7/23/2019 1988 (Leroux, Berthier) Resistance to Carboxin and Fenfuram

1/4

Resistance to

nude Jens.)

carboxin and fenfuram in Ustilago

Rostr., the causal agent of barley

loose smut

P.

EROUX AND G. BERTHIER*

I NRA, St at i on de Phy t opharm acie, Etoi l e de Choi sy, 78000 Versai l l es, France and

* NRA , SRIK La Verri -e, 78320 Le M esnil -Saint- Den France

ABSTRACT.

Two types

of strains of

U ago

nudu,

resistant to carboxin and fenfuram, were detected

on winter barley crops in 1986. The most frequent strains are similar to those found previously and

they are characterized by their great susceptibility to mepronil and flutolanil. This negative correlation

between two groups of carboxamide fungicides is not found when the other type of carboxin-resistant

isolates is considered. From these observations, we elaborate a simple teliospore-germination test which

can be used for routine survey of resistance. In field trials, when the resistant strains are prevalent (in

the absence of treatment), the efficacy of seed dressings with carboxin or fenmram against barley loose

smut is low. In such situations, which are common with the winter barley varieties Panda or Viva,

inhibitors of sterol biosynthesis such as flutriafol or triadimenol remain very active in practice.

KEYWORDS: Fungicide resistance; carboxamides; carboxin; fenfuram; barley; Ustilugo nudu

Introduction

The discovery, 20 years ago, of carboxin provided the

possibility of an efficient chemical control of barley

loose smut caused by

Ustilago nuda

(Richard and

Cognet, 1967; Ventura, Bourdin and Piedallu, 1968).

Since that time, this fungicide and several related

carboxamides (e.g. fenfuram, methfuroxam, pyra-

carbolid) have been intensively used as seed dressings,

in France and many other countries.

During the last three seasons, several cases of

reduced efficacy of these carboxamides have been

reported on winter barley crops in France. In some

situations it has been shown that heavy rainfall just

after sowing, or low dosage of chemicals applied to

seeds, were the causes of these failures. As resistance in

practice towards oxycarboxin (an analogue of

carboxin) has been found in

Puccinia horiana

(Grouet,

Montfort and Leroux, 1981), this possibility has also

been considered with the barley loose smut. The

monitoring which was conducted in France during the

spring of 1985 has indicated the presence of U

nuda

isolates, resistant to carboxamides, on several varieties

of barley (Leroux, 1986). This enabled us to collect

barley seeds contaminated with sensitive or resistant

strains. These samples were used for field experiments

during the season 1985-1986, to test the field

resistance of barley loose smut to carboxamides. This

paper presents the results of these trials (efficacy of

seed dressings and characteristics of U.

nuda

strains).

0261-2194/88/01/0016-04 03.00

0 1988 Butterworth & Co (Publishers) Ltd

CROP PROTECTION Vol. 7, February 1988, 16-19

Materials and methods

Varieties of w int er barl ey

The various samples of seeds were harvested during

summer 1985 in plots where smutted heads were

present. The resistance of teliospores from some of

these heads has been investigated (Leroux, 1986).

The three samples of cv. Viva, collected near Lyon,

Niort and Orleans, respectively, as well as the sample

of cv. Panda, were obtained from fields where

resistance to carboxin was widespread. In contrast, the

sample of cv. Thibaut came from a field where only

sensitive strains of U.

nuda

were detected. With regard

to cv. Gerbel, the sample was collected in a plot in

which resistant and sensitive isolates were present

simultaneously.

Seed dressi ngs

The seeds were treated by agitation with fungicide

powders for 15 min using a rotary shaker. For

carboxin, fenfuram and triadimenol formulations, the

rates were 1OOg a.i./quintal seed (q)f 80g a.i./q and

30 g a.i./q respectively; these are rates recommended in

France (Bourdin, 1983). Mepronil and flutriafol were

tested at 1OOg a.i./q and 5 g a.i./q respectively.

t

1 quintal=05g 100kg).

7/23/2019 1988 (Leroux, Berthier) Resistance to Carboxin and Fenfuram

2/4

P. LEROUXAND G . BERTHIER 17

TABLE 1. Effect of various chemicals on the germination ofteli ospores and the length ofpromyceli a of different strains of Ustilago nuda (each value is t h e

average obtained on at l e a s t t h r e e d i f f e r e n t i s o l a te s of each type)

S i s o l a t e

Concentra tion (mg/1) inhibi ting isolates of U. nuda

R1 isolate R2 i s o l a t e

Chemical* Spore st Promycelia~ Spores Promycelia Spores Promycelia

Benodanil 1 5 0.70 12 4.0 6.5 3 0

3.5 2.5 15 8.0 12 8 0

Carbox in 0 20 0.12 1 0 0.60 2.4 1.0

0.35 0.25 2.4 1.5 4 .6 3.0

Cyclafluramid 0 70 0.30 6- 0 2.5 13 5.0

1.0 0.70 7 5 4.0 25 8-0

Fen fura m 1.0 0.80 20 12 32 20

2.5 1.6 30 20 45 40

Flutolanil 15 7- 0 50 30 0 70 0 30

60 20 80 60 2.0 0 80

Furcarbanil 0 15 0.06 1.0 0.60 0.70 0.50

0.20 0.15 1.4 1.0 1.5 0.80

Furmecyclox 30 20 ND ND 30 18

70 45 ND ND 70 50

Mepronil 6.0 3.0 15 12 0.80 0.40

10 8.0 > 20 > 20 1.6 1.0

Methfur oxam 0 10 0 05 0.40 0.30 1.2 0 80

0.16 0.12 0 70 0.50 3.0 2.0

Oxycarboxin 65 30 > 200 200 200 100

120 90 > 2 0 0 >200 >200 180

Pyracarbol id 1 1 0. 80 6 5 4 .0 32 18

1.8 1.5 10 7 0 90 60

Antimycin A 0.04 0.05 0.04 0.04 0.06 0.08

0.12 0.20 0.12 0.20 0.20 0.20

2,4-Dinitrophenol 40 40 55 40 45 40

ND ND ND ND ND ND

Thenoy ltri fluoroacet one 25 25 25 25 25 25

80 90 70 90 90 100

* Chemical names:benodanil, 2-iodobenzanilide; carboxin, 5,6-dihydro-2-methyb1,4-oxathi-ine-3-carboxanilide; cyclafluramid, N-cyclohexyb2,5-dimethyb3-furamide; enfuram,

2-methyl-3-furanilide; flutolanil, a,cr,cr-trifluoro-Y-isopropoxy-o-toluanilide; urcarbanil, 2,5-dimethyl-3-furanilide; furmecyclox, methyl N-cyclohexyl-2,5-dimethylfuran-3-

carbohydroxamate; mepronil, Y-isopropoxy-o-toluanilide; methfuroxam, 2,4,5.~rimethyl-3-furanilide; oxycarboxin, 5,6.dihydro-2-methyl-l,4-oxathi-ine-3-carboxanilide

4,4-dioxide; pyracarbolid, 3,4-dihydro-6-methyl-2H-pyran-5-carboxanilide.

** EC50 upper number; EC90 lower number, in each column.

t Wi th eliospores, the EC50 and ECo0represent the concentrrations which give an inhibition of spore germination of 50% and 90%, respectively.

:1: Withpromycelia, the EC50 and EC90 represent the concentrations which give an inhibition of promcelial length of 50% and 90%, respectively.

ND: E C5 0 a nd

EC90 values

no t det erm i ned .

TABLE 2. Laboratory conditions for the routine monitoring of resistance

t o

carboxamides in

Ustilago nuda

Carboxin

Mepronil (0.5 mg/1)

(2- 5 mg/1) + meproni l

Strain Control or (2.5 mg/1)

of (without Carboxin Fenfuram flutolanil or flutolanil

U. nuda fungicides) (0 .5 mg/l) (7. 5 mg/l) (5 mg/1) (5 mg/l)

S + - - +

-

R 1

R2 + + + - -

+, germination of teliospores (presence of promycelium); -, no germination.

rial conditions

F o r e a c h

p l ot o f l m

2 1 8 g

s e e d w a s u s e d . S e e d w a s

s o w n o n 3 0 O c t o b e r 1 9 8 5 , e x c e p t f o r s e e d tr e a te d w i t h

m e p r o n i l w h i c h w a s s o w n o n 8 N o v e m b e r 1 9 8 5 .

C o n t r o l p l o t s w e r e s o w n a t b o t h d a t e s . T h e t r i a l h a d

t w o r e p l ic a t es a n d w a s c o n d u c t e d a t L a V e r r i ~ r e n ea r

V e r s a il le s . A t t h e b e g i n n i n g o f J u n e 1 9 8 6 , a t th e

f l o w e r i n g s t a g e , s m u t t e d a n d h e a l t h y h e a d s i n e a c h

p l o t w e r e c o u n t e d .

I n v i t r o

t e st s w i t h t el i o spo r es o f U .

n u d a

F o r e a c h e x p e r i m e n t a l c o n d i t i o n , 1 0 s m u t t e d h e a d s

w e r e c o l l e c t e d o n 1 0 d i f f e r e n t p l a n t s f i v e i n e a c h p l o t ) .

A s u s p e n s i o n o f t e li o s p o r e s i n s t e ri le w a t e r w a s

o b t a i n e d f r o m e a c h d i s e a s e d h e a d a n d p i p e t t e d o n t o

t h e s u r fa c e o f a g l u c o s e - a g a r m e d i u m w i t h o r w i t h o u t

f u n g i c i d e s. A f t e r a n i n c u b a t i o n o f 2 4 - 3 0 h a t 2 2 C ,

s p o r e g e r m i n a t i o n w a s o b s e r v e d u n d e r t h e m i c r o s c o p e

L e r o u x , 1 9 8 6 ) .

R e s u l t s

Ch a ra c t e r i s t i c s o f i s ol a t es o f

U . n u d a

T h r e e t y p e s o f s t r a in s h a v e b e e n d e t e c t e d i n o u r t r i a ls

Tab l e 1 .

T w o S a n d R 2) a r e s i m i l a r t o t h o s e d e s c r i b e d

p r e v i o u s l y L e r o u x , 1 9 8 6 ) a n d ar e c h a r a c t e r i z e d b y t h e

p h e n o m e n o n o f n e g a t iv e c r o s s r e s is t a n c e b e t w e e n

c a r b o x i n a n d m e p r o n i l . B e n o d a n i l , c y c l a f u r a m i d , f e n -

f u r a m , f u r c a r b a n i l , m e t h f u r o x a m , o x y c a r b o x i n a n d

p y r a c a r b o l i d e x h i b i t p o s i t i v e c r o s s r e s i s t a n c e w i t h

c a r b o x i n w h e r e a s f l u t o l a n i l h a s t h e s a m e e f f e c t a s

m e p r o n i l . T h e t h i r d ty p e o f s t r a in , r e s is t a n t t o

c a r b o x i n , fe n f u r a m , m e p r o n i l a n d f l u t a lo n i l R 1 ,

Tab l e 1 )

h a s b e e n f o u n d o n c v s G e r b e l a n d V i v a

see

Tab l e 4 ) .

T h e t h r e e t y p e s o f s t r ai n s d o n o t d i f f e r i n

t h e i r s e n s i t i v i t y t o t h e n o n - c a r b o x a m i d e r e s p i r a t o r y

i n h i b i to r s a n t i m y c i n A , 2 , 4 - d i n i t r o p h e n o l a n d t h e n o y l -

t r i f l u o r o a c e t o n e Tab l e 1 ) .

CROP P ROT ECT ION Vol. 7 February 1988

7/23/2019 1988 (Leroux, Berthier) Resistance to Carboxin and Fenfuram

3/4

18 Resistance to carbo xamides in Ust i lago nuda

TABLE 3. Efficacy o f various fungicides against barley loose smut (resul ts expressed as the percentage of smutt ed heads at the flowering stage)

Sowing date 30 October 1985

Sowing date 8 November 1985

Variety Carboxin Fenfuram Triadimenol * Flutri afolt Mepronil

of barley Cont rol (100 g/q) (80 g/q) (30 g/q) (5 g/q) Cont rol ( 100 g/q)

Viva (Lyon) 19.5 15.1 19.7 0.0 0.2 18.2 5.6

Viva (Niort) 17.0 15.3 19.5 0.0 0.0 18.7 11.7

Viva (Orleans) 8.6 6.0 7.1 0.0 0.0 9.1 3.6

Panda 13.9 6.2 12.0 0.0 0.0 12.7 2.2

Gerbel 2.8 0.9 2.4 0.0 0 0 2.6 1.8

Thibau t 13.0 0.0 0.0 0 0 0' 0 13 2 13.9

T r i a d i m en o l , 1 - 4 - ch l o r o p h en o x y ) - 3 , 3 - d i m et h y l - l - 1 H- 1 , 2 , 4 - t r i azo l - l - y l ) b u t an - 2 - o l .

t F l u t r l a f o l

(RS)-2,4 -di f luore~a.(1H-1,2,4-tr lazol-l -ylmethyl)benzhydryl

a l co h o l .

TABLE 4. Phenot ypes of strains of stilago nuda collected at the floweri ng stage of barley plants obtained from untreated o r carboxamide-treated seed

Sowing date 30 October 1985 Sowing date 8 November 1985

Carboxin Fenfura m Mepronil

Variety of barley Control (100 g/q) (80 g/q) Control (100 g/q)

Viva (Lyon) 1R1, 9R2 10R2 10R2 1S, 9R2 10R2

Viva (Niort) 10R2 10R2 10R2 10 R2 10R2

Viva (Orleans) 10R2 10R2 10R2 10R2 5R2 *

Panda 10R2 10R2 10R2 10R2 2R2 *

Gerbel 3S, 3R1, 4R2 3R1, 5R2 4R1, 6R2 2S, 1R1, 2R2 IS, 1R2*

Thibau t 10S -- -- 10S 10S

* L e s s t h a n 1 0 s m u t t e d h e a d s h a v e b e e n t e s t e d i n e a c h o f t h e s e c o n d i ti o n s .

TABLE 5. Carboxin resistance in stilago nuda in France (monitored in

June and July, 1985)

Variety

Number of plots* with:

Seed dressings Mixtures of

with (+ ) or Sensitive sensitive and Resistan t

without ( - ) isolates resistant isolates

carboxamides only isolates only

Antares - 2 0 0

+ 2 0 0

Barberousse - 4 0 0

+ 2 1 4

Cabro - 3 0 0

+ 0 2 1

Capri - 2 0 0

+ 0 1 1

Castel + 0 0 1

Gerbel - 2 1 0

+ 0 1 2

Igri + 1 2 0

1 0 3

Illia - 1 0 0

+ 0 2 3

Mogador - 0 2 0

Nefta + 1 0 0

Nymphe + 1 0 0

Panda - 3 2 5

+ 2 3 15

Pirate + 1 1 0

Plaisant + 1 0 0

Smash + 0 0 1

Sonja - 3 0 0

+ 2 4 1

Thibau t - 2 0 0

+ 2 1 0

Viva - 3 3 4

+ 2 4 11

* F r o m e a c h p l o t 5 - 1 0 s m u t t e d h e a d s w e r e t e s t e d a n d t h e r e s i s ta n t i s o la t e s c a n b e

e i t h e r t y p e R 1 o r t y p e R 2 .

D u r i n g o u r in v e s t i g a ti o n s i n 1 9 8 6 w e a l w a y s f o u n d

o n l y o n e t y p e o f st r ai n i n e a ch s m u t t e d h e a d . I n o u r

r o u t i n e m o n i t o r i n g w e u s e d t h e c o n d i t i o n s s e t o u t i n

Table 2

t o c h a r a c t e r i z e t h e i s o l a t e p r e s e n t o n e a c h

d i s e a s e d p l a n t .

Field act iv i t y o f fungicides

C a r b o x i n a n d f e n f u r a m d i d n o t c o n t r o l lo o s e s m u t o n

c v s V i v a a n d P a n d a w h e r e a s 1 0 0 c o n t r o l w a s

o b t a i n e d o n c v . T h i b a u t ( T a b l e 3). T h e s e r e s u lt s c a n b e

e x p l a i n e d b y t h e f a c t t h a t r e s i s t a n t s t ra i n s p r e d o m i n a t e

o n t h e f i r s t t w o v a r i e t i e s a n d a r e a b s e n t o n t h e t h i r d ( i n

t h e a b s e n c e o f s e e d d r e s s i n g s ) ( T a b l e

4).

O n c v . G e r b e l ,

c a r b o x i n h a d a n e f f ic a c y o f 7 0 w h e r e a s f e n f u r a m w a s

i n e f f e c t iv e . T h i s c a n b e e x p l a i n e d b y t h e d i f f e r e n c e s in

a c t i v it y b e t w e e n t h e s e t w o c a r b o x a m i d e s o n s t r a in s o f

t y p e R 1

Table 1) .

H o w e v e r , t h e l e v e l o f d i se a s e w a s

l o w , s o t h i s c o n c l u s i o n c a n n o t b e g e n e r a l i z e d .

S e e d d r e s s i n g w i t h m e p r o n i l d i d n o t e r a d ic a t e l o o s e

s m u t b u t s o m e t i m e s i t g a v e c o n t r o l g re a t e r t h a n 5 0 .

T h i s w a s o b s e r v e d o n l y w h e n s t ra i n s o f t y p e R 2

( s e n s i t i v e t o me p r o n i l ) w e r e p r e s e n t . O n t h e o t h e r

h a n d , t h e a b s e n c e o f a c ti v i ty o n c v . T h i b a u t c a n b e

c o r r e l a t e d w i t h t h e p r e s e n c e o f s tr a i n S w h i c h i s

t o l e r a n t t o me p r o n i l ( T a b l e s

3

and 4 ) .

D i s c u s s i o n

T h e t r i a l s c o n d u c t e d i n 1 9 8 6 c o n f i r m t h e p r e s e n c e , i n

n a t u r a l c o n d i t i o n s , o f U .

n u d

i s o l a t e s r e s i s t a n t t o

c a r b o x in . T h o s e w h i c h h a v e t h e h i g h e s t le v e l o f

r e s i st a n c e t y p e R 2 ) a r e p r e v a l e n t a n d h a v e t h e s a m e

c h a r a c t e r is t ic s a s t h e o n e s d e t e c t e d i n 1 9 8 4 a n d 1 9 8 5

L e r o u x , 1 9 8 6 ) . T h e i r m a i n p r o p e r t y i s t h e i r h i g h

s e n s i t i v i t y t o m e p r o n i l a n d f lu t o l a n i l . T h i s c a n b e

i n t e r p r e t e d a s n e g a t i v e c r o s s r e s i s t a n c e b e t w e e n t w o

t y p e s o f c a r b o x a m i d e f u n g i c i d e s . A s i m i l a r n e g a t i v e

CROP PRO TEC TI ON Vol. 7 February 1988

7/23/2019 1988 (Leroux, Berthier) Resistance to Carboxin and Fenfuram

4/4

P. LEROUX AND G. BERTHIER

c o r r el a ti o n b e t w e e n c a r b o x a m i d e s h a s b e e n f o u n d i n

s t u d i e s w i t h l a b o r a t o r y m u t a n t s o f Ust i l a g o ma y d i s

( W h i t e , T h o r n a n d G e o r g o p o u l o s , 1 9 7 8 ) ; t h e c a r b o x -

a m i d e s s e l e c ti v e l y t o x i c t o m u t a n t s t ra i n s ( s u c h a s

m e p r o n i l o r f i u t o l a n i l ) w e r e c a r b o x i n a n a l o g u e s a l s o

s u b s t i t u t e d o n t h e p h e n y l r i n g . S u c h s i m i l a r i t i e s

b e t w e e n

U. maydis

a n d

U~ nuda

c a n a l so i nd i c a t e t ha t

r e s i s t a nc e t o c a r box in i s a t t r i bu t a b l e , i n bo th c a se s , t o

m o d i f i c a ti o n o f t h e s u c c i n i c d e h y d r o g e n a s e c o m p l e x .

H o w e v e r , b i o c h e m i c a l a n d g e n e t i c s tu d i e s a re r e q u i r e d

t o e l u c i d a t e th e m e c h a n i s m s o f r e s i st a n c e to c a r b o x i n

in U. nuda.

U n d e r f i e l d c o n d i t i o n s , w h e n t h e v a r i e t i e s V i v a o r

P a n d a a r e c o n t a m i n a t e d b y s tr a in s o f U. nuda

r e s i st a n t t o c a r b o x i n , t h i s f u n g i c i d e a n d a l s o f e n f u r a m

a r e i n e f fe c t iv e . I n c o n t r a s t , 1 0 0 % c o n t r o l o f l oo s e s m u t

is a c h i e v e d w h e n t h e f u n g u s i s se n s it iv e , a s w a s t h e

c a s e w i t h t h e s a m p l e o f cv . T h i b a u t . S u c h r e s u l ts

i n d i c a t e t h a t c a r b o x a m i d e r e s i s t a n c e i s a p r o b l e m i n

pr a c t i c e f o r t he c on t r o l o f l oose sm ut o f ba r le y .

I n F r a nc e a t p r e se n t i t i s poss ib l e t o de t e c t r e s i s t a n t

s t ra i n s o n t h e m o s t c o m m o n v a r i e ti e s o f w i n t e r b a r l e y

Table 5) . Ho we ve r , t he i r JT re que nc ie s r e m a in ge ne r a l l y

l o w i n t h e a b s e n c e o f s e e d d re s s i n g s a n d t h e y a r e

d e t e c t e d o n l y w h e n c a r b o x a m i d e s a r e s t i l l e f f e c t i v e

a g a i n st t h e l o o s e s m u t o f b a rl e y . I n t h o s e f e w s i t u a ti o n s

i n w h i c h h i g h f r e q u e n c i e s o f r e s is t a n t i s o la t es a r e

f o u n d i n t h e a b s e n c e o f t r e a t m e n t w i t h r e g i s t e r e d

c a r b o x a m i d e s , t h r e e s o l u t io n s c a n b e c o n s i d e r e d :

1 . I n v i e w o f t h e l o w l e v el o f r e s is t a n c e to w a r d s s o m e

c a r b o x a m i d e s , w e c a r l u s e t h e m a t h i g h e r d o s e

l e v e l s . S o m e p r e l i m i n a r y t r i a l s w i t h e x p e r i m e n t a l

c h e m i c a l s h a v e g i v e n u n e n c o u r a g i n g r e s u l t s ( G .

B e r t h i e r , u n p u b l i s h e d d a t a ) .

2 . T h e m i x t u r e o f t w o n e g a t i v e l y c o r r e l a t e d c a r b o x -

a m i d e s c a n b e c o n s i d e r e d (e .g . c a r b o x i n +

m e p r o n i l ) . T h i s s o l u t i o n i s o f li m i t e d i n t e r e s t i n

p r a c t i c e , m a i n l y b e c a u s e s o m e s t r a i n s w i l l n o t b e

a f f e c t e d ( R1 type ) .

19

3 . A t p r e se n t , t he on ly p r a c t i c a l poss ib i l i t y i s s e e d

d r e s s i n g w i t h i n h i b i t o rs o f s t e ro l C - 1 4 d e m e t h y l a -

t i o n . I n F r a n c e , t r i a d i m e n o l a n d f l u t r i a f o l a r e

r e g is t e re d a n d a r e r e c o m m e n d e d f o r u se o n t h e

v a r ie t ie s V i v a a n d P a n d a ( E s c h e n b r e n n e r , 1 98 6) .

c k n ow l e d g emen t s

W e a r e i n d e b t e d to t h e C o m p a n i e s D o w C h e m i c a l a n d

L a Q u i n o l e i n e w h i c h p r o v i d e d s a m p l e s o f s m u t t e d

h e a d s a n d s e e d s o f b a rl e y .

Re f e r en c e s

BOURDIN, J . (1983). Le traitement des semences de c6r6ales .

Phytoma 3 5 1 , 4 0 -4 1 .

ESCHENBRENNER, P. (1986). L e trai tem ent des sem ences; un

march6 en p le ine 6vo lu t ion?

PerspectivesAgricoles

107 , 46-49 .

GROUET, D. , MONTFORT, F . AND LEROUX, P . (1981). M ise en

6vidence , en Fr ance , d une souche de

Puccinia horiana

r6s is tan te ~ l oxycarbo xine .

Phytiatrie Phytopharmacie

30 ,

3 -1 2 .

LEROUX, P. (1986). Caract6ris tiques des souches

d Ustilago nuda,

agen t du charbon nu de Forge , r6s is tan tes ~ la ca rbox ine .

Agronomie

6 , 2 2 5 -2 2 6 .

RICHARD, G. AND COGNET, J . (1967). A ction f ongic ide du Vita vax

l 6gard des cha rbons nus d e l avo ine e t de l o rge . Comptes

rendus hebdomadaires de l Acad3 mie d Agriculture 5 3 , 1 2 6 7 -

1271.

VENTURA, E. , BOURDIN, J . AND PIEDALLU, C. (1968). A ctivit6

fong ic ide de la ca rbox ine , v is ~ v is des p r inc ipaux pa ras i te s

des sem ences d e c6r6ales .

Phytiatrie Phytopharmacie

17 , 197-

207.

WH ITE, G . A ., THO RN, G. D. AND GEORGOPOULOS, S. G . (1978).

Oxa th i in ca rboxam ides h igh ly ac tive aga ins t ca rbox in-res is tan t

succ in ic deydrogenase complexes fo r ca rbox in-se lec ted

mu ta n t s o f

Ustilago ma ydis

a n d

Aspergillus nidulans. Pesticide

Biochemistry and Physiology

9 , 165-192 .

R e c e iv e d 9 M a rc h 1 98 7

Revised 17 June 1987

A c c e p te d 9 S e p te mb e r 1 9 87

C R O P P R O T E C T I O N V o l. 7 F e b r u a ry 19 88