Cucurbit downy mildew (Pseudoperonospora …

1 Cucurbit downy mildew (Pseudoperonosporacubensis) biology, ecology, epidemiology, host-pathogeninteraction and controlAle Lebeda&Yigal CohenAccepted: 5 July 2010 /Published online: 25 July 2010#KNPV 2010 AbstractCucurbit downy mildew , caused by theoomycetePseudoperonospora cubensis , is a devastating,worldwide-distributed disease of Cucurbit crops in theopen field and under cover. This review providesrecent data on the taxonomy, biology, ecology, hostrange, geographic distribution and epidemiology ofP. cubensis . Special attention is given to host-pathogeninteractions betweenP. cubensisand its economically-important Cucurbit hosts (Cucumis sativus, C. melo,Cucurbita pepo, C. maxima,andCitrullus lanatus);pathogenic variability inP. cubensisat the species,genus, and population levels; and, differentiation ofpathotypes and races. Genetics and variability of hostresistance and cellular and molecular aspects of suchresistance are considered.

2 A focus is given to methodsof crop protection, including prevention and agro-technical aspects, breeding for resistance classicaland transgenic approaches, chemical control andfungicide resistance. Novel technologies in biologicaland integrated control are also discussed. This reviewalso summarizes the most important topics for futureresearch and international for of pest plantsIntroductionPseudoperonospora cubensis (causal agent of cucurbitdowny mildew ) is one of the most economicallyimportant and widespread plant pathogens. It is abiotrophic plant parasite belonging to the kingdomChromista, class Peronosporomycetes (Thomas1996;Dick2001a; G ker et ; Voglmayr2008).Although it has been studied by mycologists and plantpathologists for more than 100 years, there is still alack of information about this pathogen in manyspecific areas (Lebeda1990,1999;LebedaandSchwinn1994).

3 Together withBremia lactucae(Lebedaet ,2008a,b; Michelmore and Wong2008)andHyaloperonospora parasitica(Slusarenko and Schlaich2003; Holub2008) it is one of the most studiedPeronosporomycete biotrophic parasites of plants. TheEur J Plant Pathol (2011) 129:157 192 DOI Lebeda (*)Department of Botany, Faculty of Science,Palack University in Olomouc, lechtitel 11,CZ-783 71 Olomouc, Czech Republice-mail: CohenBar Ilan University, Faculty of Life Sciences,52100 Ramat Gan, Israele-mail: comprehensive and internationally-available reviewson this pathogen were published thirty years ago (Paltiand Cohen1980;Cohen1981). In the present review wediscuss a wide range of specific issues related the biology, diversity, ecology,distribution, host range, epidemiology, host-pathogeninteractions, genetics of resistance, breeding and cubensisis used as a case study to demonstrate thediverse, complex interactions of downy mildews withtheir host of this review were published before inCzech (Lebeda1990; Lebeda et ;Lebedaand Urban2005).

4 The current review was broadenedand supplemented with the literature published in thelast twenty years. This literature mainly considers thetopics of variability of host-pathogen interactions,variation of pathogenicity, resistance of host plants,breeding for resistance and pathogen control, focusingmainly on efficacy of and resistance to fungicides. Theaims of this paper are to summarize the currentinformation onP. cubensis , critically discuss the areasin which we still lack basic data, and introduce theminto the wider context of biotrophic parasitism withinthe downy of nomenclaturePseudoperonospora cubensis (Berk. et Curt.) first described by Berkeley in 1868 in herbariumplant material originated from Cuba, and hence itsspecies namecubensis(Skalick 1961). It was alsoidentified as a new genus,PseudoperonosporaBerkeley,together with the description of the speciesPseudoper-onospora cubensis , therefore, served as thetype species of thePseudoperonosporagenus (Dick2001b,2002b).

5 The pathogen was first observed anddescribed on live plants by Rostovzev in TheBotanical Gardens of Moscow (Russia) in 1903(Skalick 1961).During the last century some misleading syno-nyms were used to describeP. cubensis ,suchasPeronospora cubensisBerk. et Curt.,PeronosporacubensisBerk. et Curt. ,Plas-mopara cubensis (Berk. et Curt.) Humphrey, andPeronoplasmopara cubensis (Berk. et Curt.) Clinton(Dick2001b).Recent systematic classificationAccording to recent taxonomic classification,Pseudo-peronospora cubensisbelongs to kingdom Chromista,subdivision Peronosporomycotina, class Peronosporo-mycetes (originally described as Oomycetes), orderPeronosporales ( downy mildews), family Peronospor-aceae (G ker et ; Voglmayr2008). Peronospor-omycetes is comprised of ca 900 (perhaps up to 1500)species, 75 genera and 19 families (Dick2001a,c), andnew genera were recently described (G ker et ;Voglmayr2008).

6 The genusPseudoperonosporabelongs to a taxo-nomic group on the border between genera thatregularly produce zoospores (Pythiumspp.) andgenera that never produce zoospores (Peronosporaspp.,Albugospp.) (G ker et ).P. cubensisdoes produce zoospores but its sporophores resemblethose ofPeronosporaspp. It is a species with highlydistinct host specificity attacking above-ground parts,mainly leaves, of only the Cucurbitaceae. Theformation of zoospores in this species depends onenvironmental conditions. It occurs in water only andis inhibited at high temperatures. The whole zoospo-rangium content is cleaved and biflagellate zoospores,10 13 m in diameter, are released (Thomas1996).However, there are also reports on direct germinationby germ tubes (Lange et ,c). Sporangia easilydislodge from the sporangiophore and are distributedby air or rain splash (similar to otherPseudoperono-sporaspp.)

7 (Lange et ).Pseudoperonosporaspp. has dichotomously-branched sporangiophoreswith terminal growth; the sporangia of similar age arepresent at the ends of sterigma (Choi et ;Voglmayr2003). The family Peronosporaceae includesat least 17 genera (G ker et ; Voglmayr2008).Probably the most widespread genera in Europe andNorth America areBremia, Peronospora, Hyaloper-onosporaandPlasmoparaof which representativescause serious diseases of cultivated plants (Lebeda andSchwinn1994; Voglmayr2008). The individual generaare mainly characterized by the shape and branching ofthe sporophore/sporangiophores and the ability todischarge zoospores. From this point of view,Pseudo-peronosporarepresents a transitional type betweenPlasmoparaandPeronospora(Dick2001 b,2002a,b;Voglmayr2003; ; G ker et ).According to Riethm ller et al. (2002) the genusPseudoperonosporais monophyletic, however, it has158 Eur J Plant Pathol (2011) 129:157 192close relationship withPeronospora, as they sharesimilar haustoria, conidiosporangiophore morphology,and conidiosporangium colour.

8 Recently, several haus-torial types ( clavate-branched, ellipsoid-pyriform,hyphal) were recognized for downy mildews, includingPseudoperonospora(clavate-branc hed), which are con-sidered an important diagnostic feature (Voglmayr et ).Based on the variability of the genome size, Voglmayrand Greilhuber (1998) stated that the phylogeneticposition, and the definition of individual genera, hasnot yet been clearly resolved. Recent molecular-phylogenetic studies done with Peronosporales andPeronosporaceae (G ker et ,2007; Riethm lleret ;Voglmayr2008) demonstrated that thegenusPseudoperonosporais a unique monophyleticgroup. This supported the previous opinion of taxono-mists (Constantinescu2000; Waterhouse and Brothers1981), and disagreed with Skalick s(1966) concept onthe division of the genus. Based on sporangialultrastructure and the phenetic characters shared by thespecies of the genus, Constantinescu (2000) suggestedthat a distinct genus forPseudoperonosporais justified(Riethm ller et ).

9 Indeed, comparative morpho-logical and molecular (ITS rDNA) studies ofP. cubensisandP. humulishowed that the genusPseudoperono-sporais a distinct taxonomical unit. However, recentstudies also demonstrated that both species are verysimilar (Choi et ; ; ), andP. humuliwas suggested as a synonym (Choi et ). Previous (Choi et )and recent (Sarris et ) studies of ITS rDNAshowed only a limited intraspecific variability Nevertheless, the limited ITS rDNA intraspe-cific variability stands in contrast with the very broadpathogenic variability ofP. cubensis (Lebeda andWidrlechner2003; ). Recently, themitochondrial cytochrome oxidase (COX) gene cluster,and two nuclear loci, ITS, NADH gene regions and -tubulin, were sequenced. Conserved single nucleotidepolymorphisms (SNPs) were found that consistentlydifferentiateP. cubensisandP. humuli(Mitchell et ). Host range and pathogenicity studies demon-strated that these species have distinct pathogeniccapabilities (Gent et ),P.

10 Cubensismay infecthop, but caused very little disease, whereasP. humulinever infected cucurbits (Mitchell et ). Currentstudies are focused on identifying a suite of effectorproteins fromP. cubensis , and characterizing thembased onin plantalocalization, putative function, andin part, contribution to overall pathogen virulence (Dayand Hausbeck2009).All these results unambiguously showed that adetailed understanding of inter and intraspecificvariability ofPseudoperonosporaspp. must be basedon more complex experimental approach ( Gentet ). From a purely phytopathological view-point, pathogenicity is a much more significanttaxonomic criterion as it enables specification ofintraspecific pathogenic variants (pathotypes andraces) ofP. cubensis (Lebeda et ).BiologySymptoms of infectionP. cubensisis a leaf pathogen, attacking exclusivelythe leaves of cucurbitaceous plants (Cohen1981;Thomas1996).