Pestic. Sci. 1997, 51, 290È298

Sensitivity Profiles of Mycosphaerella graminicolaand Phytophthora infestans Populations toDifferent Classes of Fungicides*

Ulrich Gisi,¤ Dietrich Hermann, Leonie Ohl & Christoph Steden

Novartis Crop Protection AG, Agrobiological Research Station, CH-4108 Witterswil, Switzerland

(Received 1 May 1997 ; revised version received 20 June 1997 ; accepted 10 July 1997)

Abstract : Prior to the use of fungicides, the baseline sensitivity of individuals in apathogen population may already di†er by a factor of 10 to 100 between the leastand the most sensitive isolates. In Mycosphaerella graminicola populations, thisfactor, measured in vitro, was 5 to 20 for both the strobilurin analogue azoxystro-bin (baseline) and the triazole cyproconazole which has been in use for severalyears. In Phytophthora infestans populations, this factor, measured in a leaf discassay, was about 100 for azoxystrobin (baseline), up to 1000 for the cyano-acetamide cymoxanil and [10 000 for the phenylamide oxadixyl ; both of thelatter have been used for many years. In M. graminicola, cross-sensitivity waspresent between all azole fungicides for the majority of the isolates, whereas nocorrelation was found between triazoles and azoxystrobin. Despite the existenceof cross-sensitivity between azoles, “box-and-whiskersÏ plots revealed large varia-tions in the sensitivity proÐles of some triazoles ; isolates resistant to triazoleshave not been detected in M. graminicola populations. In P. infestans popu-lations, the proportion of the phenylamide-resistant sub-population increasedduring the season more rapidly in treated than in untreated Ðelds, but it was lowat the beginning of the next season in all Ðelds. During disease epidemics, theÐtness of phenylamide-resistant P. infestans isolates, as characterised by lesionsize, was higher than that of the sensitive isolates, but after the overwinteringperiod, the recovery of resistant isolates was apparently lower. The presence ofboth A1 and A2 mating types of P. infestans in European populations, althoughat di†erent frequencies, allows sexual recombination and increased genetic diver-sity, a†ecting sensitivity and Ðtness. Such mixed populations can still be ade-quately controlled by using sound anti-resistance strategies.

Pestic Sci., 51, 290È298, 1997No. of Figures : 6. No. of Tables : 3. No. of Refs : 16

Key words : strobilurins, triazoles, phenylamides, cyanoacetamide, resistance,cross-sensitivity, Ðtness

* Based on a presentation at the Conference “Resistance Ï97ÈIntegrated Approach to Combating ResistanceÏ organised by theInstitute of Arable Crops Research in collaboration with the SCI Pesticide Group and the British Crop Protection Council andheld at Harpenden, Herts, UK on 14È16 April 1997.¤ To whom correspondence should be addressed.

2901997 SCI. Pestic. Sci. 0031-613X/97/$17.50. Printed in Great Britain(

Sensitivity proÐles of M. graminicola and P. infestans to fungicides 291

1 INTRODUCTION

The application of fungicides to control fungal diseaseeliminates, in most cases, the majority of the pathogenpopulation present in the crop. Nevertheless, a smallpart of the population will survive because of inade-quate fungicide coverage of some plant parts, andbecause some individuals of the pathogen populationmay be less sensitive to the fungicide prior to the appli-cation. Also, new inoculum appears in the crop bymigration from neighbouring Ðelds which have not beentreated at all, or not at the same time. The pathogenpopulation will start to grow again mainly because theoriginal amount of fungicide decreases through degra-dation and, consequently, repeated applications may benecessary, especially for fast-growing populations. Themost sensitive sub-populations are well controlled, butless sensitive and resistant sub-populations are lessa†ected or not controlled at all ; they may increase infrequency, especially when the selection pressure isstrong and persistent.

Prior to the use of fungicides, the baseline sensitivityof individuals in a pathogen population may alreadyvary by a factor of 10 to 100 between the most and theleast sensitive isolate.1 The Ðrst step in the selectionprocess is caused by the fungicide and may result in thesurvival and increase of less sensitive isolates. Thesemay become dominant as long as the selection pressurepersists, but decrease in frequency once fungicide appli-cations are terminated. In such situations the less sensi-tive individuals are (by deÐnition) less Ðt than thewild-type population. The second step in the selectionprocess is not related to sensitivity of isolates butfavours individuals with higher Ðtness attributes, e.g.with shorter incubation period and sporulation time, orwith a larger lesion size and sporulation capacity. Inorder to understand the dynamics of fungicide-treatedpopulations, it is of equal importance to monitor thesensitivity of treated and untreated populations as wellas to follow epidemiological parameters like Ðtness,virulence, mating type behaviour and frequency ofsexual recombination. Investigations on the geneticbackground of the mode of resistance may contribute toestimates of the risk of product failures due to resistantsub-populations.

In this contribution, the sensitivity proÐles ofMycosphaerella graminicola (Fuckel) Schroter and Phy-tophthora infestans (Mont.) DeBary populations aredescribed and analysed both for a fungicide not yet usedcommercially (the strobilurin azoxystrobin), and forfungicides which have been used for many years, suchas the cyanoacetamide cymoxanil, the phenylamideoxadixyl and triazole fungicides, e.g. cyproconazole.Cross-sensitivity behaviour between fungicides aswell as important epidemiological parameters oftreated and untreated populations are presented anddiscussed.

2 MATERIALS AND METHODS

In all sensitivity assays, fungicides were used as formu-lated compounds. Examples of four di†erent classes offungicide were included in the investigations : the cyano-acetamide cymoxanil (500 g kg~1 WP), the phenylamideoxadixyl (250 g kg~1 WP), the strobilurin azoxystrobin(250 g litre~1 SC) and the demethylation inhibitors(DMIs, azole fungicides) cyproconazole (100 g litre~1SL), tebuconazole (250 g litre~1 EC), epoxiconazole(125 g litre~1 SC), and prochloraz (450 g litre~1 EC). Arange of four or Ðve fungicide concentrations was pre-pared with ten-fold dilution steps. The response of thepathogens to the fungicides was rated visually and dose-response curves were constructed with the help of alogit-log computer programme; the (e†ective fun-EC50gicide concentration resulting in 50% inhibition ofgrowth or sporulation) was calculated for each isolate.M. graminicola (anamorph Septoria tritici Rob. exDesm.) isolates were obtained from pycnidia-bearinglesions of leaves collected from DMI-treated or -un-treated Ðelds in several countries over a period offour to eight weeks during several years. The isolationprocedure and the in-vitro sensitivity test method onagar plates are described in more detail by Gisi andHermann.2 P. infestans isolates were obtained frominfected leaves (from treated and untreated Ðelds) andplaced between two potato tuber halves (fortransportation). Sporangia formed after a few days weresufficient in quantity for an immediate sensitivity testwithout the need for any transfer. The sensitivity testwas performed on leaf discs produced from fungicide-treated potato plants as described in the FRACmethod-collection by Sozzi et al.3 The Ðtness evaluationof P. infestans isolates was done simultaneously with thesensitivity test on untreated leaf discs of potato, cv.Bintje, inoculated with 25] 103 sporangia ml~1 andincubated at 18¡C; the measurements were taken two,three, four and Ðve days after inoculation. For both P.infestans and M. graminicola the isolates were con-sidered to be bulk samples. For sensitivity and cross-sensitivity tests, as well as Ðtness analyses, 20 to 260isolates per country (or test) were used.

3 RESULTS

3.1 Mycosphaerella graminicola populations

In wheat, one or two fungicide applications have beenmade per season for many years to control M. gramini-cola, especially with azole fungicides. Since 1992, iso-lates of M. graminicola populations from di†erentcountries have been collected and tested for their sensi-tivity to cyproconazole. There are no indications of adecreased sensitivity ; the width of sensitivity proÐlesremained unchanged but varied by a factor of 5 to 40

292 Ulrich Gisi et al.

TABLE 1Sensitivity of Mycosphaerella graminicola to Cyproconazole for Isolates from

France, Germany England and Switzerland collected between 1992 and 1996

EC50 (mg litre~1)

Mean Min. MaxNo. of W idth of

Country Y ear isolates distribution

France 1994 9 0É11 0É04 0É30 81995 21 0É11 0É02 0É40 201996 76 0É11 0É03 0É32 11

Germany 1994 14 0É11 0É03 0É30 101995 24 0É08 0É03 0É20 71996 22 0É09 0É02 0É14 7

England 1992 259 0É18 0É03 0É90 301993 219 0É15 0É01 0É40 401994 57 0É14 0É05 0É50 101995 87 0É10 0É01 0É40 401996 93 0É10 0É03 0É24 8

Switzerland 1995 9 0É07 0É04 0É20 51996 20 0É07 0É01 0É13 13

(Table 1). The populations have remained unimodal,and no evidence of two classes within the populationshas emerged. Isolates outside the unimodal distribution,that may be considered as azole-resistant isolates, havenot been detected since 1991 and it is not knownwhether a shift could have occurred in earlier years. Onthe other hand, the “box-and-whiskersÏ plots revealedrather large variations in the sensitivity proÐles forsome populations ; this variation in both the boxes(50% of population) as well as the whiskers was muchmore pronounced for tebuconazole than for cyprocona-zole, although the minimum values were aboutEC50the same for the two molecules (Fig. 1).

Twenty-four isolates of the 1996 population fromFrance, representing the entire range of sensitivity, werechosen for cross-sensitivity studies. Between all pairs ofazole fungicides, cross-sensitivity was present with acorrelation coefficient (r) between 0É52 (P\ 0É01) and

Fig. 1. Sensitivity of Mycosphaerella graminicola populationsto cyproconazole (c) and tebuconazole (t) in England (UK),

France (F), Germany (D) and Switzerland (CH), 1996.

0É86 (P\ 0É001) (Fig. 2). All regression lines were more-or-less parallel to the transect line of the scatter plots,indicating a similar cross-sensitivity behaviour for alltested isolates, but some azoles displayed a higherintrinsic activity than others (Fig. 2B:epoxiconazole[ cyproconazole, 2C: prochloraz [cyproconazole, 2D: epoxiconazole[ tebuconazole, 2E :prochloraz [ tebuconazole). When entire Ðeld popu-lations were tested for cross-sensitivity to the pairtebuconazole/cyproconazole, a correlation between thetwo fungicides was still present (r \ 0É34 for France,r \ 0É46 for England) with high signiÐcance levels(P\ 0É01 and 0É001, respectively), but the cross-sensitivity behaviour was not very pronounced for someisolates, especially for those which were most sensitiveto cyproconazole (Fig. 3A).

When isolates from France were analysed for theircross-sensitivity between the triazole cyproconazole andthe chemically unrelated strobilurin azoxystrobin, nocorrelation could be identiÐed (r \ 0É16, P[ 0É1) (Fig.3B). The mean values of the sensitivity distributions asmeasured by values were 0É04 and 0É11 mg litre~1EC50for azoxystrobin and cyproconazole, respectively, reÑec-ting the di†erent intrinsic activities of the two mol-ecules, whereas the width of the distribution was afactor of 15 and 11, respectively. The M. graminicolapopulations have not previously been exposed toazoxystrobin and therefore, the sensitivity distributioncan be considered as a baseline. Although triazoles havebeen used for many years, the width of the sensitivitydistribution to cyproconazole was about the same asthat found for azoxystrobin (Fig. 4). There have been nodi†erences in sensitivity distributions of European M.graminicola populations to cyproconazole over the lastÐve years (Table 1), not even between treated anduntreated Ðelds (results not shown).2

Sensitivity proÐles of M. graminicola and P. infestans to fungicides 293

Fig. 2. Cross-sensitivity behaviour in Mycosphaerella graminicola to DMI fungicides. A : Cyproconazole versus tebuconazole ; B :cyproconazole versus epoxiconazole ; C : cyproconazole versus prochloraz ; D: tebuconazole versus epoxiconazole ; E : tebuconazoleversus prochloraz ; F : epoxiconazole versus prochloraz. SigniÐcance level for correlations : ** : P\ 0É01 ; *** : P\ 0É001 (n \ 24).

294 Ulrich Gisi et al.

Fig. 3. Cross-sensitivity behaviour in Mycosphaerella gramini-cola isolates from France collected in 1996. A : Cyproconazoleversus tebuconazole ; B : cyproconazole versus azoxystrobin.SigniÐcance level for correlation : ** : P\ 0É01 ; ns : not signiÐ-

cant (P[ 0É1).

3.2 Phytophthora infestans populations

Several fungicide classes, including products containingphenylamides or cymoxanil, have been used world-widefor many years to control P. infestans, the causal agentof late blight in potato and tomato. Both classes areused in combination with contact fungicides (e.g.dithiocarbamates like mancozeb). The strobilurinazoxystrobin is also active against P. infestans,4 but hasnot been used commercially so far. In a leaf disc assay,the sensitivity of the Swiss P. infestans populations of1996 was determined for the three fungicides, azoxystro-bin, cymoxanil and oxadixyl. The baseline sensitivity ofisolates to azoxystrobin varied by a factor of up to 100,whereas the sensitivity proÐles to cymoxanil and oxa-dixyl were di†erent by factors of up to 1000 and[10 000, respectively, between the most and the least

Fig. 4. Sensitivity distribution of Mycosphaerella graminicolato cyproconazole and azoxystrobin ; isolates from France col-lected in 1996. mean sensitive reference isolate ;(…) EC50 , (+)

reference isolate with decreased sensitivity to triazoles.(@)

sensitive isolate (Fig. 5). For azoxystrobin, no resistantisolates were detected and the population can bedescribed as original log-normal distribution. A largevariation for the sensitivity distribution to cymoxanilwas observed, but no resistant isolates were found. Inmycelial growth tests, this variation can be smaller.5,6In contrast, distinct subpopulations with a sensitive,intermediate and resistant response to oxadixyl werepresent in the Swiss P. infestans population (Fig. 5).There is a strong cross-resistance behaviour for P. infes-tans isolates between all phenylamide fungicides(metalaxyl, oxadixyl, benalaxyl, ofurace),7 but there wasno correlation in cross-sensitivity between azoxystrobinand oxadixyl nor between azoxystrobin and cymoxanilfor the 105 isolates collected in 1996 in Switzerland(data not shown). Cross-sensitivity analyses betweenoxadixyl and cymoxanil revealed the presence of iso-lates with six of the nine possible sensitivity com-binations (oxadixyl/cymoxanil : s/s, s/i, i/s, i/i, r/s, r/i),but no isolate contained resistance against cymoxanil(s/r, i/r, r/r) (Table 2). The most dominant sub-populations were those with full sensitivity to both oxa-dixyl and cymoxanil (s/s \ 30%) and those resistant tooxadixyl and intermediate to cymoxanil (r/i\ 37%).

Sensitivity proÐles of M. graminicola and P. infestans to fungicides 295

Fig. 5. Sensitivity distribution of Phytophthora infestans to azoxystrobin, cymoxanil and oxadixyl ; isolates from Switzerland col-lected in 1996. mean for sensitive reference isolate.(@) EC50

Over the last ten years, two important epidemiologi-cal events occurred in the Swiss (and European) P. infes-tans populations :

(1) At the expense of the resistant sub-population, theproportion of isolates intermediate in sensitivityto oxadixyl (phenylamides) increased from almostnil to about a quarter of the population (Fig. 6).These isolates can be either “mixed isolatesÏ (s] r,s ] i) or genetically stable intermediates (i) to oxa-dixyl originating from sexual recombination.

Since both mating types, A1 and A2, are presentin European populations,8 although in di†erentproportions (e.g. 96% and 4%, respectively, inSwitzerland), sexual recombination may occur9favouring genetic diversity in populations andthus allow segregation into resistant, intermediateand sensitive sub-populations from populationspreviously dominated by resistant individuals.8

(2) During the epidemic phase of the disease cycle,the proportion of P. infestans isolates resistant tophenylamides increases in both treated and

296 Ulrich Gisi et al.

TABLE 2Sensitivity of Phytophthora infestans Field Isolates to Oxa-dixyl and Cymoxanil in the 1996 population from Switzerland

(n \ 112)a

Oxadixyl Cymoxanil Proportion (%)

s s 30s i 8s r 0i s 7i i 16i r 0r s 2r i 37r r 0

a r, i and s refer to resistant, intermediate and sensitive, withvalues [1000, [20 but \1000 and \20 mg litre~1,EC50

respectively.

Fig. 6. Proportion of Phytophthora infestans isolates (% oftotal) collected in Swiss potato Ðelds between 1988 and 1996showing a sensitive (s), intermediate (i) and resistant (r)

response to phenylamide fungicides.

untreated populations. Because of fungicide selec-tion pressure, this increase is more rapid intreated compared to untreated potato Ðelds.8Nevertheless, at the beginning of the next season,the proportion of the resistant sub-population isagain rather low. These observations, made inseveral countries over many years,8,10,11 suggestthat resistant isolates have a higher Ðtness duringthe epidemic phase but are recovered less fre-quently after the overwintering period of thepathogen.8 Model trials with mixed populations(s ] r \ 9 ] 1) revealed that resistant isolates“coloniseÏ the potato tissue (leaf during epidemic,tuber during overwintering) much faster than sen-sitive isolates.8 In fact, the Ðtness of P. infestansisolates collected in 1996 in Switzerland washigher for the resistant than the sensitive isolates :the incubation period and sporulation timetended to be shorter, whereas lesion size, colo-nization rate, and thus also the Ðtness product,were higher for resistant than for sensitive isolates(Table 3).

During the season, the proportion of highly Ðt isolatesslightly increased. The few A2 type isolates tested weresomewhat less Ðt than the A1 isolates (Table 3), whichmay help to explain the low frequency of A2 isolates inEuropean P. infestans populations in potato Ðelds.8 Pre-liminary observations revealed a much higher propor-tion of A2 type isolates in P. infestans populationscollected from tomato than from potato Ðelds(Knapova and Gisi, unpublished results).

4 DISCUSSION AND CONCLUSIONS

Although azole fungicides have been used for manyyears for disease control in wheat, no M. graminicola

TABLE 3Fitness Evaluation of Phytophthora infestans Field Isolates collected in 1996 in Switzerland

L esion size (mm2)aIncubation Colonisation Sporulation Fitness No. of

Isolates period (day) After 3 days After 4 days rate (mm2 day~1)b time (day) productc isolates

PA-resistantd 2É6 (^0É5) 78 (^59)* 299 (^138)** 221 (^108) 3É8 (^0É5) 22É4 43PA-sensitive 2É7 (^0É5) 58 (^53)* 249 (^143)** 191 (^111) 4É1 (^0É6) 17É2 41Junee 2É5 (^0É5) 69 (^59) 256 (^140) 187 (^97) 4É0 (^0É5) 18É7 30Julye 2É7 (^0É5) 69 (^57) 279 (^141) 210 (^118) 3É0 (^0É5) 25É9 63A1 2É6 (^0É5) 69 (^58) 271 (^141) 202 (^112) 3É9 (^0É5) 19É9 103A2 2É5 (^0É5) 77 (^67) 263 (^195) 186 (^138) 4É0 (^0É6) 18É6 6

a */** : signiÐcantly di†erent from each other at P\ 0É05 (one-tailed t test).b Di†erence in lesion size between 3rd and 4th day.c [Colonisation rate]/[incubation period] sporulation time].d PA\ phenylamide.e Isolates collected in June or July.

Sensitivity proÐles of M. graminicola and P. infestans to fungicides 297

isolates resistant to azoles, i.e. isolates outside the log-normal distribution, have been detected in Europeanpopulations. Azole fungicides express di†erent intrinsicactivities against M. graminicola, but there is cross-sensitivity between azoles of the majority of isolates(Fig. 2).12 Certain azoles may lose some activity againstless sensitive isolates earlier than others ; therefore, thegeneral cross-sensitivity behaviour may be hidden insome cases. A shift towards a reduction in sensitivity tospeciÐc triazoles has been recorded in the UK, but it isunclear whether this shift is seasonal or if it will pro-gressively reduce the overall sensitivity of M. gramini-cola to all triazoles.13 The width of the sensitivitydistribution was about the same for the triazole cypro-conazole and the strobilurin azoxystrobin, and both arealmost perfect log-normal and unimodal distributions(Fig. 4). Since the distribution proÐle for azoxystrobincan be considered to be baseline, it is appropriate toclaim that, for cyproconazole, no major shifts in sensi-tivity have occurred so far. As exempliÐed by cyprocon-azole, the sensitivity proÐle of a product with a longspray history may not be more extended than the base-line proÐle of new chemistry, e.g. the strobilurin azoxy-strobin. In contrast, much broader baseline sensitivityproÐles have been described for other new fungicideslike quinoxyfen in Erysiphe graminis DC14 or the anilino-pyrimidine pyrimethanil1 in Botrytis cinerea Pers. exFr. It is not known whether di†erent selection processesexist for M. graminicola within triazoles as has beenclaimed to occur in Rhynchosporium secalis Davis fortriadimenol versus propiconazole.15

The sensitivity proÐle of azoxystrobin was muchwider for P. infestans (Fig. 5) than for M. graminicolapopulations (Fig. 4), probably because of di†erenttesting methods (in-vivo leaf disc versus in-vitro agarplate test). Nevertheless, the P. infestans sensitivityproÐle was much narrower for azoxystrobin (factor ofabout 100) than for cymoxanil (up to 1000) and for thephenylamide oxadixyl (factor [10 000) (Fig. 5). As dis-cussed by Gisi and Cohen,8 no genetic link has beenfound in P. infestans between sensitivity to phenylamidefungicides and mating type, nor between sensitivity tophenylamides and Ðtness. The high proportion ofphenylamide-resistant isolates occurred prior to themore frequent appearance of A2 type isolates inEurope.8 The latter isolates are mostly sensitive, andseem to be less Ðt than the A1 isolates. Increased Ðtnessof P. infestans isolates probably developed soon afterphenylamide-resistant isolates were selected from theoriginal population by the use of phenylamide fungi-cides, otherwise the presence and increase of resistantisolates during the season in Ðelds not treated withphenylamides cannot be explained.8 Migration of resist-ant sporangia, or the import in tubers of myceliumresistant to phenylamides, contribute to mixed inoculain untreated Ðelds. In addition, the presence of both A1

and A2 mating type isolates in European P. infestanspopulations allows sexual recombination and this mayhelp establish genetically diverse populations, as well asa mixture of sensitive, intermediate and resistant sub-populations to phenylamides, that may be equally Ðt.Such mixed populations can be adequately controlledwith sound anti-resistance strategies as recommendedby the FRAC group.16

It is recommended that strong anti-resistance stra-tegies be implemented early in the life cycle of a newclass of fungicide. Resistant individuals may exist inoriginal populations prior to the use of fungicides ; theyare low both in frequency and in Ðtness at the begin-ning, but may increase in frequency as a result of theselection process. The Ðrst step of this process isimposed by the fungicide but increased Ðtness may beacquired later through events unrelated to the use offungicides but through evolutionary processes.

ACKNOWLEDGEMENTS

Our sincere thanks go to C. Steiner, U. Hugelshofer, E.Rimbach, D. Edel and T. Tsamdha for technicalsupport and to Ðeld technicians in various countries forsample collection. We acknowledge the critical reviewof the manuscript by K. M. Chin.

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