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FORUM Hypersen~itivity: A Neglected Plant Resistance Mechanism Against Insect Herbivores c. WILSON FERNAKDESI Department of Biological Sciences. Northern Arizona University Flagstaff. Arizona 86011 EnV1ron. Entomol. 19(5)- 1173-1182 (1990) ABSTR.-\cr Despite many examples of plants. hypersensitive reaction against pathogens, there are exceedingly few examples of hypersensitive reactions having any importance against insect nerbivores. However. such plant defense mechanisms may be widespread among more sedenwy insect herbivores. The examples in which a hypersensitive reaction was elicited agains: insect herbivores were against galling insects. bark beetles. adelgids. and siricids. The intimate and sessile interactions during insects. egg and larval stages may have selected more specilic and more complex d~fcnses. because of the greater and more varied opportunities that t!:-e host plant has for regulating the lives of its intimate associates. Thus. it is argued that t:r.e intimate association of these herbivores during egg and larval stages set the scenario for t~ evolution of this plant defense mechanism. The dearth of accepted examples of hypersensitive reaction against insect herbivores may not reflect its actual frequency and occurrence in nature. Further investigation on plants. hvpersensitive reaction against insect herbl'ores may shed light on the ecology and evolution of insect-host plant associations. KEY WORDS lnsecta, hypersensitive reaction. induced defense. insect herbivory The hypersensitive reaction encompasses alI morphological and histological changes that. when produced by an injurious agent. elicit the prema- ture dying. or necrosis. of the infected tissue. as well as inactivation and localization of the infec- tiousagent (Mfil1er 1959. Maclean et al. 1974. Agri~ 1988). After reaching the plant.s surface. the path- ogen must penetrate into the plant .s cells. After penetration. a suitable nutritional site must be found to guarantee successful establishment. In some ca25. establishment may fail because of the rapid death of the host.s tissues at the site of infection. It is not the invaded cells. but the adjoining cells that die (White & Baker 1954. Hirata 1956). There is a positive correlation between the speed of reaction and the degree of host resistance to microorganisms (White & Baker 1954. Cóffey & Wilson 1983. Da- vidse et al. 1986). Hypersensitivity is usually con- trolled by an individual gene or. more rarely. by a few genes. Flor (1955) showed that hypersensi- tivity to fungi is determined by two specific genes. one in the host and the other in the pathogen. For further explanation of the gene-for-gene relation- ship. see reviews by Flor (1971) and Barrett (1985). Hypersensitive reaction is the primary event in resistance to fungal parasites (Maclean et al. 1974. Agrios 1988). This reaction by the host leads to a disruption of nutrient supplies to the invading mi- croorganism (Wong & Berryman 1977) and the production of many toxic metabolites. such as phy- toalexins (Bavlev & Mansfield 1982. Smith & Banks- 1986) resultiitg in the cessation of microorganism - STUDIES OF PLA-'l RESlSTANCE to insects have been centered on a wiàe spectrum of plant features, such as secondary com!X>UDds (Rosenthal & Janzen 1979, Green & Hedin 1986), nutritional factors (Rodri- guez 19i2, Wbite 1984), phenology (Feeny 1976, Faeth et al. 1981i. age (Morgan et al. 1983, Kear- sley & Whitham 1989). induced defense (Green & Ryan 19i2. Rhoaàes 1979, Haukioja 1982. Baldwin 1988 ). abscission : Kahn & CorneII1983, F ernandes & Whitham 1989), plant morphological traits (pu- bescence [Levin 1973. Pillemer & Tingey 1976, Woodman & Fernandes in press], tissue hardness [Coley 1983], coior [Tingey 1981], shape [Rausher 19i81 size [Kogan 19i51 and presence or absence of nectar-secreting glands [Wilson & Lee 1971J). Verv few studies :nave. however, addressed the im- portance of a particular type of induced defense, i.e., plant hyper!eDsitivity, as a source of plant re- sistance to inseCt herbivore attack. Plant hypersemitivity is a term primarily used by plant pathologists to describe a response to in- fection by pathogens as well as to many nonpath- ogenic stimuli :e.g.. Matta 1971, Misaghi 1982). Since the beginmng of this century. hypersensitiv- ity has been recognized as an important defense mechanism used by plants against pathogens (e.g., Ward 1902. Stakman 1915). I Current addr~ ~ento de Biologia Geral. C.P. 2486. ICB/Univenidade Federal de Minas Gerais. 30161 Belo Hori- zonte. ~1G-BraziL 0046-225X/90/1173-1182S02.00/0 (C) 1990 Entomological Societv of A~ca

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Page 1: Hypersen~itivity: A Neglected Plant Resistance Mechanism ...labs.icb.ufmg.br/leeb/publicacoes/1990.Fernandes.pdf · ABSTR.-\cr Despite many examples of plants. hypersensitive reaction

FORUM

Hypersen~itivity: A Neglected Plant ResistanceMechanism Against Insect Herbivores

c. WILSON FERNAKDESI

Department of Biological Sciences. Northern Arizona UniversityFlagstaff. Arizona 86011

EnV1ron. Entomol. 19(5)- 1173-1182 (1990)ABSTR.-\cr Despite many examples of plants. hypersensitive reaction against pathogens,there are exceedingly few examples of hypersensitive reactions having any importance againstinsect nerbivores. However. such plant defense mechanisms may be widespread among moresedenwy insect herbivores. The examples in which a hypersensitive reaction was elicitedagains: insect herbivores were against galling insects. bark beetles. adelgids. and siricids. Theintimate and sessile interactions during insects. egg and larval stages may have selected morespecilic and more complex d~fcnses. because of the greater and more varied opportunitiesthat t!:-e host plant has for regulating the lives of its intimate associates. Thus. it is arguedthat t:r.e intimate association of these herbivores during egg and larval stages set the scenariofor t~ evolution of this plant defense mechanism. The dearth of accepted examples ofhypersensitive reaction against insect herbivores may not reflect its actual frequency andoccurrence in nature. Further investigation on plants. hvpersensitive reaction against insectherbl'ores may shed light on the ecology and evolution of insect-host plant associations.

KEY WORDS lnsecta, hypersensitive reaction. induced defense. insect herbivory

The hypersensitive reaction encompasses alImorphological and histological changes that. whenproduced by an injurious agent. elicit the prema-ture dying. or necrosis. of the infected tissue. aswell as inactivation and localization of the infec-tiousagent (Mfil1er 1959. Maclean et al. 1974. Agri~1988). After reaching the plant.s surface. the path-ogen must penetrate into the plant .s cells. Afterpenetration. a suitable nutritional site must be foundto guarantee successful establishment. In some ca25.establishment may fail because of the rapid deathof the host.s tissues at the site of infection. It is notthe invaded cells. but the adjoining cells that die(White & Baker 1954. Hirata 1956). There is apositive correlation between the speed of reactionand the degree of host resistance to microorganisms(White & Baker 1954. Cóffey & Wilson 1983. Da-vidse et al. 1986). Hypersensitivity is usually con-trolled by an individual gene or. more rarely. bya few genes. Flor (1955) showed that hypersensi-tivity to fungi is determined by two specific genes.one in the host and the other in the pathogen. Forfurther explanation of the gene-for-gene relation-ship. see reviews by Flor (1971) and Barrett (1985).

Hypersensitive reaction is the primary event inresistance to fungal parasites (Maclean et al. 1974.Agrios 1988). This reaction by the host leads to adisruption of nutrient supplies to the invading mi-croorganism (Wong & Berryman 1977) and theproduction of many toxic metabolites. such as phy-toalexins (Bavlev & Mansfield 1982. Smith & Banks-1986) resultiitg in the cessation of microorganism

-STUDIES OF PLA-'l RESlSTANCE to insects have beencentered on a wiàe spectrum of plant features, suchas secondary com!X>UDds (Rosenthal & Janzen 1979,Green & Hedin 1986), nutritional factors (Rodri-guez 19i2, Wbite 1984), phenology (Feeny 1976,Faeth et al. 1981i. age (Morgan et al. 1983, Kear-sley & Whitham 1989). induced defense (Green &Ryan 19i2. Rhoaàes 1979, Haukioja 1982. Baldwin1988 ). abscission : Kahn & CorneII1983, F ernandes& Whitham 1989), plant morphological traits (pu-bescence [Levin 1973. Pillemer & Tingey 1976,Woodman & Fernandes in press], tissue hardness[Coley 1983], coior [Tingey 1981], shape [Rausher19i81 size [Kogan 19i51 and presence or absenceof nectar-secreting glands [Wilson & Lee 1971J).Verv few studies :nave. however, addressed the im-portance of a particular type of induced defense,i.e., plant hyper!eDsitivity, as a source of plant re-sistance to inseCt herbivore attack.

Plant hypersemitivity is a term primarily usedby plant pathologists to describe a response to in-fection by pathogens as well as to many nonpath-ogenic stimuli :e.g.. Matta 1971, Misaghi 1982).Since the beginmng of this century. hypersensitiv-ity has been recognized as an important defensemechanism used by plants against pathogens (e.g.,Ward 1902. Stakman 1915).

I Current addr~ ~ento de Biologia Geral. C.P. 2486.

ICB/Univenidade Federal de Minas Gerais. 30161 Belo Hori-zonte. ~1G-BraziL

0046-225X/90/1173-1182S02.00/0 (C) 1990 Entomological Societv of A~ca

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174 ENVIRONMENT AL ENTOMOLOGY Vol. 19. no.5

growth (Maclean e[ al. 1974, but see Johal & Rahe19881. Furthermore. water ar'd oxygen also arereduced. thus further decreasing the probabilitiesof establishment and success for the .invading or-ganism (Wong & Berryman 1977).

Despite numerous examples of the hypersensi-tive reaction against pathogens, there are exceed-ingly few examples of hypersensitive reactions hav-ing any importance against insect herbivores.Painter (1951 i concluded that hypersensitivity wasnot offered as an explanation for any insect-plantrelationships despite the possibility that it is in-volved as a response to insects with sucking mouth-parts. Here 1 revíe\\. the literatiíre in which hy-persensitivity is reported to be one of themechanisms by which plants respond to insect her-bivores, and I trv to evaluate whv there are so fewexamples of it i~ the insect and plant literature.

secretions showed a capacity to oxidize the o-di-phenols present on the buds of its host plant (Miles& Peng 1989). Removal of the aphids from treat-ment plants resulted in significantly elevated cate-chin levels. These studies illustrate the abilitv of asap-feeding insect to inter.vene in the host plant.sdefense mechanism, making plants more accept-able to the insect. A mucus of an unknown chemicalnature that is injected by siricid woodwasps duringoviposition reduces the host plant.s hypersensitivereaction against the larval feeding stages of thewasp and its symbiotic fungus (Madden 1988). Inanother case. a mucous substance injected by siricidfemale woodwasps during oviposition reduces thehost plant.s hypersensitive reaction against theiroffspring (Madden 1988). However, more studiesare necessarv to evaluate insect herbivore.s abilitvto manipulate localized reactions of host plants suc'-cessfullv. -

The hypersensitive response of plants to injuryand the consequent development of necrotic tissueis prevented by high temperatures (37°C [98.6°F])(Deverall1977, Király 1980). This is consistent withtne observations by Fernandes & Price (1988, inpress) that gall-forming insects are more species-rich in xeric and hot, nutrient-poor, areas than inmesic and.cooler, nutrient-rich areas. Fernandes &Price \in press) argued that galling insects survivebetter on en..ironmentally stressed plants than on

healthy plants. Environmentally, stressed conifer-ous trees were also more susceptible to bark beetleattacks (e.g., Wong & Berryman 1977; Raffa &Berryman 1982, 1983, 1987; Christiansen et al.1987).

The hypersensitive reactions of trees are less ef-fective under stress conditions (Puritch & Mullick19'i5, Christiansen et al. 1987). For instance, waterstress greatly affected the necrophylactic peridermformation in Abies grandis and consequent in-creased susceptibility of trees to insect herbivores(Puritch & Mullick 1975). The synthesis of defen-sive chemicals is an energy-expensive process (e.g.,Feenv 19'i6, Rhoades 1979); hence the success ofeliciting a h)1>ersensitive reaction must be depen-dent on current availability of energy (see Berry-man 1988). Physiologically healthy plants havemore energy (Miller & Berryman 1985), and per-haps better mechanisms for responding to theirherbivores than plants in poor physiological con-dition lsee a1So Bernard-Dagan 1988, Cheniclet etal. 1988, Tuomi et al. 1988). There is an obviousneed for cooperative endeavors between plant pa-thologists, plant physiologists, and entomologists.Onlv a multidisciplinarvapproach can unravel thefact:s that lead to an understanding of the processesand mechanisms involved in the interaction be-tween plants and their concealed or sedentary in-sect herbivores (or both). This approach taken inbark beetle-host plant-fungus systems led to anenormous understanding of the patterns and prox-imate and ultimate mechanisms involved in thesvstems.

Some Biochemical and PhysiologicalAspects of Hypersensitivity

Several metabolic changes are detected at thetime tissue necrosis appears. The respiration rate,oxidase levels, peroxidase levels, and mitochondrianumbers ali increase during the hypersensitive re-action (Királ:-. 1980). In addition, levels of phenolicand flavonoid compounds are increased (Loeben-stein 19+2). However, because several biochemicalchanges are detected simultaneously, it is difficultto decide with certainty which one is the primaryevent that causes cell and tissue necrosis and rapidloss of water. The necrotic response is the result ofa disturbance of balance between oxidative andreductive processes (Király 1980). The result is anexcessive oxidation of polyphenol compounds anda breakdown of cellular and subcellular structures.It is not known whether the excessive oxidation ofphenols by phenolases or perox~Qases is the causeor consequence of breakdown in cellular structures(Király 1980. Cruickshank 1980).

The local necrosis may be regarded as a conse-quence of a pronounced senescence effect (Farkas1978). Nevertheless, necrosis development andspread can be decreased by induction of a highrate of RNA and protein synthesis (i,e., by therejuvenation effect of cytokinin treatment and oth-er manipulations) (Király 1980), Not surprisingly,host plant tissues under the action of gall-forminginsects present a high rate of RN A and proteinsynthesis (e,g.. Bronner 1977, Rohfritsch & Short-house 1982, Meyer 1987). I postulate that in ad-dition to increa5ed nutritional quality and preven-tion of abscission (by rejuvenation), gall formersengineer the host plant tissue to produce metabo-lites that avoid or decrease the probability of ahypersensitive reaction by the plant.

Peng & Miles (1988a,b. and references therein)experimentally showed that the sap-feeding roseaphid. MaCTosiphum Tosae L., manipulates its hostplant .s chemical defenses. The phenol-oxidizingenzyme found in the aphids. salivary glands and

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FERNANDES: HyPERSE."SITIVE REACTIONS AGAINST HERBIVORES 1175October 1990

Hypersensitivity ResponseAgainst lnsect Herbivore§

Plants present a large spectrum of resistancemechanisms against insect herbivores. The defensemechanism used is largely dependent upon manyfactors. but primarily the physiological status ofthe plant. timing of attack. damage levei. type oftissue removed. and intimacy of the relationshipbetween plant and herbivore. Thus. lnseCt herbi-vores can be classifjed according to the kind andamount of injury they inflict on their host plants.Mattson et al. (1988a) classifjed phytophagous in-sects into two major groups, free-feeding and at-tached-embedded insects. Based on the potentialeffect on host growth and reproduction. ~Iattsonet al. (1988a) ranked phytophagous insects into 13feeding guilds. They argued that gall formers posethe least threat to their host plant .s growth andreproduction, whereas phloem. cambium. sapwoodborers have the greatest potentia] effect (but seeFernandes 198i). However. gallers and bark bee-t]es may influence p]ant defense mechan1Sms insimilar ways.

Price (1980) argued that the host.s spectrum ofdefense responses to parasites is dictated by theintimacv of the association Isee aJso Harris-& Fred-eriksen i984). Mattson et a]. (1988al state that withthe most intimate associations. alllife stages occurwithin p]ant tissue, such as some bark beet]es andgalling insects. The least intimate association wou]dthen be those of herbivorous insects that feed ex-terna]]y on their host p]ants. Mattson et al. (1988a)suggested that intimate interactions may select morespecifjc and more complex defenses because of thegreater and more varied opportunities t:i1at the hostplant has to regulate the lives of its intimate as-sociates. This hypothesis is supported by the factthat embedded and phytophagous insects withstrongly limited movement are more host specifjcthan free-feeding insects (see Haak & Slansky 1987 ;Mattson et al. 1988a.b). and by Maddox & Root.s(1987) fjndings that heritab]e differences amongc]ones of Solidago altissima for resistance to gallinginsects were larger than for other kinds of phy-tophagous insects.

In ]ine with Mattson and his assocÍates. argu-ments. I present examp]es where pJants respondsimi]arly to both ga]]-forming insects. bark beet]es.adelgids. and woodwasp attack. I h)1>0thesize thatthe intimacv of the association. the feeding behav-ior. damage' type. and type of plant tissue ;emovedset the stage for hypersensitive reactioD.

Hypersensitive ReactioD Against Galling In-sects. The fjrst recorded case of a hypersensitivereaction by a plant against an insect herbivore mayhave been that of grapes and their Phylloura ga]]-er. Bõtner & Schi]der (1934) observed that resistantVitis spp. were hypersensitive to P. oostatrix (Fitch).a leaf-ga]]ing insect. Resistant plants reacted to theattack of P. vastatrix with locall\" limited necrosis.As a result, ga]]s did not develo"p arouod the site

of induction. The induction sites were shut off bvan inner wound periderm from the remaining ti;-sue. The necrotic tissues were'later abscised (Miiller1959).

The eastern spruce gall aphid. Adelges abietisL., induces pineapple-like galls on Picea excelsa L.(Rohfritsch 1981). Both susceptible and resistantspruce trees were attacked by A. abietis. However.a hypersensitiv~ reaction is elicited by resistant treesduring the first stages Qfgall initiation (Thalenhorst19i2, Rohfritsch 1981 ). The greater hypersensitiv-ity of the attacked cells leads to cell collapse byplasmolysis. necrosis. and accumulation of phenolicsubstances (Tjia & Houston 1975; Rohfritsch 1981.1988). The insect that is now surrounded by thenecrotic cells has its access to soluble proteins ter--minated. Rohfritsch (1988) argued that a ..kind oihypersensitive reaction.. is the primary mechanismbv which P. excelsa trees respond to the attacks oftheir galling insects.

Hypersensitive reactions also have been reportedfor EuTosta solidaginis (Fitch,. a tephritidstemgaller on Solidago altissima L. Seventy-three per-cent of EuTosta larval mortality was due to a hy-persensitive reaction by the plant (Anderson et al.1989). Field and laboratory experiments have shownthat plant genotypes that grow faster are preferredby the ovipositing female, and that these rametsare more reactive to the insect larval stimuli forgall formation (Weis & Abrahamson 1985). An-derson et al. (1989) showed that adult females pre-ferred susceptible ramets over resistant ramets inlaboratory trials, thus suggesting that females havediscriminatory abilities. Female choice had strongeffect on larval survivorship because larvae sur-vived better in susceptible plants than in resistantplants. In susceptible plants. 100 and 97% of thelarvae developing in leaf buds and meristem, re-spectively, survived. However. only 6i a!!d 35% ofthe larvae developing in leaf buds and meristem.respectively. of resistant plants survived.

Another case that is currently under investiga-tion \unpublished data) is the hypersensitive re-action of the shrub ChTysothamnus nauseosus(Palias) Britt. to a Rhopalomyia cecidomyiid stemgall former. On resistant plants, h~1Jersensitive re-actions develop after the larvae hatch and startfeeding on plant tissue. Necrotic tissue developsconcentrically around the feeding site stoppingwater and food supply to the lan.a. These galls donot achieve normal size and do not fully developthe trichome layer that covers the gall chamber.Preliminary data indicate that hypersensitivity isthe main mortality factor for this gall former inhumid habitats.-

The feeding activity of a mite species, ETiophyescladophthiTus Nal., induces a h~1Jersensitive re-action on its solanaceous host plant. It perforatesthe wall of epiderriial cells of its host. SolanumdulcamaTa L.. causing cone-shaped feeding punc-tures (WestphaI1980. Westphal et al. 1981). Cal-lose was detected near the puncture after 20 min

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Vol. 19. no.5E~VIRONMENTAL ENTOMOLOGY1176

of the life cvcle, the insect is anchored to the treeby the feeding sty.lets that are inserted in the bark(Greenbank 1970). Abies spp. respond to their adel-gid herbivore with the formation of "rotholz," orredwood, in the xvlem tissues \see Balch 1952. Hain1988). Rotholz f~rmation appears to be a contin-uation of the host hypersensitive response to theinvading adelgids. The first fir response to the in-jury is the formation of a secondary periderm, thenecrophylactie-periderm. internal to the wound(Mullick & Jen~en 1973a.b; Mullick 19ii). whichisolates the necrotic cells of the hypersensitive re-action from the healthv. unaffected cells (Hain1988). A layer of impe~ious tissue precedes for-mation of the necrophylactic periderm (Mullick1975). However. in susceptible hosts. the formationof the impervious layer is inhibited or delayed; orboth. Mullick & Jensen ( 19i6) found that the ratesof the development of this tissue were consistentlyfaster on resistant hosts than on susceptible ones.The more effective response of European firs tothe balsam woolly adelgids compared with Amer-ican firs is due to a faster hypersensitive reactionthat kills or inhibits feeding of the insect herbivore(Hain 1988).

Hypersensitive Response Against W'oodwasps,Growth of woodwasps lan.ae of the geniis Sirex isdrastically impaired on host plants that elicit a hy-persensitive response. Hosts belong to-the generaPinus, Abies, Picea, Larix. Pseudotsuga, and Au-ricaria (Morgan 1968, ~1adden 1988). Woodwaspsare attracted to physiologica1ly stressed trees (Mad-den 1977, 1988). During oviposition, the femaleinjeets a mucus of unknown chemical nature andspecies-specific symbiotic fungal spores into the hostplant tissue. The mucus alters the water balance ofplant needles causing tissue desiccation and col-lapse of the phloem elements (Fong & Crowden1973) and resu1ting in inhibition of translocation(Madden 1988). The combination of these pro-cesses, plus plant tissue laceration during wood-wasp oviposition favors fungus establishment andgrowth. Host resistance to Sirex and its symbioticfungus is primarily due to a hypersensitive reactionby the invaded host plant \e.g., Coutts & Dolezal1966; Coutts 1969a,b). Polyphenols are producedas a specific response to the woodwasp symbiontfungus (Coutts & Dolezall966, Hillis & Inoue 1968).The mucus plays a major role in inhibiting trans-location of photosynthate- a precursor to polyphe-no1 synthesis (Madden 1988). Water-stressed treesare the most susceptible hosts to woodwasps. Inwater-stressed hosts, photosynthesis and transpi-ration decline, thus impairing host hypersensitivereactions against the invading fungus (see Madden

1988).

and the injured cel15 were transformed into nutri-tive ce115. Cel15 near the feeding 5ite5 on 5U5ceptible-plan.t5 become nutritive ce115. w~ereas on re5i5tantplant5 they become necrotic. This hyper5en5itivere5pon5e wa5 detectable on injured epidermal cel15after 10 min and led to 5evere necr05is of 5urround-ing ti55ue5 after 1 h. Polyphenolic compound5 weredetected in the necrotic region after 4 h. Water1055 at the contact 5ite between h05t and para5itemay have been the triggering mechani5m to thehyper5en5itive reaction (We5tphal et al. 1981. 5eeal5o Abawi et al. 1977. Sigee & Epton 1976). Afterthe mite had perforated a cell, its vacuolar pHincrea5ed in 5U5ceptible andre5istant plant5 (We5t-phal 1982). However. the reaction wa5 fa5ter in5U5ceptible h05t5 than in re5i5tant h05t5. which re-5ulted in the collap5e and death of injured cel15 in

the latter.Hypersensitive Reactions ~st Bark Beetles.

Hyper5en5itivity i5 a mechanism whereby conif-erou5 plant5 re5i5t bark beetle attack (e.g., Berry-man 1969. 1972; Berrvman & A5hraf 1970; Raffa& Berrvman 1982. 1987; Christiansen et al. 1987),-The ~etle5 that 5urvive the limited flU5h of pri-marv re5in are faced with the tree.s second line ofdefe'n5e-hyper5ensitive reaction in the ti5sues sur-rounding the beetle.s galler~'. The cel15 5urroundingthe attacked site degenerate. and terpenes. pol~,-phenol5, and other toxic or inhibitory compQundsare relea5ed (Miller et al. 1986. Christian5en et al.1987). As a re5ult, both beetle and pathogenic fun-gu5 inoculated by the beetle are sealed in a le5ionof dead. re5in-impregnated tissue (Wong & Ber-ryman 1977. Raffa & Berryman 1987). The ne-crotic area al50 is impregnated \\ith re5inou5 andphenolic compounds that prevent construction ofbeetle gallery, fungal proliferation. and beetle eggand larval 5urvival (Russel & Berryman 1976, Raffaet al. 1985, Christiansen et al. 1987). Hypersensitivereaction appears to be the most important defen5emechanism in lodgepole pine and Norway 5pruceagainst bark beetle attack (see Raffa & Berryman1982, Christiansen & Horntvedt 1983). The conif-erou5 tree bark-beetle fungus ~"stem is the mo5twell-5tudied example of plant h,.-per5en5itive re-action involving herbivorous insects (for additionalreference5 5ee Chri5tiansen et~. 1987, Raffa &Berrvman 1987, Berrvman & Ferrell1988, Chri5-tian5'en & Bakke 1988, Flamm et al. 1988, Raffa

1988).Hypersensitive Reactions Against Balsam

Woolly Adelgids. Hypersensitive reaction5 suc-cessfully reduce the effect caused by bal5am woollyadelgids on fir trees. North .-\.rnerican fir5, com-pared with European fir trees, experience extensivecrown dieback, or tree death. or both, as the resultof attack by Adelgis piceae (Ratzeburg};On hatch-ing, the fir5t-instar nymphs wander on the treebefore 5ettling on selected feeàing sites within thetree crown or on steffi$. This brief crawler stage i5the only motile stage. Throughout the remainder

DÍ6eu§8ion

Hypersensitivity is an important mechanismwherebv plants resPOnd to insect herbivores. Ali

L

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FERNANDES: HyPERSENSITIVE REACTIOr.;S AGAINST HERBIVORES 1177October 1990

the cases in \vhich hypersensitivity was found tobe a mechan1Sm operating against insect herbivoreswere for galiers, bark beetles, adelgids, and wood-wasps. However, plants' hypersensitive reactionsmay be common against other phytophagous in-sects particularly less mobile insects during theirfeeding stages. such as coccids, psyllids, and gallingsawflies. The intimacy of the association posed bythe h~rbivorous feeding habit and quality of thetissue remo\.ed ma\, have set the scenario for thedevelopment and évolution of this plant defensemechanism. Adoptmg an ..optimal defense view,.'Berryman ( 1988) proposed that defensive traits areselected to optimize plant fitness in the face ofdifferent herbivore attack patterns and life historystrategies\seealsoRaffa & Berryman 1987). Hence,different plant defense strategies should be ex-pected against the different insect herbivore guilds.

Other plant defense mechanisms should be ex-pected for free-feeding insect herbivores. It wouldbe detrimental to a plant to be hypersensitive tofree-feeding herbivores, because free feeders canmove about and among plants. The immediate con-sequence of this strategy \vould be a cork tree! Theapparent lack of substantial evidence for significantgenetic variation among plants resistant to mostfree-feedin2 leaf herbivores is corroborative of thisview (e.g., ~ Maddox & Root 1987, and revie\"by Mattson et al. 1988a). Conversely, differentialpl~pt resistance to sap-feeding, gall-forming, andbark beetle insects are very common in the liter-ature (e.g., Edmunds & Alstad 1981; Wilson &Moore 1986; Mattson et al. 1988a,b; Rohfritsch1988).

Hypersensitive reactions of plants ultirnately mayhave inHuenced the distribution of movement-con-strained insect herbivores. The sessile habit is com-plete in galling insects because they can not leavetheir galls once formed, but leafminers, stem bor-ers, and bark beetles can still move with some free-dom inside their host or even leave it (e.g., Gross& Price 1988). Hence, leafminers and stem borerscan avoid or select feeding areas inside the host.Several gallers develop from eggs laid inside theirhost plants, and thus cannot choose where to inducethe gall. However. the females must have evolvedbehaviors to avoid laying eggs in plant parts wherenecrosis is more likely to happen. DeClerck &Steeves (1988) reported that the cecidomyiid CYs-tiphora sonchi (Bremi) lays its eggs through thestomata of its host plant, Sonchus arvensis L., thusavoiding injury to the host and a possible hyper-sensitive reaction against the egg. Furthermore,larval behaviors may have evolved to elicit reju-venation of tissue that guarantees a highly nutri-tious diet and at the same time prevents necrosis.For example, galling aphids and psyllids penetratethe tissues of food plants intercellularly and feedprimarily on phloem sap, thus bypassing the con-tents of parenchymal cells en route (Campbell etal. 1986. Raman 1987). These behaviors corrobo-

rate the view that more specifjc insects such asgallers. bark beetles. and sap-feeders can avoidfeeding on plant tissues where hypersensitive re-sponses are likery to occur.

More studies on plants. hypersensitive reactionsto herbivores are needed. Closer observations shouldbe made during the herbivore.s oviposition periodto verify site selection and host response to egglaying and injury. Because microorganisms may beassociated with insect gall formation (e.g., Cornell1983. Price et al. 198i), we must verifv if the hv-persensitive reaction is directed to the. insect hér-bivore or to the associated microorganisms, as seenin the bark beetle svstems, as well as in the siricid-fungus systems. Ind.eed much of plant defense maybe adapted to the symbiont microbes rather thanthe insect herbivore. For instance, Jones et al.(1981a.b) showed that allelochemical defenses ofbaldcypress inhibited silkworm enteric microor-ganisrns by altering the physiological state of thesilkworm .s gut. The loss of the microbial nutritionalcontribution caused silkworm larval growth inhi-bition. ~tany other examples exist (e.g., Hedin etal. 19i5. Martin 198i), indicating that this phe-nomenon may be widespread. Insect herbivore-microbe mutualisms are widespread in nature andinfluence the success and radiation of marn' insectorders. such as Isoptera and bark beetles (Breznak19i5,.Jones 1984, Price 1984. CampbeII1989). Mi-croorganisms contact with plants happened muchearlier in evolutionary time than contacts betweeninsects and plants (e.g., Atsatt 1988). Thus, it ispossible that many plant defenses, such as hyper-sensitivity reaction, and perhaps phenolic com-pounds, are responses directed to symbiont rnicro-organisms rather than the herbivore. Phenoliccompounds are very widespread and an importantplant response against microorganism invasion(Matta 19i1, Misaghi 1982). Recent studies havealso shown that many defense mutualisms haveevolved between plants and endophytes (e.g., Car-ro111988, Clay 1988). The pursuing of studies onthese phenomena may broaden our limited, two-dimensional (herbivore-host plant) view of herbi-

vore-plant relationships.A theory for plant defensive responses on a cel-

lular levei was developed by Berryman (1988) (seealso Bernard-Dagan 1988, Cheniclet et al. 1988,Lieutier & Berryman 1988a,b). In this theof)..parenchyma cells react to alI kinds of injuries in asimilar way (see Hadwiger & Beckman 1980, Had-wiger et al. 1981, Lieutier & Berryman 1988b).Plant cell wall polysaccharide fragments are re-leased by mechanical damage or by the action ofenzymes secreted either by the host plant or her-bivore during herbivore feeding (Darvill & Albers-heim 1984). The release of these fragments triggersthe attacked host plant to produce some defensivechemicals. The chemicals produced would be con-tained ",ithin vacuoles and nonliving plant tissuesor transported via the conducting tissue and would

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Vol. 19. no.5ENVIRONME!-.IAL ENTOMOLOGY1178

activate celis remote from the point of injury (Ber-ryman 1985). thus causinga systemic reaction observed in some plants (e.g., Edwards & Wratten1983. Kúc 1983). This type of résponse is elicitedby enàogenous or endoelicitors that are productsof the plant itself (Berryman 1988). Exogenous orexoelicitors lenzymes or toxins secreted by the in-vading organism or fragments of their extemal skinreleaseà by the action of plant enzymes) wouldgive rise to a different plant response (see Ryan1984. ~1iller et al. 1986. Berrvman 1988). In thiscase. host parenchyma cells become hyperactive.thus producing large quantities of defensive chem-icals that are synthesized in an apparently uncon-trolled manner. The defensive substances or theirprecursors and cell fragments are released into theconàucting plant tissues blocking the penetrationof the pathogen and extending the reaction zone(Be~man 1988). Hyperactivity will cease as soonas the invasion is contained.

?\'evertheless. our knowledge about the biochem-ical anà cellular bases for the hypersensitive re-sponse to phytophagous insects is still fragmentar).and rudimentary. There is an increased need formore focused studies on this plant resistance mech-anism as more examples of its widespread occur-rence are discovered. It is true that well-docu-mented cases of the hypersensitive reactlon againstinsect herbivores are rare. However, a phenome-non mav lack documentation for reasons other thanthe sca~cih. of its occurrence. For instance, studiesof host'resistance could have missed hypersensitiv-ity as a mechanism because of the way in whichstudies were done. In addition, a phenomenon alsomay appear rare due to rigid standards posed bythe scientific community for its identification andverification. Thus, the dearth of accepted hyper-sensitive reaction examples against insect herbi-vores may not reflect its actual frequency and oc-currence in nature. Further investigation on plants.hypersensitive reaction against herbivorous insectsmay shed light in many other areas of ecology andevolution- and perhaps bridge our fragmentar)'knowledge of many fields in biology.

Acknowledgment

I thank T. G. Whitham. P. W. Price, S. Suter, K. C.Larson. O. Rohfritsclr, E. Westphal. J. States. R. De-clerck-Floate. M. J. C. Kearsley, a special anonymousreviewer .and two other anonymous reviewers for theirenthUSIasm and helpful comments on early drafts of thismanuscript. I also acknowledge a scholarship providedby the Conselho Nacional de Ciência e Tecnologia inBrazil :CXPq. process #200.747/84-3-Z0). and the fa-cilities Dro\ided bv Northern Arizona University.

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Received fOT publication 27 OCtObeT 1989; accepted28 MaTch 1990.

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