Articlebibliographique *

MECHANISMS CONFERRING PLANT INCOMPATIBILITY TO (*) David T. KAPLAN*and Noel T. KEEN Departments of Nematology and Plant Pathology, University of California, Riverside, Ca 92521, USA.

1

SUMMARY Incompatibility (resistance) of plants to parasites is conferred by repulsive chemicals in a few cases but rarely, if at all, by penetration barriers or nutritional deficiencies in the host plant. The major incompatibility mechanism(s) appear(s) to be the post-infectional occurrence of (( hypersensitive r) reactions. Although the role O€ preformed simple phenols in this type of incompatibility is obscure, available information suggests that inducibly formed structural and chemical (viz. phytoalexins) barriers to nematode development maybe responsible. No firm conclusions may be made at presenton the validity of possible mechanisms sincc much of the earlywork is difficult to interpret and contains procedural inadequacies. Thus, appraisal of incompatibility mechanisms to nematodes requires additional testing of the hypotheses, especially as to the existence of such mechanisms at the localized site where and when incompatibility is expressed. An understanding of incompatibility may be attained more easily by utilizing those experimental approaches that have recently been used to study incompatibility systems to microbial parasites. Some of these are suggested which may be used in future nematode research.

RÉSUMÉ

Mécanismes conférant au2 plantes l’incompati biliti au2 nimatodes 1 Une revue de la littérature a démontré quela réaction d’incompatibilité (la résistance)des plantes aux nématodes est due, dans certains cas, à des substances répulsives pour le parasite mais pratiquement jamais à l’existence de barrikres s’opposant à sa pénétration ou au manque d’éléments nutritionnels dans la plante hôte. Le ou les méca- nisme(s) majeur(s) conduisant à l’incompatibilité semble(nt) donc êt‘re l’apparition de réactions d’ (( hypersensi- bilité O aprks l’infection. Bien que dans ce type de réaction d’incompatibilité le rôle des phénols préformés soit encore obscur, l’information dont on dispose permet de penser que la formation, après l’infection, de barrières de nature chimique (par exempleles phytoalexines) ou structurale pourrait être responsablede la réaction d’incompati- bilité. Cependant, à l’heure actuelle, on ne peut pas se prononcer en faveur d’un des mécanismes possibles car une expérimentation criticable rend une grande partie des travaux publiés difficile à interpréter. C’est pourquoi une étude plus fine est nécessaire avant qu’on puisse se prononcer sur la nature des mécanismes de la réaction d’incom- patibilité aux nématodes. Il faudra notamment chercher à savoir si les mécanismes proposés apparaissent en même temps que la réaction d’incompatibilité, d’une part, et s’ils sont localisés aux sites mêmes où la réaction d’incom- patibilité s’exprime, d’autre part. L’utilisation d’approches expérimentales variées, comme cela a été fait dans le cas des systkmes bactériens,viraux ou fongiques, devraitpermettre d’atteindre cet objectif. Nous proposons quelques-unes de ces approches expérimentales qui pourraient être utiles dans le cas des systkmes à nématodes.

(l) Portion of a thesis submitted by thesenior author in partial fulfillment of the requirements for the Ph. D. de- gree in Plant Pathology, University of California, Riverside. The authors’ research is supported by the National Science Foundation. * Presentaddress : USDA HorticulturalResearch Laboratory, 2120 Camden Rd,Orlando, FL 32803, USA.

Revue Nématol. 3 (1) :123-134 (1980) 123 D.T. Kaplan h N.T. Keen

Economics, availability,andgovernment riers posed by the plant.Since failure to perform regulations portend reduced future reliance on any of these would resultin incompatibility, chemical control of nematode-incitedplant it is notsurprising that examples of natural diseases. Greateremphasis will probably be plant disease defense are known for most of placed on alternative methods of disease control them. Also, natural incompatibility in a single and on the biology underlyingtheir effecti- plant may result from the multiplier effect of veness. Because genetic resistance is and proba- twoconsecutive mechanisms, neither of which hly will remain a prime contxol measure of need be absolutely effective against the patho- diseases caused by plant pathogenic nematodes, gen. Suchsequences have been suggested for a review is presented of research published in resistance to certainnon-pathogenic fungi by the last- few yearson the mechanisms which Heath(1974), but, no convincing evidence for limit nematode development and reproduction. them against nematodes exists. Those papers will be emphasizedwhich have appearedafter the last reviews on the topic (Cook, 1974; Dropkiri, 1976; Giebel, 1974; Attraction and repulsion Levin,1976; Rohde, 1972; Webster, 1975). Comparisons will also be madeto selected Both ecto- and endoparasitic nematodes share researchon mechanisms of incompatibility to a common environment during initial stages of bacterial and fungal plant pathogens .in order the life cycle, andmust successfully migrate to demonstrate similarities and differences and through therhizosphere to a root. Root exudates to suggestexperimental approaches for future may be important as attrac,tants or repellants, studies of nematode systems. and substantial evidence exists indicating that Because of itshistorical connotation with roots exude attractant substances (Green, 1971). yield and not necessarily pathogen devélopment, Certain plants mayalso be protected fromnema- the, termresistance will not be routinely used in tode infection by releasing repellantmaterials this review; instead incompatibility will be used into therhizosphere. Several plants (e.g., African to denote the unsuitability of a plant for (( nor- marigold, onion, garlic, asparagus, and pangola mal 1) pathogendevelopment relative tothat grass)have been suspected of reducing soil omurringin a compatible interaction, where populations of nematodesinthis manner. development and reproduction are considerable. Earlywork by Rohde and Jenkins (1958) Generalincompatibility is theability of al1 suggested that release of a glycoside with nema- members of a plant species toprevent repro- ticidalproperties into soil by asparagusroots duction of an entirenematode or microbe was responsible for resistance to 'Paratrichodorus species. Thus,the nemat,odeor microbe is a minor. Concentrations of the glycoside in lea- nonpathogen on the plant species inquestion, chates collected from pottedplants indicat.ed although it may be pathogenic on certain other that adequateconcentrations were present. in plant species. Specificincompatibility is that the rhizosphere to protect plants from infection exhibited by only certain cultivars or genotypes by the ectoparasite. The compound was nema- of a single plant species and is generally effective ticidal in zlitro and significantly reduced infection against only specific strains or races of a micro- of tomato by P. minor when applied as a soil organism or nematode spec,ies. In its mostrefined drench or foliar spray. The asparagus glycoside form, the specificity of both partners is deter- may therefore be a factorconferring disease mined by alleles at single geneticloci, viz. incompatibility since the availableevidence gene-for-gene systems (Days, 1974; Price, Cavi- demonstrates that. an effective concentration of ness & Riggs, 1978;Webster, 1975). Most of theactive compoundis released into rhizos- the nematology literaturehas been concerned phere. with specific (viz. cultivar)incompatibility to Intercropping of marigolds (Tagetes patula certainnematode species. L.) reduces nematode infection of other plants Regardless of the host-parasiteinteraction (Giebel, 1974;Hackney & Diclrerson, 1975; considered,compatibility is dependent on the Motsinger, Moody & Gay,1977; Rohde, 1972; pathogen'sability to develop and escape bar- Winoto,1969). Marigolds contain cr-terthienyls - . 124 Revue Nématol. 3 (1): 123-134 (1980) Mechanisms of plant incompatibility to nematodes

which have in vitro nematicidal activity (Uhlen- chemical (Schonbeck & Schlosser, 1976)bar- broek & Bijloo,1958, 1959). This has led to riers have been reported which prevent penetra- speculation concerning the possible protective tion of plant tissues by bacterialand fungal role of terthienyls in soil, but their presence in non-pathogens. Such barriers do not appear to the rhizospherehas not been demonstrated be effective againstplant-parasitic nematodes. (Hackney & Dickerson,1975). This and t,he The action of stylet penetration combined with fact that aqueous suspensions of terthienyls at enzyme release bynematodes (Chitwood & concentrationsup to 200 ppm appliecl asa ICrusberg, 1977;Deubert & Rohde,1971; soil drenc,h did not control Meloidogyne javanica Krusberg, 1960, 1964; Tracey, 1958) seem capa- (Daulton & Curtis, 1963) question the validity ble of overcoming mechanicalbarriers such as of a terthienyl protective mechanism. Toxicity plant ce11 walls or cuticles. For instance, equal of terthienyls may, in fact, be less than believed. infection of resistantand susceptible cultivars Gommers (1972),and Gommers and Geerligs has been reported for : Meloidogyneincognita (1974) have demonstrated that in oitro nemati- and Cotton (McClure, Ellis & Nigh, 1974a), or cidal activity of theterthienyls is greatly en- bushtype snap beans(Fassuliotis, Deakin & hanced by near ultraviolet light and therefore Hoffman, 1970), M. hapla and alfalfa,(Orion & theymay be relativelyinnocuous in soils. Cohn, 1975), Rotylenchulusreniformis and soy- Experimentalresults indicate that marigolds bean(Rebois, 1973) or Cotton (Carter,1974), function as trap crops(Hackney & Dickerson, schaclztii andradish (Muller, 1978), 1975), and they may reduce crop damage when M. incognita acrita and cucumbers (Fassuliotis, planted in rotation or as an intercrop; however, 1970) or lucerne (Reynolds, Carter & O'Bannon, the role of theterthienyls in this process is 1970), and Ditylenchusdispaci and pea (Muse, still unclear. 1969). Grifin and Waite (1971) observed signi- More convincing evidence for repulsiona ficant differences in penetratïon of resistant and mechanism of incompatibility comes from gene- susceptible alfalfa seedlings by Ditylenchus tic research with cucumbers. Haynes and Jones dipsaci at 200, but not at other temperatures. (1976) found that cucumber plantscarrying a Unlike M. incognita and D. dipsaci, M. lzapla dominant allele at theBi (bitter) locus attracted had a higher rate of infection in a susceptible significantly fewer Meloidogyne incognita lar,vae alfalfa cultivar regardless of temperature (Grif- to theroots than didthe near-isogenic bibi fin & Elgin, 1977). D. dipsaci infected but did (non-bitter)genotype. The Bi locus permits not reproduce in sweet clover,onion, tomato, plants to accumulatecurcurbitacins, toxic tri- sugarbeet, and (Griffin, 1975). From these terpenoids that are also important in resistance studies 'one concludes that nematodes freely to otherplant pests (Dacosta & Jones,1971). penetrate roots of hosts and nonhosts alike and The bibi genotype does not confer production that incompatibility at this stage may occurbut of the compounds. Whenplants of thetwo is rare. This is very similar to the interactionof cucumbergenotypes were exposed to high fungal pathogens with plant cultivars involved numbers of M. incognita in greenhouse tests, in gene-for-gene relationships in whichonly a plants having the Bi genotype attracted signi-' few examplesare known of cultivar or single ficantly less larvae than those with bibi; howe- gene resistance at the l'evel of penetration (e.g., ver,the root-hot indices anddetrimental Zimmer, Schaelling & Urie, 1968). efl'ects on plant growth were indistinguishable. Thus, although the Bi gene appears to reduce the number of nematodes attracted to cucumber Nutrition roots, it does not provide an effective barrier to those nematodes that do reach and penetrate Thenutrition hypothesis (Garber, 1956 ; them. Lewis, 1953) was devised to explain the incom- patibility of plants to certainpathogens. In Penetration itssimplest form, the hypothesis suggests that certain plants are incompatible to a patho- Preformed morphological (Royle,1976) and gen becausethey lack one or moreessential

Revue Ntmatol. 3 (1): 123-134 (1980) 125 D.T. Iiaplan & N.T. Keen nutrients.With few exceptions (cg., Strange, 1977; Reynolds,Carter & O'Bannon,1970). Smith & Majer, 1972), this idea has seldom been The actual mechanism(s) responsible .for move- supported by studies with microbial pathogens ment of larvae out of roots is unknown. Rather and has been disproven in most. Although the than being based on nutrition, it may reflect an idea has beenapplied to incompatibility to activehost response which createsconditions nematodes(Wallace, 1961), little or no direct adverse to nematodes within the root. evidence supports it. It has been hypothesized that nutrition may be important in sexual differentiation in certain Active 'incompatibility nematodes(Davide & Triantaphyllou, 1968) and this may reflect a mechanism of incompati- Many studieshave reported post-infection bility.For instance, increased development of changes in the chemical composition of plants non-feeding males which are not required for infected wit,h nematodes to which they are in- reproduction (parthenogenic nematodes), would compatible, but proof is generally lacking that clearly reduce nematode reproduction by redu- suchalterations are causally related tothe cing the total number of egg-laying females as expression of incompatibility. As 'is truewith well as minimize immediate damageto the plant. inc,ompatibility to many fungus parasites, limi- Orion (1973) found ' that chlorofluorenol, a ted colonization and development of nematodes growthinhibitor of the. morphactingroup, in incompatible plants is frequently associated inhibited giant ce11 formation in galls of tomato with the so-called hypersensitivereaction (HR). roots,retarded nematode development, and Classically, the HR has been considered to caused an increase in the percentage of, males. involve localized host ce11 necrosis and disor- Chlorofluorenol did not directly affect; nematode ganization as well as restricted pathogen deve- metabolism in vitio, but inhibited synchronous lopment at theinfection site. In thecase of plant division of nuclei withingiant cells, thereby pathogenic nematodes, the HR may cause im- apparently limiting nutrient availability. simi- A mobilization of the nematode and inhibition of lar effect on sexual differentiation and develop- nematode development (AI Tait, 1974; Kaplan, ment of nematodesoccurred when maleic" 1978; Orion & Cohn, 1975;Ramana & Rao, hydrazide, a plant growthinhibit.or, was applied 1977;Thomason, Rich & O'Melia, 1976;Van ta the foliage of and tomato seedlings Gundy & Kirkpatrick,1964). Although hyper- infected by M. javanica and M. incognita sensitivity is not completely understood, evi- (Davide & Triantaphyllou, 1968). Translocation dence fromseveral fungus-plantstudies indi- of maleic hydrazide from foliage to roots pre- cates that necrosis or disorganization of host cells ventedestablishment of normalhost-parasite per SC! is not causally related to pathogen res- relationships by suppressing giantce11 formation. triction (Iiiraly, Barna & Ersek, 1972; Mayama, Involvement of nutrition in sexual differentia- et al., 1975;Sato & Tomiyama,1977; Tani ef tion has been further substantiated in studies al., 1975), but may be a usual consequence of involving M. incognita (Trudgill,1972) and the inc.ompatible response. Meloidoderafloridensis (Triantaphyllou & Hirs- In hypersensitivereactions to fungi,plant chmann,1973), in which nematodes were cells appear to specifically recognize the patho- plzysically removed from their nutritional source. gen very earlyafter initial contact(Keen & Thus, the datasuggests that altered sex expres- Bruegger, 1977) andthis initiates a series of sion attributedto changes inhost nutrient events including de novo DNA transcription and levels may be > mechanism of incompatibility protein biosynthesis, finally producing chemical to certain nematodes. (viz. phytoalexins) or physical (e.g., induced Migration of larvae from roots shortly after lignification or suberization) barriers. If recog- infection may be nutritionally related. Larvaeof nition for incompatibility does not oc,c.ur, Pralylenchus scribneri migrated out of roots of however, the plant will be compatible. Incompa- limabean (Rich,1976), and M. hapla and tibility isan active process andcompatibility M.. incognitaacrita were noted to leave roots a passive failure of the plant torespond defensi- of incomp_atiblealfalfa cultivars (Griffin .& Elgin, vely.- -- This is not to argue~. against t.he.. well

126 Reuue Nématol. 3 (1) : 123-134 (1980) Mechan isrns of plant incompatibility to nematodes

known occurrence of metabolic and anatomical rance of vacuolar inclusions throughoutthe changes in plantsinfected by compatible obligate affected cell. Membrane-bound organelles such parasites such as sedentary endoparasitic nema- as nlitochondria and the Golgi apparatus disap- todes. However, it is now well establishedon peared.However, the endoplasmic reticulum genetic and biochemical grounds that specific increased in length and was observed as long- recognition generally occurs only to the incom- branched chains extending throughoutthe dense patiblepathogen, and that c,ompat.ibility is a cytoplasm. These observationssuggest that passivefailure of thehost to recognize the changes in the host ce11 may result from lyso- pathogen and'respond (Keen & Bruegger, 1977). some disruptionand/or synthesis of proteins Consistent with gene-for-gene systems invol- (enzymes) which affectdisorganization of the ving obligate fungal parasites (Ellingboe,' 1972; cell. Tbey reinforce the conclusion that the HR Keen & Littlefield, 1979), theHR tonematodes is a specific plant response to the pathogen, but may be invoked at different times following the aswith al1 microscopy studies to date,they initiation of a feeding siteby sedentarya offer little insight into biochemical mechanisms. parasiticnematode. Inthe case of sedentary Rohde(1972) previously summarized the endoparasites such as species of ' Meloidogyne, possible role of preformed simple phenols in the HR may be invoked relatively early (e.g., the incompatible host-parasite interaction. Phe- Paulson & Webster, 1972; Van Gundy & Kirk- no1 accumulationand products of phenolic Patrick, 1964) before appreciable giant ce11 or oxidationhave been associated with cellular syncytiumformation occurs, or later, after browning ina variety of plants infected by giant cell/syncytium formationhas already several plant-parasitic nematode genera (Chang, progressedconsiderably (Endo, 1965; Powell, 1969; Giebel, 1970; Giebel, Krenz & Wilski, 1962;Cotten & Hayes,1969). Perhaps the 1970;Hung &: Rhode, 1973). While phenols efficiency of host reco.gnition of the pathogen is appear to have limited toxicity, certain oxida- a variable character dependent on the host and tionproducts are moreactive. Quinones have nematode genotypes as in fungal systems (Keen been reported to be the most toxic forms and & Littlefield, 1979). also the most reactive (Chang, 1969 ; Farkas & Histopathologicalobservations of incompa- Kiraly,1962; Giebel, 1970;Hung & Rohde, tiblereactions to nematodeshave included 1973). changes in nuclear size andshape, density of The effect of phenolic compounds on nematode cytoplasm, thickness ofce11 walls, and safranin behavior and metabolism has also been studied. staining (Al Tait,1974; Carter, 1974; Dropkin Chlorogenic acid adversely affected nematode & Nelson, 1960; Hung & Rohde, 1973; Kaplan, coordination(Chang, 1969; Macaron, 1975). 1978; McClure, Ellis & Nigh,1974b; Muse, The effects of chlorogenic acid,oxidation pro- 1969; Rebois, Madden & Eldridge, 1975; Rohde, ducts of chloragenic acid,necrotic tissue, 'and 1972; Veech & Endo, 1970). Transmission elec- crude extracts from necrotic tissue, on migration tron microscopy has enabled us to take a closer and respiration of Pratylenclms penetrans have look at theseevents and, despite the limjted been studied in vitro (Chang, 1969). Chlorogenic number of studies published, some conclusions acid actedas an attractant, but its oxidation may be drawn. The HR to sedentary endopara- products possessed nematode repellant proper-

sitic nematodes is localized in host cells in the ties.Similarly, chlorogenic acid did not affect , vicinity of the nematode and appears to involve nematoderespiration, but oxidationproducts host ce11 lysis and disorganization. The progres- of the phenol caused significant reductionsin sion of ultrastructural changes involved in the oxygen uptake. Crude extracts of necrotic hypersensitiveresponse of tomato to Meloido- tissue also reduced respiration. Polymerization gyneirzcognita (Endo & Wergin, 1971; Paulson of oxidation products, however, destroyed their & Webster, 1972) has been carefully studied. activity(Rohde, 1972). The HR includedinitial increases in electron Although levels of preformedphenols in density and increased afinity for certain stains roots have also been positively correlated with by the cytoplasm. Then, a loss of ce11 membrane resistance of certain plant cultivarsto nematodes distinctness was accompanied by the disappea- (Cohn, 1974;Ponin et al., 1977;Rohde, 1972;

Revue Nematol. 3 (1) :123-134 (1980) . 127 D.T. Kaplan Le- N.T. Keen

Sidhu & Webster,1973; Singh & Choudhury, This may be important because ,agents such as 1974; Szczygiel & Giebel, 1970),their signifi- ethylene,which stimulate cyanide insensitive cance inincompatibility is not yet clear. The respiration, also increased thecapacity for correlation of phenols with nematode incompa- phytoalexinproduction in potatoes (Henfling, tibility is not always correct (Feldman & Hanlcs Lister & Kuc, 1978) and sweet potatoes (Haard, 1971; Brueslce & Droplcin, 1973),and critical 1977), providing that the tissues were exposed comparisons of phenol levels in near-isogenic to a suitable elicitor. compatible and incompatible host lines have not Post-infectionalproduction of phytoalexins been made. Thus, no convincing evidence exists has often been associated with the hypersensi- indicating the involvementof simple, preformed tive response and isgenerally regarded as an phenolic compounds or their oxidation products important defense mechanismagainst certain in incompatibility of plants to fungi, bacteria, fungalpathogens (Iieen & Bruegger, 1977)- or nematodes.The majority of experiments Some efforts have been madeto determine if studying the relationship of host phenol compo- phytoalexins are,also associated with incompa- sition to nematode incompatibility have consi- tibility ta nematodes (Kaplan, 1978;Rich, Keen dered such &anges long after the expression of & Thomason, 1977; Veech, 1978b). Pralylenchzzs incompatibilityhas occurred. Proof of phenol scribneri elicitshypersensitivea reaction in involvementrequires demonstration that ade- roots of lima bean (Phaseolus lunatus), but not ' quate concentrations of theactive compound(s) inthose of snapbean (Phaseolusvulgaris) arepresent in the immediate vicinity of the (Thomason, Tich & O'Melia, 1976). Rich, Iieen' parasite at thetime incompatibility is expressed. andThomason (1977) showed that coumestrol Giebel (1974) regardedsimple phenols as and psoralidin accumulated in lima bean roots modifiers of IAA oxidase activity in a holistic beginning one dayafter inoculation, concomi- hypothesis of incompatibility based onbiochem- tant with the first appearance of hypersensitive icalstudies of theinteraction of Globodera symptoms ; neither hypersensitive lesions nor rostochiensis andpotato (Solanumtuberosum). significant accumulation of the two conlpounds It was hypothesized that hormone levels predi- occurred in the compatible, inoculated P. vul- cate compatible or incompatible reactions and garis roots.Incubation of P. scribneri in low that hydroxyproline rich glycoprot,eins and ce11 concentrations of coumestrol (10-15 pg/ml) for Wall lignification areimportant events in 48 hours in vitro reducednematode motility incompatibility (Giebel & Iirenz, 1975 ; Giebel by 50 %. However, motility of M. javanica, a & Stobiecka, 1974): We consider the hypo- compatiblenematode on lima bean, was not thesisunproven because there is aconceptual affected by this compound at concentrations of problem in the design of several of the experi- 25 pglml. Thissuggested that coumestroland ments presented inits support. The delicate psoralidin represent phytoalexins that may be timing and nature of the host-parasite interac- importantin the hypersensitiveresistance of tions were not carefully c,onsidered, and chemi- lima bean roots to P. scribneri. cal analyses of infected tissues were conducted Veech (1977, 1978b), and Veech and McClure long after incompatibility was expressed (Giebel, (1977) observed that the expression of incompa- 1970,1974; Giebel, Iirenz & Wilski,1970). tibilityin Cotton (Gossypiumhirsutum) to Consequently, it is difficult to differentiate Meloidogyne incognita was positively correlated between changes in the hostwhich were respon- with post-infectional increases in the concentra- sible for 1imiting.parasite development and those tion of methoxy-substituted terpenoid aldehydes which may have occurred secondarily. Theterpenoid aldehydes accumulated atthe Zacheo et al. (1977) also notedincreased 'nematode infectionsite (Veech, 1979),and hydroxyproline-rich protein content in tomato crude extracts of the terpenoid aldehydes were mitochondria after incompatibility to Meloido- toxic to M. incognita in vitro (Veech, 1978~). gyne incognita was expressed. They interpreted The available evidence is thus consistent with their data to indicate that cyanide insensitive the idea that the compounds may account for respiration may be an important feature of the restricted nematode development. hypersensitive defense reaction-. to nematodes. -. - We recently studied the interactions of two . -- . - - .. 128 Revue Nérnatol. 3 (1) : 123-134 (1980) Mechanisnw of plant incornpatibility to nematocles cultivars with two species of root-knot innematode-plant systems. Normal incompa- nematodes to further test the hypothesis that tiblereactions may be completely blocked by incompatibilitymay be dependentupon phy- DNA transcription inhibitors or mRNA trans- toalexinaccumulation. The soybean phytoa- lation inhibitors (e:g., Vance & Sherwood, 1976) lexin glyceollin has been firmly associated with whenapplied shortlyafter or immecliately restriction of pathogendevelopment in the before inoculation. When inhibitors have little soybean-Phytophthora megasperma var. sojae or no effect on the pathogen at concentrations host-parasite system (Keen & Bruegger, 1977), used,normally incompatible plants will react and possibleinvolvement of the compoundin in a completely compatible manner. Pre-inocu- the nematode system was tested. The incompa- lation heat treatments also freyuently block the tible reaction of cv. Centennial to M. incognita normal expression of incompatibility to fungal was positively correlated with significant accu- parasites(Chamberlain, 1972; Dolce, Nakae & mulation of glyceollin (Kaplan & Keen,1977; Tomiyama,1976) and nematodes (Dropkin, Kaplan,1978), wllile the relatedcompatible 1969;Irizarry, Jenlcins & Childers, 1971; cultivarPickett 71 accumulatedlittle. The Paulson & Webster, 1972). Actinomycin D and highest concentration of phytoalexin was found blasticidin S have been used(Yoshikawa, in the stele of incompatible roots, the primary Yamauchi & Masago, 1978a, b) to delnonstrat,e site of the incompatibleresponse as deduced that reversa1 of normal incompatibility expres- by microscopic studies (Kaplan, 1978). Glyceol- sion insoybeans to Phylopl~fhora nzegasperrna lin accurnulated in this tissue when cytoplasm var. sojae also blockecl glyceollin production. in host cells in the immediatevicinity of the The experiments clearly supported a causal role nematode turned brown. Bot11 soybean cultivars for the phytoalexin in the expression of incom- were compatible to M. javanica;giant cells patibility. Using similar experimentswith the developed in the stele, and significant glyceollin oat-Puccinia coronafa var. auenae host-parasite accumulation did not occur in either. Glyceollin system,Tani ancl Yamamoto (1979) showed hada nematistatic effect on M. incogrzita in that blasticidin S also bloclced the incompati- vitro at low conc,entrations but did not affect bility of oat plants to the fungus. As in many M. javanica.These observations suggest but llost-parasite systems, incompatibility in oats to do notprove that accumulation of glyceollin Puccinia normally involved activationof pheny- may be responsible for the expression of incom- lalanine, ammonia lyase, peroxidase, and poly- patibility and that failure of the plant to ac- phenol oxidase. Suc11 increases in activity had cumulatethe phytoalexin may account for been thought tobe causally relatedto incompati- a compatible 'reaction. bility, not only to fungi, but also to nematodes. Inducedstructural barriers may also be in- However,when incompatibility wasreversed volved in the HRof certain plant rootsto nema- withblasticidin S, thesame' increases inthe todes (Al Tait, 1974; Giebel, Kranz ' & Wilski, three enzymes were observed(Tani & Yama- 1970; Rebois, Madden & Eldridge, 1975). Thus moto, 1979; Yamamoto et al., 1977; Yamamoto, far, however, no critical testing of the possible Hokin & Tani,1978). These experimentsthus causalrelationship of thesebarriers to incom- preclude activation of PAL, peroxidase,and p'atibility has beendone. Thus,these may be PPO as the directcause of incompatibility. wound Bealing responses that only occur after Similarapproaches may be usefulin testing the. expression of incompatibility. other suggestedincompatibility mechanisms. In addition totranslation and transcription inhibjtors, reversa1 experimentsmight involve Future considerations pre-inoculation heattreatments and cytolcinin application whic,h b1oc.k incompatibilityin Reversa1 experiments have been very useful certainplant-nematode interactions (Dropkin, to test critically the role of suggestedmecha- Helgeson & Upper,1969; Iiochba & Samish, nisms for the incompatibility of plants to certain 1971).Sawhney andWebster (1979)recently furigus pathogens and should be used to study usedcycloheximide to inhibitthe visible HR physiologically important defense mechanisms of incompatibletomato roots to Meloidogyne

Revue Nématol. 3 (1): 123-134 (1980) 129 D.T. Kaplan LE N.T. Keen

incognita. However, the nematodesstill failed the substantial number of such lines with and .to form galls or multiply,even thoughcyclohexi- without dominant resistance genes to microbial mide applied to genetically compatible tomat,o pathogens, we areunaware of near-isogenic plants did not interfere withgall formation. The nematoderesistant lines in which the desired reason for the failure of nematodes to multiply 7-15 back-crosses have been made.Without in the inhibitor-treated incompatible plants is suc,h lines, it is more dificult to critically test unknown.Perhaps c.yclohesimide blocked the the relevance of possible mechanisms of incom- visible HR,but not the c.hemica1 mechanism patibility. Consequently, it is hoped t-hat plant for nematode inhibition. breeders will incorporat>e severalof the available A difflculty in t>esting suggested mechanisms' single genes for nematode resistance into near- of incompatibility to pathogens is determining isogenic back-crossed lines. whether the mechanism occurs at the time and Arelated approach thathas not been well cellular locale where incompatibility is expressed. exploited in testing hypotheses of incompatibi- Althoughdetermination of theconcentration lity mechanisms is the use of virulentand of toxicants or amounts of structuralbarriers avirulentstrains (races) of thesame pathogen within incompatible infection sites as small as species on a single plant genotype. Since virulent those initiated by nematodes is dificult, recent andavirulent races or strainsexist in several progress with incompatible reactions to fungal plant-nematode systems (for review, see Webs- pathogens suggests approaches to the question. ter, 1975), they could be more widely used in Satoand Tomiyama (1977)made thin serial incompatibilityresearch. slices of petioles inoculated with incom- There is no informationon mechanisms of patible Phytophtlzorci infestans races and deter- incompatibility to ectoparasitic nematodes. Al- mined their levels of the phytoalexin rishitin. though these nematodes have wide host ranges, This allowed a relativelycritical assessment cultivars that reduce field populationsare of phytoalexin concentration soon after inocu- known(Cohn, 1974; Schmitt,1977). While lation. Localization of the broad bean phytoa- greaterdiffkulty is encountered in worliing lexins wyerone and wyerone acid were studied with these nematodes, several laboratories have inepidermal strips (Mansfield, Hargreaves & been successful. It would be of interestto Boyle, 1974) of leaves infected by the incompa- understand the mec.hanisms by which non-host tiblefungus Botrytis cinerea with fluorescence cultivarslimit ectoparasitic nematode repro- microscopy.Presence of the highly fluorescent duc,tion. phytoalexins was observed in host cells imme- Fromthis review it isobvious that more diately surrounding hypersensitive lesions soon effort is needed to elucidat>e changes inhost after inoculation. Since this was at or slightly metabolism which are essential to incompatible before thetime whenpathogen development responses. Such information might beused to was restricked, it supported a causal role for devise novel disease control mesures for thephytoalexins. Sherwood and Vance (1976) diseases in which classical methodsare inef- have performed similar experiments usinp phlo- fectiveor dificult to use. Whetherthis will roplucinol staining to demonstrate lignin deposi- materialize is unclear, but a certain prerequisite tionin inc,ompatibleinfection sites in reed is elucidation of the actual mechanisms confer- canary grassleaves. Application of techniques ringnatural incompatibility. such as these, especiallg fluorescence micros- copy withintact or freshly-sectioned roots infected withincompatible nematodes, might be useful in determiningwhether levels of phytoalexins or simple phenols were suficiently high at the infection sites to account for restric- ACKNOWLEDGMENTS tedpathogen development. Another impediment in researchon nematode- We thank J. G. Baldwin, 1. J. Thomason, and S. D. plantincompatibility mechanisms is the un- VanGundy for suggestions. M. LeGrand read the availability- of near-isogenic plant lines. Unlike~. manuscript and translated the summary.. .. -

130 Revue Nématol. 3 (1) : 123-134 (1980) Mechanism of plant incomnpatibility €0 nematodes

REFERENCES DROPKIN,V. H. (1969). The necrotic reactionof tomato and other hosts resistant to Meloidogyne : reversal AL TAIT,B. (1974). Light and electron microscopy of bytemperature. Phytopathology, 59 : 1632-1637. resistantand susceptible alfalfa roots infected by DROPKIN,V. H. (1976). Nematode parasites of plants, Meloidogyne hapla. Diss.Abstrs., 35B : 672. their ecology andthe process of infection. In : BERG&J. B., FARAUT,J. & RITTER,M. (1976). Modi- Heitefuss, R. & Williams, P. H. (Eds) Physiological fications d'activitésenzymatiques sous l'influence PlantPathology, Heidelberg,Springer-Verlag : del'infection de plantes par des nématodes. Ann. 222-246. Phytopathol., 8 : 1281130. DROPKIN,V. H., HELGESON,J. P. & UPPER,C. D. BRUESICE,C. H. & DRO'PKIN,V. H.(1973). Free (1969). Thehypersensitivity reaction of tomatoes phenols androot necrosisin Nematextomato resistantto Meloidogyneincognita : reversalby infected withthe root knot nematode. Phytopa- cytokinins. J. Nematol., 1 : 55-61. thology, 63 : 329-334. DROPKIN,V. H. & NELSON,P. E.(1960). The histo- CARTER, W. W. (1974). Histological responses of pathology of root-knotnematode infections in resistantand susceptible Gossypiumarboreum to . Phytopathology, 50 : 442-447. Rotylenchulusreniformis. J. Nematol., 6 : 138. ELLINGBOE,A. H. (1972). Genetics and physiology of CHAMBERLAIN,D. W. (1972); Heat-induced susccp- primaryinfection by Erysiphegraminis. Phyto- tibility to nonpathogens and cross-protection against pathology, 62 : 401-406. Phytophthoramegasperma var. sojae insoybean. ENDO,B. Y. (1965). Histological responses of resistant Phytopathology, 62 : 645-646. ' andsusceptible soybean varieties, and backcross CIIANG, L. M. (1969). The repellent effect of necrotic progenyto entry and development of Heterodera tissueon thenematode, Pratylenchuspenetrans glycines. Phytopathology, 55 : 375-381. (Cobb, 1917), Filipjev & SchuurmansStekhoven, ENDO,B. Y. & WERGIN,W. P. (1971). Fine-structural 1941. University of Massachusetts, M. S. Thesis. changesin red clover (Trifoliumpratense) roots CI-IITWOOD,D. J. & KRUSBERG,L. R.(1977). Pecto- duringpenetration by the root-knot nematode, lytic enzymes inthree populations of Ditylenchus Meloidogyne incognita. J. Nematol., 3 : 309 (Abstr.). dipsaci. J. Nematol., 9 : 187-192. FARICAS,G. L. & KIRALY,Z. (1962). Role of phenolic COHN, E.(1974). Relations between Xiphinema and compounds in the physiology of plant diseases and Longidorus and their host plants. In : Lamberti, F., disease resistance. Phytopath. Z., 44 : 105-150. Taylor, C. E.Seinhorst, J. W. (Eds) Nernatode FASSULIOTIS,G. (1970). Resistance of Cucumis spp. Vectors of Plant Viruses, New York, Plenum Press : tothe root-knot nematode, Meloidogyneincognita 365-386. acrita. J. Nematol., 2 : 174-177. COOK,R. (1974). Nature and inheritance of nematode FASSULIOTIS,G., DEAKIN,J. R. & HOFFMAN,J. C. resistance in cereals. J. Nematol., 6 : 155-174. (1970).Root-knot nematode resistance in snap COTTEN, J. & HAYES,J. D. (1969). Genetic resistance beans : breedingand nature of resistance. J. am. tothe cereal cystnematode (Heteroderaavenae). Soc.hort. Sci., 95 : 640-645. Heredity, 24 : 596-601. FELDMAN,A. W. & HANKS, R.W. (1971). Attempts to DA COSTA, C. P. & JONES,C. M. (1971). Cucumber increasetolerance of grapefruit seedlings tothe beetle resistance and mite susceptibility controlled burrowingnematode (Radopholussimilis) by bythe bitter gene in Cucumissativus L. Science, application of phenolics. Phytochemistry, 10 : 701- 172 : 1145-1146. 709. DAULTON, R.A. C. & CURTIS, R. F. (1963). The effects GARBER,E. D. (1956).A nutrition-inhibition hypo- of Tagetes spp. on Meloidogyne javanica in Southern thesis of pathogenicity. Am. Nat., 90 : 183-194. Rhodesia. Nematologica, 9 : 357-362. GIEBEL,J. (1970). Phenolic content in roots of some DAVIDE,R. G. & TRIANTAPHYLLOU,A. C. (1968). solanaccae and itsinfluence on IAA-oxidase activity 'Influence of the environment on development and asan indicator of resistanceto Heterodera rosto- sexdifferentiation of rootknot nematodes. III. chiensis.Nematologica, 16 : 22-32. Effect of foliar application of maleic hydrazide. GIEBEL,J. (1974). Biochemical mechanisms of plant Nemnatologica, 14 : 37-46. reistànce tonematodes : a review. J. Nematol., DAY, P. R. (1974). Genetics of host-parasite interaction. 6 : 175-184. San Francisco, Freeman Press, 238 p. GIEREL,J. & KRENZ,J. (1975).Role of aminoacids DEUBERT,K. H. & ROIIDE,R. A. (1971).Nematode in plant tissue response to Heterodera rostochiensis. enzymes. In : Zuckerman, B. M., Mai, W. F., & II. Effect of proline and hydroxyproline. Nematol. Rohde, R. A. (Eds) PlantParasitic Nematodes medit., 3 : 49-53. (Vol. II.), New York, Academic Press : 73-90. GIEBEL,J. & STOBIECICA,M. (1974). The role of amino DOICE,N., NAICAE, Y.& TOMIYAMA,K. (1976). Effect acidsin plant tissue response to Heterodera rosto- of blasticidin S on theproduction of rishitinin chiensis. 1. Proteinprolineandhydroxyproline potato tuber tissue infected by an incompatible race content in roots of susceptible and resistant sola- of Phytophthora infestons. Phytopath.Z., 87 : 337-344. naceous plants. Nematologica, 20 : 407-414.

Reuue Nématol. 3 (1) : 123-134 (1980) 131 D.T. Kaplan & N.T. Keen -:"~

GIEBEL,J., KRENZ,J. & WILSKI, A. (1970). The for- KAPLAN,D. T.(1978). Characterization of soybean mation of ligninlike substances in roots of resistant incompatibility t.o Meloidogyneincognita andits potat,oes underthe influence of Heterodera rosto- association to glyceollin accumulationin infected chiensis larvae. Nematologica, 16 : 601. root tissue. Ph. D. Dissert., Univ. California, River- GOMMERS, F. J. (1972). Increase of thenematicidal side, 115 p. activit.y of A-terthienyl and related compounds by KAPLAN,D. T. & KEEN, N. T. (1977). De novo syn- light,. Nemalologica, 18 : 458-462. thesis of an isoflavonoid compound by soybeans in response to infection. J. GOMMERS,F. J. & GEERLIGS,J. W. G. (1973). Lethal Meloidogyne incognita Ne- matol., 9 : 274. ' effect of nearultraviolet light on Prntylenchus penetrans fromroots of Tagetes.Nematologica, KEEN,N. T. & BRUEGGER,B. B. (1977). Phytoalexins 19 : 389-393. and chemicals that elicit. their production in plants. GREEN,C. D. (1971). Mating and host finding behavior In : Hedin, P. (Ed.) Host Plant Resistance to Pests, of plantnematodes. In : Zuckerman, B. M., Mai, AmericanChemical Societ,y Symposium, Series, : W. F., & Rohde,R. A. (Eds) PlantParasitic 62 1-26. Nematodes (Vol. II), New York, Academic Press : KEEN,N. T. & LITTLEFIELD,L. H. (1979). Thepossible 247-266. association of phytoalexinswith resistance gene GRIFFIN,G. D. (1975). Parasitisnl of nonhost cultivars expression in flax to Melampsora lini., Physiol. ,Pl. by Ditylenchus dipsaci. J. Nematol., 7 : 236-238. Pathol., 14 : 265-280. Z., & GRIFFIN,G. D. & ELGIN,J. H., JR. (1977). Penetra- KIRALY, BARNA,B. ERSEK,T. (1972). Hyper- tionand development of 1Vleloidogynehapla in sensitivity as a c.onsequence, not the cause, of plant resistantand susceptiblealfalfa under differing resistance t.o infect.ion. Nature, Lond. 239 : 456-458. temperatures. J. Nematol., 9 : 51-56. KOCHBA,J. & SAMISH, R.M. (1971). Effect of liinetin GRIFFIN,G. D. & WAITE, W.W. (1971). Attraction of and 1-naphthyl-acetic acid on root-hot nematodes Ditylenchusdipsaci and Meloidogynehapla by inresistant and susceptible peach rootstoclrs. resistant and susceptible alfalfa seedlings. J. Nema- J. amer. Soc. hort.Sei., 96 : 458-461. fol., 3 : 215-219. KRUSBERG,L. R.(1960). Hydrolytic and respiratory HAARD,N. F. (1977). Potentiation of wound induced enzymes of species of Ditylenchus and . formation of ipomeamarone by cyanide insensitive Ph,ytopathology, 50 : 9-22. respiration in sweet potato (Ipomoea bafatas). KRUSBERG,L. R. (1964). 1nvestigat.ions on Difylenchus Z. Pflanzenphysiol., 81 : 364-368. dipsaci polygalacturonase and its relat.ion t.0 para- sitism of thisnematode on-alfalfa (Medicago & O. HACKNEY, R. W.DICKERSON, J. (1975).Marigold, sativa).Nematologica, 10 : 72 (Abstr.). castorbean, and as controls of Meloidogyneincognita and Pratylenchus alleni. LEVIN,D. A. (1976). The chémical defenses of plants J. Nemafol., 7 : 84-90. to pathogensand herbivores. A. Rev. Ecol. Syst., 7 : 121-159. HAYNES, R.L. & JONES,C. M. (1976). Effects of the Bi locus incucumber on reproduction, attraction, LEWIS, R.W. (1953). An outline of the balance hypo- and response of the plant to infection by the sou- thesis of parasitism. Am. Naf., 37 : 273-281. thernroot-knot nematode. J. amer. Soc. hort. MACARON,J. (1975). Gtude de la résistance de deus Sei., 101 : 422-424. varietés de tomateaux Meloidogyne spp.et au HEATII,M. C. (1974).Light and electron microscope Phytophthoraparasitica. Nematol. medit., 3 : 35-41. studies of theinteractions O€ hostand non-host MANSFIELD, J. W., HARGREAVES,J. A. & BOYLE,F. C plantswith cowpea rust Uronzycesphaseoli var. (1974). Phytoalexin production bylive cells in broad uignae.'Physiol. Pl. Pathol., 4 : 403-414. bean leavesinfected with Botrytiscinerea. Nature HENFLING,J. W. D. M., LISTER,N. & Kuc, J. (1978). Lond., 252 : 316-317. Effect of ethylene on phytuberinand phytuberol MAYAMA, S., DALY,J. M., REHFELD,D. W. & DALY, accumulation in potatotuber slices. Phytopatho- C: R.(1975). Hypersensitive response of near- logy, 68 : 857-862. isogneic wheatcarrying the temperat,ure-sensitive HUNG,C. L. & ROHDE,R. A. (1973). Pbenol accumu- Sr6 allele for resistance to stem rust.. Physiol. lationrelated to resistance in tomato t,o infection Plant Pathol., 7 : 35-47. byroot-knot and lesion nematodes. J. Nematol., MCCLURE,M. A. ELLIS, K. C. & NIGH, E. Id.(1974a). 5 : 253-258. Resistance of cotaton to theroot-knot nematode, IRIZARRY,H., JENICINS,W. R. & CHILDERS, N. F. Meloidogyneincognita. J. Nemafol., 6 : 17-20. (1971). Interaction of soi1 temperature and Meloi- MCCLURE,M. A. ELLIS,K. C. & NIGH, E. L. (1974b). dogyne spp. on resistance of the comnlon bean, 'Post-infectiondevelopment and histopathology of Phaseolusvulgaris L., tothe root-knot disease. Meloidogyne incognita in resistant Cotton. J. Nema- .. .Nemafropjca, 1-:41-42: fol:, 6 : 21-26. -- _- . - .. 132 Reuue Nématol. 3 (1) : 123-134 (1980) Mechanisms of plant, incompati bilityto nemutodes

MOTSINGER,R. E., MOODY,E. H. & GAY,C. M. (1977). ROHDE,R. A. & JENICINS,W. R. (1958).Basis for Reaction of certainFrench marigold (Tagetes resistance of Asparagusofficinalis var. altilia L. , patula) cultivars to threeMeloidogyne spp. J. Nema- to thestubby root nematode Trichodoruschristiei fol., 9 : 278. (Allen1957). Univ.Maryland Agric. Expt. Sta. M~LLER,J. (1978). L’élevage monoxénique d’Hete- Bull., A-97 : 1-20. rodera schachtii sur cruciferes et son application pour ROYLE,D. J. (1976). Structural features of resistance la sélection des plantes résistantes. Revue Nématol., to plant diseases. In : Friend, J. & Threlfall, D. R. 1 : 47-52. (Eds) BiochernicalAspects of Plant-ParasiteRela- MUSE, B. D. (1969). Histopathology of susceptible and tionships, London, Academic Press : 161-193. resistant reactions in(I Wando )) pea seedlings to two SATO,N. & TOMIYAMA,IC. (1977).Relation between populations of Ditylenchusdipsaci. J. Nematol., inhibition of intracellularhyphal growth of Phy-

1 : 299 (Abstr.). toDhthora infestans andrishitin ~~ concentrations ~~ in ORION,D. (1973). Studieson plant root-knot nematode in’fected potko cells. Ann. phyto-path.Soc. Japan, interrelationships. OEPPIEPPO Bull., 9 : 67-71. 43 : 598-600. SAWHNEY, R.& WEBSTER,J. M. (1979):The influence ORION,D. &‘COHN, E. (1975). A resistant response of of some metabolicinhibitors on the response of citrus roots to the root-knot nematode,Meloidogyne susceptible,’resistant cultivars of tomatoto Meloi- javaniea. Marcellia, 38 : 327-328. dogyneincognita. Nematologica, 25 : 86-93. PAULSON,R. E. & WEBSTER,J. M. (1972).Ultras- SCHMITT,D. P. (1977). Suitabilityof soybean cultivars tructure of the hypersensitive reaction in roots of to Xiphinelnaamericanum and Macroposfhonia tomato, Lycopersiconesculentum L., toinfection ornata. J. Nematol., 9 : 284 (Abstr.). by the root-knot nematode, Meloidogyne incognita. Physiol.Pl. Pathol., 2 : 227-234. SCI-IONBECII,F. & SCIILOSSER,E. (1976).Preformed substances as potential protectants. In : Heitefuss, PONIN,1. Y., VOINILO,V. A., GLADRAYA,R. M. & R. & Williams, P. II.(Eds) PhysiologicalPlant TIMOFEEV,N. N. (1977). Nematode-resistant potato Pathology, Encyclopedia of Planf Physiology, Berlin, varieties and ways of using them. Pl. Breed. Abstr., Springer-Verlag : 653-678. 47 : 7545. SI-IERWOOD, R. T.S: VANCE,C. P. (19%). Histochem- POWELL,N. T. (1962). Histological basis of resistance istry of papillae formed in reed canarygrass leaves toroot-knot nematodes in flue-curedtobacco. in response tononinfecting pathogenic fungi. Phytopathology, 52 : 25 (Abstr.). Phytopathology, 66 : 503-510. PRICE,M., CAVINESS,C. E., & RIGGS,R. D. (1978). SIDHU,G. & WEBSTER,J. M. (1973). Genetic control Hybridization of races of Heteroderaglycines. of resistance in tornato. 1. Identification of genes for J. Xernatol., 10 : 114-118. hostresistance to Meloidogyneincognifa. Nema- RAMANA, K.V. & RAO,Y. S. (1977). Histopathogene- tologica, 19 : 546-550. sis inrice roots infested by Hoplolaimusindicus. SINGII,B. & CEIOUDIIURY,B. (1973). The chemical Indian J. Nematol., 5 : 232-234. characteristics of tomatocultivars resistant to REBOIS,R. V. (1973). Effect ofsoi1 temperature on root-knotnematodes (Meloidogyne spp.). Nema- infectivity and development of ‘Rotylenchulus reni- tologica, 19 : 443-448. formis on resistantand susceptible soybeans, STRANGE,R. N., SMITH,H. & MAJER, J. R.(197-i). Glycine rnax. J. Nernatol., 5 : 10-13. Choline, one of twofungal growth stimulants in REBOIS,R. V., MADDEN, P. A. & ELDRIDGE,B. J. anthers responsiblefor the susceptibility of wheat (1975). Some ultra-structural changes inducedin to Fusariumgraminearum. Nature, Lond., 238 : resistantand susceptible soybeanroots following 103-104. infection by Rotylenchulusreniformis. J. Nematol., SZCZYGIEL,A. & GIEBEL,J. (1970). Phenols in the leaf 7 : 122-139. buds of two strawberry varieties resistant and sus- REYNOLDS,H. W., CARTER, W. W. & O’BANNON,J. H. ceptibleto Aphelenchoidesfragariae. Proc. Int. (1970). Symptomless resistance of alfalfa to Meloi- Nematol.Symposium, Warsaw : 247-253. dogyneincognita acrita. J. Nematol., 2 : 131-134. TANI,T., & YAMAMOTO,H. RNAand protein syn- RICI-I, J. R. (1976). Association of coumestanswith thesesand enzyme changes during infection. In : the resistance of lima bean (Phaseoluslunatus) to Daly, J. M. (Ed.) Recognitionand Specificity in Pratylenchus scribneri and some other host-parasite Host-Parasite Interactions (In press). relations of thisnematode. Ph. D. Dissert.,Univ. TANI,T., YAMAMOTO, H., ONOE,k T. NAITO, N. (1975). , California,Riverside, 72 p. Initiation of resistanceand host ceIl collapse in RICH, J. R., KEEN, N. T. & THOMASON,1. J. (1977). thehypersensitive reaction of oat leaves against Association of coumestans with the hypersensitivity Pucciniacoronata avenue. Physiol. Pl. Pathol . of lima bean roots toPratylenchus scribneri. Plzysiol. 7 : 231-242. Pl. 10 : 105-116. Pathol., THOMASON,1. J., RICH,J. R. & O’MELIA,F. O. (1976), ROIIDE, R. A. (1972).Expression of resistancein Pathologyand histopathology of Pratylenchus plantsto nematodes. A. Reu.Phytopath., 10 : scribneri infection of snapbean and lima bean. 233-252. J. Nematol., 8 : 347-352.

Revue Nimatol. 3 (1) :123-134 (1980) 133 D.T. Kaplan & N.T. Keen

TRACEY,M. V. (1958). Cellulase and chitinase in plant VEECH,J. A. & MCCLURE, M. A. (1977). Terpenoid nematodes. Nematologica, 3 : 179-183. aldehydes in Cotton roots susceptible and resistant TRIANTAPHYLLOU,A. C. & HIRSCNMANN,H. (1973). to the root-knot nematode, Meloidogyneincognita. Environmentally controlled sex expression in Me- J. Nematol., 9 : 225-229. loidodera floridensis. J. Nematol., 5 : 181-185. WALLACE,H. R. (1961). The nature of resistancein TRUDGILL,D. L. (1972). Influence of feeding duration chrysanthemumvarieties to Aphelenchoides rit- on moulting and ses determination of Meloidogyne zemabosi.Nematologica, 6 : 49-58. incognita.Nematologica, 18 : 476-481. WEBSTER,J. M. (1975). Aspects of the host-parasite UHLENBRECK,5. H. & 'BIJLOO,J. D. (1958). Inves- relationship of plant-parasiticnematodes. In : tigations on nematicides. 1. Isolation and structure Dawes, B. (Ed.) Advances in Parasitology (Vol. 13), of nematicidala principle occurring in Tagetes London and New York, Academic Press : 225-250. roots. Rec.Trav. Chim. Pays-Bas Belg., 77 : 1004- WINOTO, R.S. (1969). Studies on the effect of Tagetes 1009. speeies on plant parasiticnematodes. Wageningen. UHLENBRECK,J. H. & BIJLOO, J. D. (1959). Inves- Veenman & Zonen, 134 p. tigations on nematicides. II. Structure of a second nematicidalprinciple isolated from Tagetes roots. YAMAMOTO,H., HOKIN, H. & TANI,T. (1978). Pero- Rec.Trav. Chim. Pays-Bas Belg., 78 : 382-390. xidaseand polyphenoloxidase inrelation to the crown rust resistance of oat leaves. Phytopath., Z., VANCE,C. P. & SIIERWOOD,R. T. (1976). Cyclohc- 91 : 193-202. ximidetreatments implicate papilla formationin resistance of reed canarygrassto fungi. Phyto- YAMAMOTO,H., HOKIN, H., TANI, T. & &DOTA, G. pathology, 66 : 498-502. (1977). Phenylalanine ammonia-lyase in relation to VAN GUNDY,S. D. & KIRKPATRICK,J. D. (1964). the crown rust resistance of oat leaves. Phytopathol. Nature of resistance in certain citrus rootstocks to Z., 90 : 203-211. citrusnematode. Phytopathology, 54 : 419-427. YOSHIKAWA,M., YAMAUCHI,K. & MASAGO,W. (1978~). VEECII, J. A. (1977).The relationship between ter- De novo messenger RNA and protein synthesis are penoid aldehydesand the resistance of Cotton to required for phytoalexin-mediated disease resistance Meloidogyneincognita. J. Nematol., 9 : 287-288 in soybean hypocotyls. Plant Physiol., 61 : 314-317. (Abstr.). YOSHIKAWA,M., YAMAUCHI,K. & MASAGO, H. (1978b). VEECH,J. A. (1978~). The tosicityof terpenoid alde- Glyccollin : its role in restricting fungal growth in hydes to nematodes. ,J. Nematol., 10 : 301 (Abstr.). resistant soybean hypocotyls infected with Phyto- VEECH, J. A. (1978b). An apparentrelationship phthoramegasperma var. sojae.Physiol. Plant between methoxy-substitutedterpenoid aldehydes Pafhol., 12 : 73-82. andthe resistance of Cotton to Meloidogyneinco- ZACHEO, G., LANIBERTI,F.,. ARRIGONI-LISO,R. & gnita.Nematologica, 24 : 81-87. ARRIGANI,O. (1977). Mitochondrial protein-hydro- VEECII,J. A. (1979). Histochemicallocalization and xyprolinecontent of susceptible andresistant nematotoxicity of terpenoidaldehydes in Cotton. tomatoes infected by Meloidogyne incognita. Nema- J. Nematol., 11 : 240-246. tologica, 23 : 471-476. VEECH,J. A. & ENDO,B. Y. (1970).Comparative ZIMMER, D. E., SCHAELLING,P. & URIE,A. L. (1968). morphology andenzyme histochemistry in root Thenature and inherit,ance of secdling rust resis- knotresistant and susceptible soybeans. Phyto- tance of Nebraska 1-1-5 safflower. Phyfopafhology, pathology, 60 : 896-902. 58 : 1451-1456.

Accepti pour publication le 16 août 1979.

134 Rcvzze Nénzatol. 3 (1) : 123-124 (1980)