The Role of Phytochemistry in Attacking the Leafy Spurge - American

Chapter 21

The Role of Phytochemistry in Attacking the Leafy Spurge (Euphorbia esula) Problem

Downloaded by UNIV OF MICHIGAN ANN ARBOR on February 18, 2015 | http://pubs.acs.org Publication Date: January 8, 1987 | doi: 10.1021/bk-1987-0330.ch021

Gary D. Manners Western Regional Research Center, Agricultural Research Service, U.S. Department of Agriculture, Albany, CA 94710

Individual chemical constituents isolated and char acterized from the noxious weed Euphorbia esula were assessed biologically and/or chemotaxonomically in relation to the allelopathy of E. esula, the allelopathy of Antennaria microphylla to E. esula, and the insect biological control of E. esula. Kaemferol 3-glucuronide and 1-hexacosanol obtained from aqueous extracts of E. esula are considered important allelochemicals in this weed. Biological assays, utilizing E. esula test systems, support hydroquinone and arbutin (obtained from extractives of A. microphylla) as major participants in the allelopathy of A. microphylla to E. esula. The distribution of triterpenes (α,β-amyrinand δ -amyrenone) and unique jatrophane diterpenes charac terized in E. esula leaf and root extracts have strong potential for the chemotaxonomic differenti ation of E. esula varieties relative to insect biological control of this weed. Leafy spurge (Euphorbia esula) is a dicotyledonous, herbaceous, deeprooted, perennial noxious weed infesting more than four million acres of open rangeland in the upper great plains of the United States and the prairies of Canada. This lateciferous plant is toxic to live stock ( 1_), allelopathic to desirable forage plants (2^) and poses a serious threat to livestock production on open rangelands. While leafy spurge can be controlled by herbicides (3) or vigorous cultivation, the cost of control is continuous since current chemical means do not eradicate this weed. More than 20 million dollars a year is spent for the control of this plant, and its agroeconomic impact is greater than 12 million dollars per year in the state of North Dakota alone (4). Recent research efforts on the leafy spurge problem have concentrated on increased herbicide e f f i ciency and the successful application of insect biological control methods. This paper summarizes the results of phytochemical examinations of plant-plant and plant-insect interactions involving leafy spurge This chapter not subject to U.S. copyright. Published 1987 American Chemical Society

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

21.

MANNERS

A ttacking the Leafy Spurge

Problem

229

which could p o t e n t i a l l y provide new or improved methods for i t s control or eradication. These phytochemical investigations have resulted i n the characterization of potential allelochemicals from leafy spurge and of constituents phytotoxic to spurge from Antennaria microphylla, a plant reported a l l e l o p a t h i c to leafy spurge (2_). Chemical examination of leafy spurge leaf and root material has also provided chemotaxonomic information of p a r t i c u l a r relevance i n the selection of subspecies of the weed that are susceptible to insect b i o l o g i c a l control.


Plant-Plant Interactions (Leafy Spurge) Several studies have examined the chemistry of Euphorbia species. A majority of these investigations have focused on the chemical character of the plant latex r e l a t i v e to taxonomy ( 5 ^ ) or mammalian t o x i c i t y (7^8^)· Toxic ingenane diterpenes (phorbols) have also been obtained from the latex of E_» esula (9-11). Other chemical i n v e s t i gations of the a e r i a l portions of leafy spurge have led to the characterization of hydrocarbons (12), long-chain alcohols (13,14), long-chain aldehydes (14), triterpenes (12,15), flavonoids (16), and the description of an unidentified a l k a l o i d (12). None of the chemical studies examined the chemical composition of leafy spurge i n r e l a t i o n to allelopathy. Allelopathy of Leafy Spurge. The lack of forbs and the occurrence of bare ground i n stands of leafy spurge was considered evidence that the weed was a l l e l o p a t h i c (1_). The phytotoxicity of aqueous extracts of leafy spurge plant material and accompanying s o i l toward several test species v e r i f i e d the observed a l l e l o p a t h i c behavior of the plant (2). The extracts were i n h i b i t o r y to the germination and growth of forb test species. Aqueous leaf extracts were more toxic to the test species than the stem extracts while root extracts were the most toxic. S o i l extracts were also toxic but at a lower l e v e l than the plant extracts. These results prompted our empirical phytochemical examination of leafy spurge plant material i n an e f f o r t to define the chemical source of the observed allelopathy (17). A i r - d r i e d a e r i a l plant material was solvent extracted with hexane to remove nonpolar constituents and then extracted with water according to Scheme I. The water extract was l i q u i d / l i q u i d extracted with ethyl acetate. A lettuce seed bioassay of the crude ethyl acetate extract (EA) (dried i n vacuo) showed a 22% reduction of root elongation at 200 ppm. The organic extract was extracted with aqueous sodium bicarbonate to produce a c i d i c and basic fractions which were neutralized and extracted with ethyl acetate to achieve neutralized a c i d i c (NA) and neutralized basic (NB) f r a c t i o n s . Fraction NA (dried ill vacuo) maintained the previous l e v e l of phytot o x i c i t y observed for f r a c t i o n EA i n a lettuce seed bioassay. Preparative chromatographic f r a c t i o n a t i o n of NA yielded kaemferol 3-glucuronide (K-3-G), previously described i n E_. esula (16), and p-coumaric acid (11) as major constituents. Lettuce seed root growth bioassay of K-3-G produced a 49% reduction of root elongation at 500 ppm. In contrast, kaemferol (III) (the aglycone of K-3-G) characterized i n f r a c t i o n NB showed a low l e v e l of stimulatory a c t i v i t y at the same concentration. The coumarin scopoletin (IV) was also i s o l a t e d from f r a c t i o n NB i n low y i e l d . The observed b i o l o g i c a l a c t i v i t y of K-3-G, coupled with i t s r e l a t i v e l y high y i e l d (1.4 X 10"^ moles/kg plant material) and water


230

ALLELOCHEMICALS: ROLE IN AGRICULTURE AND FORESTRY

Scheme I.

The Chemical Separation of Leafy Spurge Plant Material Leafy Spurge (21 kg) IHexane/Soxhlet extn.

Hexane Soluble (837 gm) (1-hexacosanol, triterpenes)

Hexane Extd. Plant Material

IH20 Slurry

H 0-Soluble Downloaded by UNIV OF MICHIGAN ANN ARBOR on February 18, 2015 | http://pubs.acs.org Publication Date: January 8, 1987 | doi: 10.1021/bk-1987-0330.ch021

2

extn.

Residual Plant Material

L i q . / l i q extn. (EtOAc) EtOAC Soluble (EA) (147 gm) Aq.

NaHC0

3

2

NaHC03

Soluble

NaHC03 Insoluble LtOAC

H+/EtOAC EtOAC S o l . (NA)

H 0 Soluble

H 0 Sol. 2

EtOAC S o l . (NB)

(Kaemferol 3glucuronide, pcoumaric acid)

(Kaemferol, scopoletin)

H O ^ ~ ^ C H I I ,R=H VI,R=0H

I,R=g1ucuroni c aci d III,R=H

2

Chromatography

Chromatography

HO,

H 0 Sol.

OH

OR V,R=H VI I , R = g l u c o s e

= CHCOOH

Ο

ôI VIII

s o l u b i l i t y , suggests the compound is an important chemical p a r t i c i pant i n the observed allelopathy of leafy spurge. The very high y i e l d of nonpolar (hexane extract) constituents i n the spurge plant material ( » 5% of t o t a l plant weight) also suggests their potential participation i n the a l l e l o p a t h i c complex of this weed. The hexane extract showed a remarkably high y i e l d (15%, 5 X 10"^ moles/kg plant material) of a single long-chain alcohol (1-hexacosanol). Lettuce seed bioassay of this alcohol produced a 15% reduction i n root length elongation at 500 ppm. The low s o l u b i l i t y of this compound i n the aqueous test system suggests the alcohol may function as a chronic allelochemical i n leafy spurge stands.



21.

MANNERS

Attacking the Leafy Spurge

231

Problem

P h y t o t o x i c i t y to Leafy Spurge. The o b s e r v e d r e d u c t i o n o f l e a f y spurge encroachment i n t o i n c r e a s i n g l y dense s t a n d s o f A n t e n n a r i a m i c r o p h y l l a ( s m a l l e v e r l a s t i n g ) suggested t h a t s m a l l e v e r l a s t i n g was a l l e l o p a t h i c t o l e a f y spurge (I). Laboratory experiments with s m a l l e v e r l a s t i n g p l a n t and s o i l e x t r a c t s c o n c l u s i v e l y showed i n h i b i t i o n o f g e r m i n a t i o n and s e e d l i n g development of l e a f y spurge and t h e s u p p r e s s i o n o f spurge growth i n c o m p e t i t i o n w i t h s m a l l e v e r l a s t i n g ( 2 ) . The experimental observations coupled with the noncompetitive p h y s i c a l c h a r a c t e r o f s m a l l e v e r l a s t i n g (low g r o w i n g , s h a l l o w - r o o t e d ) compared to l e a f y spurge ( d e e p - r o o t e d , v i g o r o u s r o o t b u d d i n g ) s u g g e s t e d the o b s e r v e d dominance o f s m a l l e v e r l a s t i n g t o be the r e s u l t o f an a l l e l o c h e m i c a l e f f e c t r a t h e r than c o m p e t i t i o n . However, c h a r a c t e r i z a t i o n o f s m a l l e v e r l a s t i n g a l l e l o c h e m i c a l s was n o t attempted i n t h e study. Based upon the p o t e n t i a l i m p o r t a n c e o f b i o l o g i c a l l y a c t i v e c h e m i c a l c o n s t i t u e n t s o f s m a l l e v e r l a s t i n g as p o s s i b l e models f o r more e f f i c i e n t agents t o c o n t r o l l e a f y s p u r g e , a c h e m i c a l i n v e s t i g a t i o n o f s m a l l e v e r l a s t i n g was u n d e r t a k e n ( 1 8 ) . S m a l l e v e r l a s t i n g p l a n t m a t e r i a l was c o l l e c t e d , a i r d r i e d , hammermilled and s e q u e n t i a l l y e x t r a c t e d w i t h n - h e x a n e , e t h y l e t h e r , a c e t o n e and m e t h a n o l . L e t t u c e and l e a f y spurge r o o t growth b i o a s s a y s were used t o determine which e x t r a c t p o s s e s s e d s i g n i f i c a n t b i o l o g i c a l a c t i v i t y (Table I ) . These r e s u l t s showed t h a t the e t h e r e x t r a c t ( d r i e d i n v a c u o ) o f s m a l l e v e r l a s t i n g r e d u c e d the growth o f l e t t u c e and l e a f y spurge s e e d l i n g s by 74% and 76% r e s p e c t i v e l y a t 500 ppm. Much lower r e d u c t i o n s o f spurge r o o t growth were o b s e r v e d f o r t h e hexane, a c e t o n e and methanol e x t r a c t s ( d r i e d i n v a c u o ) . On the b a s i s of the b i o a s s a y r e s u l t s , t h e e t h e r e x t r a c t was chosen as the most probable source of a l l e l o c h e m i c a l s i n s m a l l e v e r l a s t i n g . A p o r t i o n o f the d r i e d e t h e r e x t r a c t was f r a c t i o n a t e d on a Sephadex LH-20 c h r o m a t o g r a p h i c column. L e t t u c e r o o t growth b i o - a s s a y showed s i g n i f i c a n t a c t i v i t y (68% and 77% r e d u c t i o n o f r o o t e l o n g a t i o n ) i n two f r a c t i o n s . E a c h o f these f r a c t i o n s was s e m i p r e p a r a t i v e l y chromatographed on a s i l i c a HPLC column. Three p h e n o l i c compounds, hydroquinone [V, 0.002%(w/w) o f d r y p l a n t w t . ] , c a f f e i c a c i d [ V I , 0.012%(w/w)] and a r b u t i n [ V I I , 0.034%(w/w)] were Table

I.

The E f f e c t o f S m a l l E v e r l a s t i n g E x t r a c t s on the Growth o f L e t t u c e Roots and t h e E l o n g a t i o n o f L e a f y Spurge Roots

Lettuce Cone.(ppm) Extract

Hexane Ether Acetone Methanol

L e a f y Spurge Cone.(ppm)

100

300 500 growth, % of c o n t r o l

91 77 92 81

100 41 84 69

97 26 63 66

500 growth, % of c o n t r o l

300

78 36 62 65

Solubility Factor

82 24 58 60

3

0 2 1 3

E m p i r i c a l s o l u b i l i t y of e x t r a c t : 0 = i n s o l u b l e , 1 = mostly i n s o l u b l e , 2 = m o s t l y s o l u b l e , 3 = t o t a l l y s o l u b l e i n aqueous t e s t s y s t e m .

a

Source: Reproduced with permission from reference 18. 1986 Weed Science Society of America.

Copyright



232


i s o l a t e d , c r y s t a l l i z e d and characterized. Pure commercial samples of each of the three phenols and p-benzoquinone (VIII), the oxidation product of hydroquinone (included to evaluate the possible i n vivo oxidation of hydroquinone), were tested i n lettuce and leafy spurge root elongation tests and i n leafy spurge c e l l cultures (Table I I ) . The high l e v e l of t o x i c i t y of both hydroquinone and p-benzoquinone toward leafy spurge was evident i n both the root elongation and c e l l culture bioassays, with root length reductions of 93% and 90% and c e l l culture reductions of 80% and 64% respectively at 300 ppm. The observed phytotoxicity of arbutin to spurge seedlings (51% reduction i n spurge root length at 300 ppm)was i s i n contrast to the observed growth stimulation e f f e c t of arbutin on lettuce root growth. Caffeic acid showed a lower i n h i b i t i o n of spurge root elongation (64% at 300 ppm) with some mild stimulation appearing at low concentrations. The c e l l culture bioassay of c a f f e i c acid supported the root growth bioassay r e s u l t s . Table I I .

The E f f e c t of Chemical Constituents Occurring i n Small Everlasting on the Growth of Lettuce Roots, Root Elongation and C e l l Culture Growth of Leafy Spurge

Lettuce roots

Compound

Hydroquinone Caffeic acid Arbutin p-Benzoquinone

50

19 51 115 11

100

300 500 growth, % of control 12 9 0 48 18 13 114 113 119 9 6 0

Spurge roots

Spurge c e l l s

50

100 300 200 300 500 growth, growth, % of control % of control 36 7 0 79 20 24 110 81 36 106 105 103 81 70 49 87 86 74 34 10 0 87 36 19

Source: Reproduced w i t h p e r m i s s i o n from r e f e r e n c e 1986 Weed S c i e n c e S o c i e t y o f A m e r i c a .

18.

Copyright

Hydroquinone, arbutin and c a f f e i c acid have been reported to occur i n several plant f a m i l i e s , but the appearance of hydroquinone and arbutin i n small everlasting represents only the second reported occurrence of these compounds i n Compositae. The two compounds have been previously reported i n three species of Serratula (Compositae) (19). Hydroquinone and arbutin have been considered as a l l e l o p a t h i c agents i n the aqueous leachates of species of manzanita (Arctostaphylos) (20^,2^) and chaparral (Adenostoma) (22). Because of the low t o x i c i t y of arbutin, i t has been speculated (2(3,22^ that hydroquinone and p-benzoquinone, o r i g i n a t i n g from a large arbutin pool by hydrolysis and oxidation, were the chemical agents responsible for the observed allelopathy of manzanita and chaparral. Tests of hydroquinone on wild oats (Avena fatua) and bromegrass (Bromus r i g i d u s ) (20) showed s i g n i f i c a n t r a d i c a l growth suppression at 50 ppm. The high water s o l u b i l i t y of arbutin provides e f f i c i e n t leacha b i l i t y of the compound from plant tissues and subsequent transport and absorption by other plants. The ultimate chemical form (hydroquinone vs. arbutin) available for absorption would be dependent upon the extent of decomposition ( i e . hydrolysis) a f f e c t i n g arbutin transport .



21.

MANNERS

Attacking

the Leafy Spurge

Problem

233

Glass and Bohm (23) showed arbutin and hydroquinone to be readily and continuously absorbed by the roots of barley plants. This study showed that hydroquinone was glycosated by the barley to form arbutin and was therefore e f f e c t i v e l y detoxified. I f the equilibrium of the d e t o x i f i c a t i o n mechanism of a plant i s sensitive to an oversupply of the toxic and detoxified compound, an oversupply of a detoxified compound could produce equilibrium amounts of the toxic compound. C e l l culture bioassay (Table II) showed that hydroquinone i s not s i g n i f i c a n t l y detoxified i n vivo i n leafy spurge, indicating the s u c c e p t i b i l i t y of the plant to low levels of hydroquinone which could originate from an oversupply of arbutin. The observed t o x i c i t y of p-benzoquinone i n the c e l l cultures and seed bioassays also indicates that oxidation processes a f f e c t i n g hydroquinone w i l l not detoxify the compound rn vivo. This investigation has shown hydroquinone to be a potent phytotoxin toward developing leafy spurge roots. Hydroquinone, originating from a chronic oversupply of arbutin, i s considered to play a s i g n i f i c a n t role i n the observed allelopathy of small everl a s t i n g toward leafy spurge. Plant-Insect Interactions (Leafy Spurge) The high cost of chemically c o n t r o l l i n g leafy spurge and the i n a b i l i t y to eradicate the weed by chemical means has prompted the consideration of b i o l o g i c a l control by an insect predator as a viable alternative. Euphorbia esula has been successfully controlled by natural insect predators i n Europe (24). However, these predators have not been successfully u t i l i z e d i n North America (25). The recognition of several morphologically d i f f e r e n t accessions of leafy spurge i n North America (26,27) suggests either the occurrence of separate North American and European leafy spurge species or subspecies that can not be d i f f e r e n t i a t e d morphologically or i n t r a species physiological and/or chemical differences. Intraspecies chemical and biochemical comparisons of leafy spurge accessions should provide important information for the chemical taxonomic d i f f e r e n t i a t i o n of the accessions and the chemical relationship to insect prédation. Our recent chemical examination of leafy spurge leaf (_28) and root (_29) material provides new information about this weed with primary application to i t s taxonomic d i f f e r e n t i a t i o n as i t relates to b i o l o g i c a l control. Leafy Spurge Wax. Leaves of four North American accessions and one European accession of Euphorbia esula were dipped i n chloroform (30 sec.) to obtain leaf wax samples for a n a l y t i c a l gas chromatography/mass spectrometry (GC/MS) analysis (28). The wax samples were partitioned into acetone soluble and acetone-insoluble f r a c t i o n s . The GC/MS analysis showed the acetone-insoluble portion to contain hydrocarbons, long-chain aldehydes and alcohols, f a t t y acids and fatty acid esters while the acetone soluble portion contained terpenes and terpene esters. The yields of the general chemical classes as determined i n the analysis of the five samples are summarized i n Table I I I . A high y i e l d of long-chain alcohols (primarily 1-hexacosanol) i s found i n a l l the accessions. While the y i e l d s are generally comparable i n the North American samples, a s i g n i f i c a n t l y


234


lower occurrence of alcohols and a higher l e v e l of hydrocarbons appeared i n the European sample. Table I I I . Percent Composition and Y i e l d of E p i c u t i c u l a r Waxes of Five Accessions of Euphorbia esula Accession North American


Component

no. 5

no. 13

Austrian no. 10

no. 17

no. 14

Hydrocarbons Free alcohols Aldehydes Free acids Esters Triterpenes Triterpene esters Unidentified

12 54 1 3 17 3 2 8

18 52 1 2 13 5 2 7

16 53 2 3 7 10 4 5

14 57 1 2 10 7 3 6

25 29 4 4 18 11 2 7

Y i e l d (% dry wt.) Acetone-sol.(%) Acetone-insol.(%)

0.9 5.8 94.2

1.1 7.8 91.2

1.2 13.7 86.3

1.2 10.6 89.4

0.1 11.5 88.5

Table IV.

Percent Composition of Free Triterpenes of Five accessions of Euphorbia esula Accession North American

Terpene

no. 5

3 -Amyrin δ -Amyrenone α -Amyrin 24-Me-Cycloartenol Lupeyl acetate Unidentified

5 11 37 28 4 15

no. 13 4 7 41 31 5 12

no. 14 9 7 67 5 1 11

Austrian

no. 17 4 8 55 19 4 7

no. 10 44

— 22 23 2 9

Five triterpenes were i d e n t i f i e d and quantified i n the acetonesoluble portion of the spurge leaf wax (Table IV). Except for a reduced amount of 24-methylene-cycloartenol i n accession 14, general comparability of triterpene composition can be seen among the four North American spurge accessions. In contrast, the Austrian leafy spurge accession shows a greater amount of $ -amyrin and a much lower amount of α -amyrin and a t o t a l lack of δ -amyrenone. These dramatic differences i n triterpene occurrence support the suggested designation of North American leafy spurge as an intraspecies hybrid of E_. esula and E_. virgata (26) and substantiate the potential importance of chemical analysis for taxonomic d i f f e r e n t i a t i o n within Euphorbiacae.


21.

MANNERS

Attacking

the Leafy Spurge

Problem

235


Leafy Spurge Root Extractives. Prior chemical examinations of leafy spurge have considered only a e r i a l portions of the plant. Our recent chemical examination of root material r e l a t i v e to mammalian t o x i c i t y and/or allelopathy (29) resulted i n the i s o l a t i o n and characteriza tion of two new jatrophane diterpenes (esulone A (IX) and esulone Β (X)) from the ether extract of the roots. B i o l o g i c a l assay of esulone A showed i t to be moderately phytotoxic (29% root length reduction (lettuce seeds) at 250 ppm), moderately toxic (LD50 78 ± 23 mg/kg) and mildly inflammatory (10~5 to 10~^M, dermal) to mammals with no hyperplasia.

IX,R=0H,H X,R=0Ac,H

XI,R=xylose X I I,R=glucose

Jatrophane diterpenes have not been previously described i n E_. esula, although twelve of the compounds have been described i n other species of Euphorbia (31-37) and Jatropha g o s s y p i i f o l i a (38, 3 9 ) . The unique s t r u c t u r a l character of these diterpenes and their exclu sive d i s t r i b u t i o n i n the family Euphorbiacae may allow their use as s p e c i f i c chemotaxonomic markers within the family. Application of a n a l y t i c a l HPLC methods developed i n the i s o l a t i o n of the jatrophane diterpenes to extracts of other E. esula accessions has revealed d i s t i n c t i v e l y d i f f e r e n t u n i d e n t i f i e d jatrophane diterpenes (30) among the accessions. The r a r i t y and e x c l u s i v i t y of these compounds within Euphorbiacae warrants continued chemical examination and d i f f e r e n t i a tion of E^. esula accessions i n relationship to successful insect biological control. A preliminary chromatographic examination of the acetone extrac tives of leafy spurge roots resulted i n the i s o l a t i o n and c h a r a c t e r i zation of S^'-di-O-methylellagic acid 4 - 3 -D-xyloside (XI) ( 3 0 ) . This e l l a g i c acid glycoside has been previously characterized from the bark of the Indian timber tree Anogeissus l a t i f o l i a (40). A second e l l a g i c acid glycoside obtained from the leafy spurge root acetone extract was t e n t a t i v e l y i d e n t i f i e d as 3,3'-di-O-methylellagic acid 4-D-glucoside (XII) of the basis of spectral data and a com parison of physical c h a r a c t e r i s t i c s of this compound with those reported for i t s occurrence i n the heartwood of the Indian tree Terminalia paniculata (41). The s o l u b i l i t y c h a r a c t e r i s t i c s of these compounds prevented their b i o l o g i c a l assessment as phytotoxins. Characterization of these e l l a g i c acid glycosides i s the f i r s t report of e l l a g i c acid derivatives i n Euphorbia esula.


236



Literature Cited 1. Selleck, G.W.; Coupland, R.T.; Frankton, C. Ecol. Monogr. 1962, 32, 1. 2. Selleck, G.W. Weed Sci. 1972, 20, 89. 3. Lym, R.G.; Messersmith, C.G. North Dakota Farm Res. Bull. 1983, 40, 16. 4. Messersmith, C.G.; Lym, R.G. North Dakota Farm Res. Bull. 1983, 40, 8. 5. Evans, F.J.; Kinghorn, A.D. Bot. J. Linn. Soc. London 1977, 74, 23. 6. Adolf. W.; Hecker, E. Israel J. Chem. 1977, 16, 75. 7. Evans, F.J. and Taylor, S.E. In "Progress in the Chemistry of Organic Natural Products"; Herz, W.; Griesbach, H.; Kirby, G. W., Eds.; Springer-Verlag: New York, N.Y., 1983; Vol. 44, p.l. 8. Hecker, E. In "Carcinogenesis"; Slaga, T.J.; Sivak, Α.; Boutvell, E., Eds.; Raven Press: New York, N.Y., 1978; Vol. 2, p. 16. 9. Kupchan, S.M.; Uchida, I.; Branfman, A.R.; Dailey, R.G.; Fei, B.Y. Science 1976, 191, 571. 10. Upadhyay, R.R.; Bakhtavar, F.; Ghaisarzedh, M.; Tilabi, J. Tumori 1978, 64, 99. 11. Seip, E.F.; Hecker, E. Planta Med. 1982, 46, 215. 12. Farnsworth, N.R.; Wagner, H.; Horhammer, L.; Horhammer, H.P.,; Fong, H.H.S. J. Pharm. Sci. 1968, 57, 933. 13. Starratt, A.N. Phytochemistry 1972, 11, 293. 14. Starratt. A.N.; Harris, P. Phytochemistry 1971, 10. 1855. 15. Starratt. A.N. Phytochemistry 1973, 12, 231. 16. Wagner, H.; Donninger, H.; Seligmann, O.; Nogradi, M.; Farkas, L.; Farnsworth, N. Chem. Ber. 1970, 130, 3678. 17. Manners, G.D., unpublished results. 18. Manners, G.D.; Galitz, D.S.; Weed Sci. 1985, in press. 19. Yatsyuk, Y.K.; Lyashenko, S.S.; Batyuk, U.S. Khim. Prir. Soedin. 1968, 4, 54; Chem. Abstr. 1968, 69, 8878n. 20. Hanwalt, R.B. Biochem. Interaction Plants Proc. Conf. Publica tion 1968, (Pub. 1971), 33. 21. Chou, C-H,; Muller, CH. Amer. Midl. Natur. 1972, 88, 324. 22. McPherson, J.K.; Chou, C-H,; Muller, C.H. Phytochemistry 1971, 10, 2925. 23. Glass, A.D.M.; Bohm, B.A. Planta 1971, 100, 93. 24. Schroeder, D. Z. Angew. Entomol. 1980, 90, 237. 25. Dunn, P.H.; Radcliffe-Smith, A. Res. Rep. North Cent. Weed. Conf. 1980, 37, 48. 26. Ebke, D.H.; McCarthy, M. K. Proc. North Cent. Weed Cont. Conf. 1980, 35, 13. 27. Galitz, D.S.; Davis, D.G. North Dakota Farm Res. Bull. 1983, 40, 20. 28. Manners, G.D.; Davis, D.G. Phytochemistry 1984, 23, 1059. 29. Manners, G.D. J. Chem. Soc, Perkin Trans. I 1985, 2075. 30. Manners, G.D., unpublished results. 31. Uemura, D.; Hirata, Y. Tetrahedron Lett. 1975, 1701. 32. Uemura, D.; Katayama, C.; Uno, E.; Sasaki, K.; Hirata, Y. Tetrahedron Lett. 1975, 1703. 33. Uemura, E.; Hirata, Y. Tetrahedron Lett. 1975, 1697. 34. Uemura, Ε.; Nobuhara, K.; Nakayama, Y.; Shizuri, Y.; Hirata, Y. Tetrahedron Lett. 1976, 4593.



21.

MANNERS

Attacking

the Leafy Spurge

Problem

237

35. Shai, R.; Rastogi, R.P.; Jakupovic, J.J.; Bohlmann, F. Phytochemistry 1981, 20, 1665. 36. Yamura, S.; Kosemura, S.; Ohba, S.; Ito, M.; Saito, Y. Tetrahedron 1981, 22, 5315. 37. Seip, E.H.; Hecker, E. Phytochemistry 1984, 23, 1689. 38. Kupchan, S.M.; Sigel, C.W.; Matz, M.J.; Renauld, J.A.S.; Haltiwanger, R.C.; Bryan, R.F.J. J. Am. Chem. Soc. 1970, 92, 4476. 39. Taylor, M.D.; Smith, A.B. III; Frust, G.T.; Gunasekara, S.P.; Bevelle, C.A.; Cordell, G.A.; Farnsworth, N.R.; Kupchan, S.M.; Uchida, H.; Branfman, A.R.; Dailey, R.G., Jr.; Sneden, A.T. J. Am. Chem. Soc. 1983, 105. 3177. 40. Deshpande, V.H.; Patil, A.D.; Rama Rao, A.V.; Venkataraman, K. Indian J. Chem. 1976, 14B, 641. 41. Ramachandra Row, L.; Subba, G.S.R. Tetrahedron 1962, 18, 357. RECEIVED January 10, 1986


The Role of Phytochemistry in Attacking the Leafy Spurge - American

Recommend Documents