t s o f the d e v e l o p ment and s p e c i f i c i t y o f the h o s t ' s a l l e l o c h e m i s t r y .


The

Parasitic_Angiospe£ms

P a r a s i t i c angiosperms a r e r e p r e s e n t e d throughout t e n f a m i l i e s , and b e c a u s e o f t h e i r agronomic importance much has been w r i t t e n about them (5-8). They can e i t h e r be f a c u l t a t i v e o r o b l i g a t e and i n many ways a r e t y p i f i e d by the h e m i p a r a s i t e A g a l i n i s purpurea and the h o l o p a r a s i t e S t r i g a a s i a t i c a (both S c r o p h u l a r i a c e a e ) . While A g a l i n i s p u r p u r e a i s c a p a b l e o f p a r a s i t i z i n g a wide v a r i e t y o f h o s t s , S t r i g a a s i a t i c a has a h o s t r a n g e t h a t i s r e s t r i c t e d t o g r a s s e s , s u c h as c o r n , s o r g h u m , m i l l e t , s u g a r c a n e , and r i c e . Because o f t h i s p a r a s i t i s m o f g r a i n c r o p s , S t r i g a i n f e s t a t i o n s a r e v e r y d e v a s t a t i n g and a f f e c t the f o o d s u p p l y o f m i l l i o n s o f people i n A f r i c a and A s i a . S t r i g a has a t l e a s t two l e v e l s o f h o s t r e c o g n i t i o n , one a s s o c i a t e d w i t h g e r m i n a t i o n , and a n o t h e r a t t h e l e v e l o f t h e d e v e l o p m e n t o f t h e h a u s t o r i u m , a s p e c i a l i z e d a t t a c h m e n t organ common t o a l l r o o t p a r a s i t e s . Our l a b o r a t o r y has shown t h a t t h e s e p r o c e s s e s a r e m e d i a t e d by s e p a r a t e and s p e c i f i c c h e m i c a l cues p r e s e n t i n the h o s t (_8). G e r m i n a t i o n , the f i r s t commitment t o a h o s t , h a s b e e n f o u n d t o be i n d u c e d i n S t r i ga by s t r i g o l , a s e s q u i t e r p e n o i d exuded by c o t t o n r o o t s (9). However, c o t t o n d o e s n o t s e r v e as a h o s t f o r S t r i g a , a n d , i n f a c t , can be used as a c a t c h c r o p t o r e d u c e S t r i ga i n f e s t a t i o n . The germination s t i m u l a n t from a n a t u r a l host has y e t t o be i d e n t i f i e d . H a u s t o r i a l development i n S t r i g a i s v e r y t i g h t l y r e g u l a t e d . R i o p e l and B a i r d (J_0) have shown t h a t , r e g a r d l e s s o f temperature, induction of the h a u s t o r i u m i s not p o s s i b l e 5 to 7 days p o s t germination. T h i s i m p l i e s t h a t g e r m i n a t i o n must take p l a c e at a d i s t a n c e where the growing r a d i c l e can r e a c h t h e h o s t ' s s u r f a c e i n a p e r i o d o f 5 d a y s , r o u g h l y 5 mm. In a d d i t i o n , S t r i g a d e v e l o p s o n l y a t e r m i n a l h a u s t o r i u m ( F i g u r e 1), and o n c e f o r m e d , r a d i c l e elongation ceases. F o r s u c c e s s f u l h o s t attachment, h a u s t o r i a l i n d u c t i o n must o c c u r w i t h i n c a . 50 ym o f t h e h o s t s u r f a c e . T h e r e f o r e , t h e c h e m i s t r y m e d i a t i n g t h e s e p r o c e s s e s must not o n l y e x p l a i n how S t r i g a r e c o g n i z e s a h o s t , b u t a l s o a c c o u n t f o r t h e mechanism o f d i s t a n c e r e g u l a t i o n . H a u s t o r i a - i n d u c i n g F a c t o r s from

Gum

Tragacanth

A x e n i c c u l t u r e s o f A g a l i n i s grown i n the absence o f a h o s t d e v e l o p few or no h a u s t o r i a (4,11). I n d u c t i o n o f t h i s organ i s r a p i d upon



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exposure of A g a l i n i s purpurea to host roots ( 1 J _ ) . F u l l y formed haustoria can be observed w i t h i n 12 hr, and t h i s response can e a s i l y be quantitated. By use of haustorial induction i n A g a l i n i s as a bioassay, the f i r s t haustorial inducers, xenognosin A (1) and Β ( 2 ) , were i s o l a t e d and c h a r a c t e r i z e d from gum tragacanth (j_2,J_3), a commercially a v a i l a b l e p l a n t exudate. An e f f i c i e n t t o t a l s y n t h e s i s of x e n o g n o s i n A, which allowed s u f f i c i e n t f l e x i b i l i t y for the study of s t r u c t u r e - a c t i v i t y r e l a t i o n s h i p s , p o i n t e d toward a s t r i c t s t r u c t u r a l s p e c i f i c i t y (J_4) . These studies established the meta-methoxyphenol moiety and the propene double bond as c r i t i c a l f o r b i o l o g i c a l a c t i v i t y (j_3). A simple change i n the regiochemistry of the methoxy s u b s t i t u e n t , as i n compound 3, d r a s t i c a l l y reduced the a c t i v i t y , and removal of either the methoxy or the hydroxy groups rendered the compound t o t a l l y inactive. T h i s s p e c i f i c i t y seemed q u i t e remarkable s i n c e A g a l i n i s p a r a s i t i z e s a broad spectrum of hosts. Nevertheless, flavanoids and phenolics have f r e q u e n t l y been c i t e d as p l a y i n g a r o l e i n a l l e l o p a t h y (JJ5). Xenognosin A has also been found in Pi sum as a stress metabolite (J_6,j_7), and xenognosin Β has been shown to be a b i o s y n t h e t i c precursor of the phytoalexin medicarpin (J_8). These f i n d i n g s suggested that the xenognosins are c o n s t i t u t i v e an t i b i o t i c s necessary for host defenses ( 8 ) and supported A t s a t t s o r i g i n a l proposal that such compounds could serve as r e c o g n i t i o n cues f o r a suitable host. The i d e n t i f i c a t i o n of the xenognosins, hence, constituted the f i r s t experimental support that p a r a s i t i c angiosperms mediate host s e l e c t i o n through the i d e n t i f i c a t i o n of s p e c i f i c molecules present i n , and p o t e n t i a l l y exuded by, t h e i r hosts. T

Haustorial Inducer i n a Natural Host Attempts to document and quantitate exuded materials from A g a l i n i s host plants gave r e s u l t s that were not r e a d i l y e x p l a i n e d by the simple exudation of s p e c i f i c a l l e l o p a t h i c agents ( 8 , ] _ 9 , 2 0 ) . Since Striga requires a more c r i t i c a l commitment to host p l a n t s and a more s p e c i f i c host s e l e c t i o n , i t was reasoned that a study of t h i s o b l i g a t e p a r a s i t e may h e l p d e f i n e the mechanism f o r h o s t recognition. If recognition i s mediated by exuded materials, they must be present i n s u f f i c i e n t concentrations i n the s o i l only near the s u r f a c e of the host root, but may exist in higher concentra tions within the root. Therefore, the roots of Sorghum, a grass e a s i l y grown i n the laboratory and r e a d i l y parasitized by Striga, were extracted and f r a c t i o n a t e d as d i r e c t e d by a bioassay f o r h a u s t o r i a - i n d u c i n g a c t i v i t y (2Λ). This procedure allowed for the p u r i f i c a t i o n of 100 yg of a s i n g l e c r y s t a l l i n e yellow compound from 600 g of Sorghum roots ( 2 2 ) . Electron impact mass spectroscopy ( 7 0 eV, 2 0 0 ° C ) of t h i s compound gave a molecular i o n at m/ζ 1 6 8 . 0 3 8 9 , and a chemical composition of C H 0 „ ( c a l c . 1 6 8 . 0 4 2 2 ) . The UV s p e c t r u m 0

M

0

c. ^ c.

cm

o

8

4

- 1 - 1

2 8 4 (ε = 1 0 , 2 3 3 M cm ) and 3 7 6 nm (ε = 4 4 7 max )] of the natural product was c h a r a c t e r i s t i c of a quinonoid

[(CH C1 ): ^

o

8

X

m o v


554



nucleus.

This data, together with the

H NMR [(CDCl^): δ 3.75 (s,

6H); 5.83 ( s , 2 H ) ] s u p p o r t e d a d i m e t h o x y - s u b s t i t u t e d pbenzoquinone structure. Three isomeric benzoquinones, d i f f e r i n g only i n the p o s i t i o n of the methoxy substituents, s a t i s f i e d the data (4, 5 or 6 ) . NMR spectroscopy, instrumental i n the c h a r a c t e r i z a t i o n of the xenog n o s i n s , was of l e s s u t i l i t y f o r the s t r u c t u r a l e l u c i d a t i o n of these highly symmetrical quinones. Mass s p e c t r o m e t r i c a n a l y s i s , however, gave fragment ions at m/z 112 and 80, indicating a r e t r o Diels-Alder cleavage of the benzoquinone r i n g of either quinone 4 or 5 . The benzoquinone 6 would be expected to give fragment ions at m/ζ 142 and 82. Moreover, i t s q u i n o n o i d protons should resonate f u r t h e r downfield (δ 6.58). These data ruled out 2 , 3 dimethoxy-p-benzoquinone as the haustorial inducer. The e l e c t r o n i c and v i b r a t i o n a l spectra of benzoquinones are very diagnostic. Of the two possible isomers remaining, the 2,5s u b s t i t u t e d quinone ( 5 ) would be expected to give two d i f f e r e n t e l e c t r o n i c t r a n s i t i o n s of equal i n t e n s i t y around 280 nm, and only one carbonyl s t r e t c h i n g band. The F o u r i e r transform infrared spectrum (Ch^C^) of the haustorial inducer showed strong absorp t i o n s at 1698 (vC=0), 1646 (vC=0) and 1597 cm" (vC-C). These spectroscopic data e s t a b l i s h e d the h a u s t o r i a l inducer as 2,6dimethoxy-p-benzoquinone (2,6-DMBQ, 4 ) . 1

A l l three isomeric dimethoxyquinones were synthesized (2224), and these synthetic compounds confirmed the assignment of 2,6-DMBQ as the haustorial inducer. In order t o probe the s t r u c t u r a l s p e c i f i c i t y of the quinone, several s y n t h e t i c analogues were prepared (_22) and t e s t e d f o r haustoria-inducing a c t i v i t y . These r e s u l t s are presented in Table I. The monomethoxy (9) and ethoxymethoxy quinones ( 8 ) were only one-tenth as a c t i v e as 4 . More d r a s t i c s t r u c t u r a l a l t e r a t i o n s completely abolished a c t i v i t y . The u n s u b s t i t u t e d benzoquinone (10), as w e l l as the dimethyl ( 1 1 ) and the dihydroxy ( 1 2 ) derivatives, which l a c k a methoxy f u n c t i o n a l i t y , were t o t a l l y inactive. As i n the xenognosins, the presence of at l e a s t one methoxy f u n c t i o n a l i t y appears to be of c r i t i c a l importance. A l l three isomeric dimethoxyquinones f u l f i l l t h i s requirement, but only 2 , 3 DMBQ ( 6 ) and 2,6-DMBQ (4) induce haustoria. Both compounds have been shown to i n h i b i t mitochondrial e l e c t r o n t r a n s p o r t (25,26). In c o n t r a s t , the 2,5-isomer ( 5 ) shows no such i n h i b i t i o n o f r e s p i r a t i o n and does not induce haustoria. A possible connection between the i n h i b i t i o n of e l e c t r o n transport and the haustoriainducing a c t i v i t y of these quinones has yet to be c l a r i f i e d . Discussion To date, several naturally occurring compounds which are capable o f i n d u c i n g t h e development o f t h e h a u s t o r i u m have been characterized. The f i r s t haustorial inducers i d e n t i f i e d were the xenognosins, and t h e i r connection with the host's constitutive a n t i b i o t i c s suggested that they were s p e c i f i c r e c o g n i t i o n cues (8). 2,6-Dimethoxy-p-benzoquinone, the only a c t i v e p r i n c i p l e



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Figure 1. Electron Micrograph of the Developing Haustorium Striga a s i a t i c a . (Courtesy of Dr. Vance Baird).


of


556


Table I.

R

B i o l o g i c a l A c t i v i t y of Benzoquinone Analogues

2

R

3

R

R

5

4

0CH

3

H

H

5

0CH

3

H

0CH

6

0CH

3

0CH

7

0CH

3

8

0CH

9

0CH

6

0CH

0.32

3

H

H

1 .80

H

H

0CH C0 H

0.47

3

H

H

0CH CH

2.00

3

H

H

H

5.00 inactive

3

3

2

2

H

H

H

H

CH

3

H

H

CH

OH

H

OH

H

Q

(μΜ)

inactive

11

The ED^

5Q

H

3

10

12

ED

3

inactive

3

represents the concentration necessary

inactive

to induce

t o r i a l development i n 50% of the Striga seedlings.


haus


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found i n Sorghum, has a wide spectrum of b i o l o g i c a l a c t i v i t y ( 2 7 31 ) , i n c l u d i n g a l l e l o p a t h y ( 3 2 , 3 3 ) . Therefore the quinone, l i k e the xenognosins, could be t i e d i n with host defenses. Xenognosin A c o n t a i n s the b i o l o g i c a l l y c r i t i c a l meta-methoxy phenol and the quinone possesses the same moiety at a higher o x i d a t i o n s t a t e . S t r u c t u r a l modifications a l t e r i n g t h i s r e l a t i o n s h i p eliminate the a b i l i t y of both compounds to induce haustorial development. While t h i s s i m i l a r i t y i s s t r i k i n g , 2,6-DMBQ, unlike the xenognosins, i s widely d i s t r i b u t e d among the plant kingdom and has been found i n r o o t s , bark, a e r i a l p o r t i o n s , and f r u i t s of higher plants ( 3 4 ) . Various substituted quinones are biosynthesized i n many plants v i a the shikimate pathway and formed through a c r i t i c a l oxidative decarboxylation of benzoic acids, such as s y r i n g i c acid ( 3 5 , 3 6 ) . R e c o g n i z i n g t h i s common decarboxylation step i n the biosynt h e s i s of q u i n o n e s sheds new l i g h t on M a c Q u e e n ' s (37) demonstration that s e v e r a l phenolic acids are inducers of haust o r i a l development i n S t r i ga h e r m o n t h i ca ( T a b l e I I ) . The p h e n o l i c s are as potent as the quinones (Table I ) , and i n both c l a s s e s of compounds a methoxy s u b s t i t u e n t i s i m p o r t a n t f o r biological activity. These findings suggested that the a c t i v i t y of the acids could be the r e s u l t of their metabolic breakdown to the quinones ( 2 2 ) . This connection between the benzoic acids and the quinones provided the f i r s t evidence for a unifying mechanism of h a u s t o r i a l i n d u c t i o n . However, a l l attempts to i d e n t i f y the acids, quinones, or any h a u s t o r i a - i n d u c i n g a c t i v i t y i n Sorghum exudate were unsuccessful. Studies of pathogenic fungi suggested an explanation f o r the absence of inducer molecules i n host root exudate. Quinones such as 2,6-DMBQ have been shown to be released by white r o t f u n g i as terminal oxidation products of l i g n i n model compounds ( ^ 8 ) . These findings substantiated previous r e p o r t s ( 3 9 - 4 1 ) that l a c c a s e s , phenol oxidases using 0^ as the oxidant, are d i r e c t l y involved i n l i g n i n degradation (_42,43) . In f a c t , the presence of such enzymatic a c t i v i t y has been correlated with virulence i n white rot fungi. A s p e c i f i c chromogenic compound, s y r i n g a l d a z i n e , has been developed to test for the presence of these enzymes (_44^) . The compound, which i s yellow i n i t s reduced form, i s oxidized to a r e d - p u r p l e q u i n o n e m e t h i d e i n the p r e s e n c e of l a c c a s e or peroxidase. I t has been used as a f a s t and simple s c r e e n i n g procedure for these enzymes in pathogenic fungi (44_). The use of s y r i n g a l d a z i n e to s t a i n the r o o t s of l e t t u c e , pea, and Sorghum seedlings shows enzymatic a c t i v i t y l o c a l i z e d in the root hair zone of these plants ( 2 2 ) . Both A g a l i n i s and S t r i g a , which have poorly developed or no root h a i r s , thus show the presence of phenol oxidase along the surface of the root and on the meristematic t i p , a region not stained in the other plants. While t h i s h i s t o c h e m i c a l assay does not prove that these enzymes have the required s p e c i f i c i t y , i t does provide evidence f o r the presence and d i f f e r e n t i a l l o c a l i z a t i o n of the necessary oxidative enzymes. Fungal laccases r e a d i l y oxidize ortho- and p a r a - s u b s t i t u t e d phenols ( 4 5 - 4 8 ) , such as s y r i n g i c ( 1 5 ) and sinapic ( 1 3 ) acids, to the corresponding quinones. Experiments with T r i t i c u m vulgare


558



Table I I .

B i o l o g i c a l A c t i v i t y of Phenolic Compounds ED

ED50

5 0

COOH

COOH

5.2xlO" M* I.O/jg/mL 6

OCH7

2.5 pig/mL

5.lxlO" M* 0.1 pg/mL 7

OCH*

inactive

H CO^Nj^OCH 3

inactive

OH

inactive

3

OCH3

The Εϋ_ represents the concentration necessary to induce 50% of Λ

the Striga seedlings to form haustoria.

*MacQueen, M. ( 3 7 ) .



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(wheat) i n d i c a t e that 2-methoxy- and 2,6-dimethoxy-p-benzoquinone arise from o x i d a t i v e d e c a r b o x y l a t i o n of v a n i l l i n and s y r i n g i c a c i d , r e s p e c t i v e l y (_44). Thus, i t i s conceivable that p a r a s i t i c enzymes could o x i d i z e xenognosin A ( 1 ) to a methoxy quinone. S t r u c t u r a l m o d i f i c a t i o n s such as reduction of the propene double bond (e.g., dehydro-xenognosin A), a change i n the methoxy p o s i t i o n (e.g., 3 ) , or removal of the hydroxy group would d r a s t i c a l l y reduce the b i o l o g i c a l a c t i v i t y (8). While the presence of oxidative enzymes on the parasite and the s t r u c t u r a l correlations seen with the a c t i v e h a u s t o r i a l i n d u c e r s do not provide unequivocal evidence i n f a v o r of host recognition mediated through d e g r a d a t i o n of host s u r f a c e components by p a r a s i t i c enzymes, they present a strong argument for such a mechanism. P r e l i m i n a r y experiments suggest t h a t h i g h molecular weight carbohydrates can be removed from Sorghum root surface, which on incubation with Striga s e e d l i n g s generate 2,6DMBQ. A more thorough characterization of the surface components from the roots of Sorghum and of the p a r a s i t i c enzymes responsible f o r the r e l e a s e of 2,6-DMBQ need to be completed before t h i s mechanism of host r e c o g n i t i o n can be f u r t h e r s u b s t a n t i a t e d . However, t h i s process would unify the mechanism through which both S t r i g a and A g a l i n i s c o n t r o l t h e i n i t i a t i o n o f h a u s t o r i a l development. Haustorial formation represents a meristematic d i f f e r e n t i a t i o n i n S t r i g a and r a d i c l e e l o n g a t i o n terminates with the induction of haustorial development. These o b s e r v a t i o n s imply that the distance between the parasite's meristematic root t i p and the host root surface i s c r i t i c a l . Premature haustorial induction would r e n d e r t h e p a r a s i t e u n a b l e t o reach i t s h o s t . With A g a l i n i s , early haustorial induction i s not f a t a l , but s u c c e s s f u l a t t a c h m e n t t o a h o s t p r o v i d e s a s e l e c t i v e advantage. This mechanism of b i o l o g i c a l recognition may be common to many of the p a r a s i t i c Scrophulariaceae. In f a c t , surface recognition between two eukaryotic organisms i s a fundamental feature of a l l e l o p a t h y . An a c t i v e s c r e e n i n g of the environment by s p e c i f i c plant enzymes could provide more s p e c i f i c i n f o r m a t i o n about c o m p e t i t o r s , and even information about the l o c a t i o n of those plants. The proof of such a mechanism would go one step f u r t h e r t o d i s p e l the b e l i e f t h a t p l a n t s are p a s s i v e organisms, only able to u t i l i z e the resources of their surrounding environment, and h i g h l i g h t s one of the plant kingdom's elaborate and sophisticated uses of chemistry. Ac knowledgments We a r e i n d e b t e d t o t h e Research C o r p o r a t i o n and the F r a s c h Foundation for support, the USDA (5901-0410-9-0257 and 58-7B30-3597) f o r j o i n t l y supporting t h i s laboratory and that of Professor James Riopel at the University of V i r g i n i a , and The U n i v e r s i t y of Chicago Cancer Center for instrumentation support. DGL gratefuly acknowledges support from the Alfred P. Sloan Foundation and the C a m i l l e and Henry Dreyfus Foundation, Inc. and MC i s grateful for support from the Aileen S. Andrew Foundation.


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Literature Cited 1. DeCandolle, M. A. P. " Physiology Vegetal, Vol I I I " ; Bechet Jeune, Lib. Fac. Med.: Paris, 1832. 2. Molisch, H. "Der E i n f l u s s einer Pflanze auf d i e a n d e r e — Allelopathie"; Fischer: Jena, 1937. 3. Alsatt, P. R.; Hearn, T. E.; Nelson, R. C.; Heineman, R. T. Ann. Bot. 1978, 42, 1177-1184. 4. Alsatt, P. R. Am. Nat. 1977, 3 , 579-586. 5. K u i j t , J . "The Biology of P a r a s i t i c Flowering Plants"; University of California Press: Berkeley, 1969. 6. Musselman, L. J . Ann. Rev. Phytopath. 1980, 18, 463-489. 7. Riopel, J . L. In "Vegetative Compatibility"; Moore, R., Ed.; Academic Press: New York, 1983; pp. 13-34. 8. Lynn, D. G. In "The Chemistry of Allelopathy: Biochemical I n t e r a c t i o n s among P l a n t s " ; Thompson, A. C., Ed; ACS SYMPOSIUM SERIES No. 268, American Chemical S o c i e t y : Washington, D.C., 1985; pp. 55-81. 9. Cook, C. Ε.; Whichard, L. P.; Wall, M. E.; Egley, G. H.; Coggan, P.; Luhan, P.Α.; McPhail, A. T. J . Am. Chem. Soc. 1972, 94, 6198-6199. 10. R i o p e l , J . L.; Baird, V. W. In "The Biology and Control of Striga"; Musselman, L. J . , Ed.; CRC Press: Orlando, i n press. 11. R i o p e l , J . L.; Musselman, L. J . Am. J . Bot. 1979, 66, 570575. 12. Lynn, D. G.; S t e f f e n s , J .C.;Kamat, V. S.; Graden, D. W.; Shabanowitz, J.; Riopel, J . L. J . Am. Chem. Soc. 1981, 103, 1868-1870. 13. Steffens, J . S.; Lynn, D. G.; Kamat, V. S; R i o p e l , J . L. Ann. Bot. 1982, 50, 1-7. 14. Kamat, V. S.; Graden, D. W.; Lynn, D. G.; S t e f f e n s , J . C.; Riopel, J . L. Tetrahedron Lett. 1982, 23, 1035-1038. 15. B e l l , A. A. Ann. Rev. Plant Physiol. 1981, 32, 21-81. 16. Carlson, R. E.; Dolphin, D. H. Phytochemistry 1982, 21, 1733-1736. 17. Carlson, R. Ε.; Dolphin, D. H. Phytochemistry 1981, 20, 2281-2284. 18. Dewick, P. M. J . Chem. Soc. Chem. Commun. 1975, 656-658. 19. Steffens, J .C.;Roark, J . L.; Lynn, D. G.; Riopel, J . L. J . Am. Chem. Soc. 1983, 105, 1669-1671. 20. Steffens, J .C.;Lynn, D. G.; Riopel, J . L. submitted. 21. Nickrent, D. C.; Musselman, L. J.; Riopel, J . L.; Eplee, R. E. Ann. Bot. 1979, 43, 233-236. 22. Chang, M.; Lynn, D. G. J. Chem. Ecol. 1986, i n press. 2 3 . Bolker, H. I.; Kung, F. L. J . Chem. Soc. (C). 1969, 22982304. 24. Matsumoto, M.; Kobayashi, H. J. Org. Chem. 1985, 50, 17661768. 25. Chappel, J . B.; Hansford, R. G. In "Subcellular Components, Preparation and F r a c t i o n a t i o n " ; Birnie, G. D.; Fox, S. Μ., Eds.; Butterworths: London, 1972, 2nd ed.; pp. 43-56. 26. Redfearn, E. R.; Whittaker, P. A. Biochim. Biophys. Acta 1962, 56, 440-444.


49.

CHANG ANDLYNN

27. 28. 29. 30. 31.


32. 33. 34. 35. 36. 37. 38. 39. 40. 41. 42. 43. 44. 45. 46. 47. 48.

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RECEIVED January 3,1986


Plant-Plant Recognition: Chemistry-Mediating Host Identification in the

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