Báo cáo khoa học: "Preliminary study of the monoterpene response of three pines to Ophiostoma clavigerum (Ascomycetes : Ophiostomatales) and two chemical elicitors"

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Nội dung Text: Báo cáo khoa học: "Preliminary study of the monoterpene response of three pines to Ophiostoma clavigerum (Ascomycetes : Ophiostomatales) and two chemical elicitors"

Original article Preliminary study of the monoterpene response of three pines to Ophiostoma clavigerum (Ascomycetes : Ophiostomatales) and two chemical elicitors F Lieutier AA JA Millstein Berryman 1 Ardon 45160 Olivet, France; INRA, 2 Washington State University, Department of Entomology, Pullman, WA 99164, USA 15 March (Received 3 August 1990; accepted 1991) Summary — The monoterpene response of phloem and sapwood of individual pines belonging to 3 species (Pinus contorta, Pinus ponderosa and Pinus monticola) to inoculation with Ophiostoma cla- vigerum and injection with chitosan, a proteinase inhibitor-inducing factor and a control buffer, was investigated quantitatively and qualitatively. The total quantity of monoterpene in the reactive tissues increased with each treatment but to different levels. In each tree, the monoterpene composition of the reactive tissues differed from that of the unwounded tissues, but was the same whatever the in the case of an injection with buffer control. In addition, phloem and sapwood re- treatment, even sponses were qualitatively identical although constitutive compositions differed greatly. The compo- sition of reactive tissues was not very different from that of unwounded sapwood. The direction of variation of each monoterpene from unwounded to reactive tissues differed according to the particu- lar tree. Only phellandrene + limonene reacted consistently. From these results we cannot conclude that chitosan is a natural elicitor, and the non-specificity of the response for the aggression favors the hypothesis that an elicitor originates from the tree itself. Because of this non-specificity, and the fact that the three trees responded in a qualitatively different manner, we suggest that the qualitative monoterpene response of the tree is not adapted to any specific aggressor even though these trees are usually hosts of the same bark beetle-fungus complex. Thus, the role of monoterpenes in the in- duced defensive response is very likely a quantitative and dose-dependent relationship. / Pinus contorta / Pinus ponderosa / Pinus monticola / Ophiostoma clavige- monoterpenes / chemical elicitors / defense reaction / gas chromatography rum Étude préliminaire de la réponse monoterpénique de trois pins à Ophiostoma cla- Résumé — vigerum (Ascomycètes : Ophiostomatales) et à deux éliciteurs chimiques. La réponse mono- terpénique du phloème et de l’aubier de 3 arbres appartenant aux espèces Pinus contorta, Pinus ponderosa et Pinus monticola a été étudiée d’un point de vue quantitatif et qualitatif, après des ino- culations du champignon O clavigerum et des injections de chitosane, d’un facteur induisant une inhibition de protéinase (PIIF) et d’une solution tampon témoin. La quantité totale de monoterpènes (hydrocarbures) mesurée après 3, 7 ou 14 jdans les tissus réactionnels augmente après chaque traitement, mais atteint des niveaux différents, le plus élevé étant obtenu après inoculations du champignon. Dans le cas du chitosane, la réponse est quantitativement proche de celle dirigée contre O clavigerum chez P ponderosa, mais ne diffère pas de celle dirigée contre le PIIF et la solu- tion tampon chez les 2 autres arbres (tableau I). Dans chaque arbre, la composition monoterpénique des tissus réactionnels diffère de celle des tissus non altérés, mais s’avère semblable quel que soit
le traitement, même avec les inoculations de tampon témoin (tableau II et fig 1). De plus, les réponses du phloème et de l’aubier sont qualitativement identiques, bien que leur composition initiale soit très différente. La composition des tissus réactionnels n’est en outre pas très différente de celle de l’aubier inaltéré (fig 1). Le sens de variation de chaque monoterpène entre le tissu inaltéré et le tissu réaction- nel varie selon l’arbre considéré; seul le groupe phéllandrène + limonène réagit toujours dans le même sens (fig 2). Il n’est pas possible de conclure de ces résultats que le chitosane est un éliciteur naturel, et la non- spécificité de la réponse vis-à-vis de l’agresseur est en faveur d’une hypothèse qui situerait dans l’arbre lui-même l’origine de l’éliciteur. À cause de la non-spécificité de la réponse et du fait que les 3 arbres réagissent différemment d’un point de vue qualitatif, il est suggéré que la réponse monoterpé- nique qualitative d’un arbre n’est pas adaptée à un agresseur particulier, bien que ces arbres soient des hôtes habituels du même couple scolytide-champignon. Ainsi, le rôle des monoterpènes dans la réaction de défense induite est très probablement de nature quantitative et dépendrait de la dose ac- cumulée. monoterpène / Pinus contorta / Pinus ponderosa / Pinus monticola / Ophiostoma clavigerum / éliciteur chimique / réaction de défense / chromatographie en phase gazeuse INTRODUCTION proteinase inhibitor-inducing factor and a (PIIF) (Lieutier and Berryman, 1988). Here we demonstrate both qualitative and quan- The fungus Ophiostoma clavigerum titative changes in monoterpenes induced (Robinson-Jeffrey and Davidson) Upad- in the same tissues by the same inocula- hyay plays a decisive role in the mecha- tions and injections. Note that chitosan is a nisms of establishment of the bark beetle mixture of β-(1,4) glucosamine polymers Dendroctonus ponderosae Hopk in North which are constituents of arthropod integu- American pines, particularly Pinus contorta ments and of most fungal cell walls (Had- var latifolia Engelmann, Pinus ponderosa wiger and Beckman, 1980). PIIF is com- Lawson and Pinus monticola Douglas posed of pectic oligomeric fragments (Reid et al, 1967; Safranyik et al, 1975; derived from plant cell walls, the most ac- Shrimpton, 1978; Raffa and Berryman, tive being α-(1,4) galacturonic acid poly- 1983). During bark beetle attacks, this fun- mers and oligomers (Ryan et al, 1985). gus stimulates host parenchymal cells to Both chitosan and PIIF are possible elici- produce resin which impregnates the tis- tors of induced responses in plants natural- located around the site of attack sues ly attacked by insects and fungi (Hadwiger (Reid et al, 1967; Berryman, 1969; Lieutier et al, 1981; Walkers-Simons et al, 1984; and Berryman, 1988). This induced reac- Green and Ryan, 1972). tion is the main line of tree defense against the attack of the bark beetle and Quantitative and qualitative monoter- its associated fungus. However, the nature pene modifications in response to the at- and the origin of the chemical elicitor re- tack of bark beetles and associated fungi sponsible for the stimulation of the paren- have been reported in conifers by several chyma cells is not clear. authors. Shrimpton (1973), Raffa and Ber- ryman (1982a), Schuck (1982) and De- In a previous paper, we reported the lorme and Lieutier (1990) noted an in- histological changes induced in the reac- crease of the total monoterpene content of tive tissues of these 3 pine species by arti- phloem and sapwood in the induced reac- ficial inoculations of O clavigerum and in- tions of P contorta, Abies grandis (Lindley), jections of 2 chemical elicitors, chitosan
sample of each treatment was taken on Picea abies Karst and Pinus sylvestris L, one each tree. Reactive phloem (with cambium) and respectively. Miller et al (1986) reported a sapwood were removed and cut longitudinally in greater increase in the total monoterpene half. One half was immersed in a cupric acetate content of Lodgepole pine phloem in re- solution for histological observations (Lieutier sponse to chitosan than to either PIIF or O and Berryman, 1988) and the other was immedi- clavigerum. Qualitative changes in the atly placed on dry-ice and stored at -60 °C. Two monoterpene fraction of the phloem were wk after treatment, samples of unwounded phloem and sapwood were also collected and observed by Russel and Berryman (1976) stored in the same manner. and Raffa and Berryman (1982a) in A Monoterpene analyses were performed on grandis, by Raffa and Berryman (1982b) in samples collected after 3 and 14 d. Samples col- P contorta, by Cook and Hain (1985) in Pi- lected 14 d after treatment were divided into 3 nus taeda L and by Delorme and Lieutier pieces, starting at the point of inocula- 20-mm (1990) in P sylvestris. In the last 2 cases, tion and working away from the wound, giving the qualitative changes were the same for sub-samples at 0-20 mm, 20-40 mm, and 40- a given tree for all treatments (ie, 2 differ- 60 mm Three-d-old samples consisted of a sin- gle 0-20 mm piece. Each phloem sub-sample ent strains of the same fungus in P taeda, was finely chopped and then shaken in 10 ml 3 different fungus species and 1 beetle in pentane for 24 h. The extracts were filtered by P sylvestris). Shrimpton (1973) was unable flash chromatography in silica-gel G which was to observe any qualitative changes in P rinsed thrice in pentane. They were concentrat- contorta sapwood, with the exception of β- ed under a stream of nitrogen to 0.5, 1 or 2 ml phellandrene after natural attacks by D according to the richness in total monoterpenes. Analyses were performed on a Perkin-Elmer ponderosae. However, Schuck (1982) re- Sigma-3 gas chromatograph equipped with a ported changes in some monoterpene flame ionization detector and a 30 m x 0.2 mm components of P abies sapwood after capillary column (Supelco SE-30). The carrier wounding. gas was helium at 1.1 ml/min at 18 psi. The col- umn temperature program was 80 °C for 14 min, a rise of 20° per min to 100 °C, then 100 °C for MATERIALS AND METHODS 40 min. The injector and detector temperatures were constant at 250 °C. Three replicates were performed for each sub-sample. Peaks were The experimental devices and techniques were identified by comparison with the retention times previously described by Lieutier and Berryman of pure monoterpenes added to the samples (1988). One specimen of each tree species and by enhancement after these additions. For (P contorta, P ponderosa, P monticola, 30 cm = P contorta, comparisons were also made with diameter breast height from an even-aged mass spectrography results from Raffa and Ber- mixed conifer stand) received a total of 12 inocu- ryman (1982b). The quantitative values were de- lations (4 treatments replicated thrice) in July termined by means of an electronic digital inte- 1985 at breast height using the cork-borer tech- grator using p-cymene as an internal standard nique (Wright, 1933; Wong and Berrryman, (this terpene was found to be lacking in prelimi- 1977). The first treatment was inoculation with O nary chromatograms). clavigerum, the second with chitosan, and the The monoterpene compositions of the sam- third with PIIF. Fungal cultures were 10-15 d ples were compared by principal component old. The chemical solutions consisted of a ni- analysis (PCA), for each tree separately, and trous acid cleaved crab shell chitosan and a raw considering only monoterpenes which were PIIF extract from tomato plants dissolved in 0.05 present at levels of 0.5% or greater in each sam- M sterile phosphate buffer (pH 7) at the rate of 1 ple. This analysis was carried out with SAS soft- mg/ml. The fourth treatment was an injection of ware (SAS Institute). the sterile buffer alone. All inoculations consist- ed of 100 μl of chemical solution or a 5-mm plug In the present study, each tree species was of agar containing fungal mycelia. On each sam- represented by only one individual. However, pling occasion (3, 7 and 14 d after treatments), our aim was not to define the qualitative re-
peaks were labelled T1 to T4. β- sponse of these species but rather to compare the terpene composition of responding tissues phellandrene and limonene made up a sin- with that of unwounded tissues of the same gle peak, but P contorta contains mainly β- tree. Although there is a great deal of variation phellandrene (Raffa and Berryman, 1982b; in the monoterpene composition of conifer spe- Smith, 1983) and P ponderosa mainly lim- cies (see, for example, Cates and Alexander, onene (Smith, 1966). As an example, table 1982), variations between species are much greater to the extent that they can be used as II gives the monoterpene percentages for taxonomic characteristics (Zavarin et al, 1977). the response of the trees to fungus after Our study was designed to examine the ex- 14 d in comparison with unwounded tis- tremes of variability in the defensive reaction to sues. In this table, some major differences a pathogen and 2 elicitors. can be noticed between reactive and un- wounded tissue. Figure 1 allows a general qualitative comparison between treat- RESULTS ments, dates, tissues, and distance from the inoculation point for each tree. were filtered on silica gel, As the extracts The first axis of the PCA (fig 1) ex- oxygenated compounds were probably plained 58.6, 72.5 and 55.6%, the second lost from the samples. Thus, in the follow- axis 20.8, 13.1 and 21.8% and the third ing, the word "total monoterpene" refers axis 7.2, 6.9 and 9.9% of the variability, re- only to hydrocarbides which in fact corre- spectively in P contorta, P ponderosa and spond to most of the monoterpene com- P monticola. The first axis compared un- pounds. wounded phloem to reactive tissues and Concentrations of total monoterpenes can be called the reaction axis. In P pon- (hydrocarbides) in the different phloem derosa and P monticola, the second axis, and sapwood samples are presented in ta- with the first, separated unwounded sap- ble I. As we have only 1 tree per species, wood from reactive tissues. In P contorta, between-tree comparison of absolute val- unwounded sapwood was separated from ues is not possible. We therefore compare reactive tissues by the third axis. Thus, 3 values between treatments within trees. main types of monoterpene composition O clavigerum generally induced a higher were identified: unwounded phloem, un- accumulation of monoterpenes than the reactive tissues wounded sapwood, chemical treatments. In P ponderosa how- (phloem and sapwood together) (fig 1; ta- ever, the quantitative response to chitosan ble II). was often close to the response to the fun- gus. The terpene accumulations induced In all trees and in all 3 axes, reactive by PIIF and buffer alone were always less phloem could not be separated from reac- than that induced by the fungus. They tive sapwood. In addition, the composition were also less than that induced by chito- of reactive tissue did not appear very dif- san in P ponderosa (phloem and sap- ferent from that of unwounded sapwood, wood, 14 d after injury) and in the phloem with only small differences occurring in the of P monticola. concentration of some monoterpenes (ta- ble II). The changes in phloem composition Seventeen different peaks (not always induced by treatments are summarized in present) were obtained by gas chromato- figure 2, the response to fungus inocula- graphy when reactions were compared with unwounded tissue. One peak was tion after 14 d being chosen as being re- heptane, 12 were monoterpenes, and 4 presentative of all treatments (cf, fig 1). (probably monoterpenes) unidentified Monoterpene fractions changed differently
most distant from the in different tree species, except for β- parts of the reaction of inoculation or injection; eg, PIIF phellandrene limonene which always de- point + creased. Some reactive phloem samples (20-40 mm after 14 d) and buffer (20-40 had a monoterpene composition similar to mm after 14 d) from Lodgepole pine phloem. In addition to the 3 main types of unwounded phloem (fig 1),but always in
reactive sapwood and phloem samples re- monoterpene composition, some phloem samples appeared intermediate between from fungus inoculation after 14 d; sulting unwounded phloem and reactive tissues these samples had the highest values (fig 1).These also originated from parts of along axis 1. The 2 others included reac- the reaction distant from the point of inocu- tive phloem after 3 d or phloem treated by lation or injection; eg, chitosan (20—40 mm buffer, PIIF or chitosan, the value on axis 1 after 14 d) from Lodgepole pine, chitosan being lower than the previous subgroup. It (40-60 mm after 14 d) and buffer (20-40 possible, however, to recognize was not mm after 14 d) from Ponderosa pine, chit- such subgroups in P ponderosa and osan (20-40 mm after 14 d) and PIIF (20- P monticola. 40 mm after 14 d) from Monticola pine. In these intermediate samples, the ratio of INTERPRETATION AND DISCUSSION monoterpenes was similar to that of some unwounded phloem, the ratio of others was similar to that of reactive phloem, while others had a ratio intermediate be- Comparison between treatments tween the 2 categories of phloem. The fungus sample (40-60 mm after 14 The increase in total monoterpenes (hydro- d) in P ponderosa and the buffer sample carbides) after treatment is in agreement (20-40 mm after 14 d) in P monticola were with all previous results of phloem and atypical, not being separated from un- sapwood reactions in different conifer spe- wounded or reactive phloems by axis 1 but cies (Shrimpton, 1973; Russel and Berry- by axis 2. In fact, these 2 samples differed man, 1976; Raffa and Berryman, 1982a, b; from their respective group by 1 terpene Schuck, 1982; Miller et al, 1986; Delorme (β-pinene in P ponderosa and T3 in and Lieutier, 1990). We observed differ- P monticola) which had an "abnormally" ences in the responses of a given tree to high concentration. fungus, chitosan, PIIF or buffer, the former In the case of P contorta, it was possi- quantitative treatment inducing a higher ble to recognize 3 subgroups inside the re- accumulation of resins. Chitosan induced a active samples (fig 1).One consisted of all quantitative reponse comparable with that
pothesis is the case after beetle- fungus at- induced by the fungus, or higher than that induced by PIIF and buffer, only in some tack. cases. Our results are thus not in a com- This non-specificity, together with the plete agreement with those of Miller et al fact that we found sterile phosphate buffer (1986) and with our previous histological inducing the same qualitative response, observations in suggesting a possible role make it difficult to prove the role of chito- of chitosan as natural elicitor of defensive san and PIIF as natural elicitors. Moreover, metabolism in conifers (Lieutier and Berry- it favors the hypothesis that the elicitor 1988). man, originates from the tree. Nevertheless, Raf- fa and Berryman (1982a) found that mono- In the qualitative response, considering terpene composition of the reaction of note that situations where the monoter- we Abies grandis induced by inoculations with composition of the reactive tissues pene Trichosporium symbioticum Wright differed similar to that of unwounded tissues was significantly from uninjured phloem in or was intermediate, were all found in sam- terms of many compounds, while the com- ples collected far from the point of aggres- position of the reaction to mechanical sion. This allows us to consider these situ- wounding differed significantly from un- ations as either outside the reaction or wounded phloem by only one compound. being an incomplete reaction. This opinion Thus the reaction to fungal inoculation was is strengthened by the fact that the total qualitatively different than to mechanical concentration of monoterpenes in these wounding. As a consequence, our results cases was similar to that of unwounded tis- in pines do not agree with those of Raffa sues. On the contrary, in situations close and Berryman (1982a) in firs. to the point of aggression, all reactions clearly differed qualitatively from unwound- ed phloem. Moreover, they all had the Comparison between tissues same qualitative composition. Each of the trees responded in a different way. Howev- er, we can conclude that the responding The monoterpene composition of reactive tissues of a given tree all have the same tissue was similar for phloem and for sap- monoterpene composition irrespective of wood in all 3 species, but the composition treatment, and that this composition differs of constitutive tissues was different. Thus, from the unwounded tissues of the same the reaction state of tissues can be charac- tree. terized by a well-defined monoterpene The conclusion that the reaction is composition in a particular tree, and this non- specific for the agression supports the re- does not depend on the initial composition sults of Cook and Hain (1985), with Loblol- of the tissue. Shrimpton (1973) did not find ly pine and 2 strains of Ophiostoma minus, significant qualitative changes in the sap- and of Delorme and Lieutier (1990) with wood of P contorta in response to attacks Scots pine and 3 different fungi and 1 bee- by D ponderosa. This is explained by the tle species. In his histological studies, Mul- fact that reactive sapwood had a composi- lick (1977) suggested that response to inju- tion close to that of unwounded sapwood. ry is not in defense but rather to restore Shrimpton (1973) only found an increase tissues and block sapwood conduction, in β-phellandrene, which is contrary to our processes which are inherent, and not spe- results, but this may be due to between- cific as to the incitant. However, we need tree variation in the qualitative response, as observed by Schuck (1982) in the sap- more information to suggest if such a hy-
wood of P abies and by Delorme and Lieu- Berryman, 1977). In our experiments, how- tier (1990) in the phloem of P sylvestris. pines did not exhibit a consis- ever, the 3 tent differential response to O clavigerum. The existence of a defined monoter- Moreover, resistance of P ponderosa to pene composition of reactive tissues for a Dendroctonus brevicomis LeConte seems given tree, whatever the tissue, fits the hy- to be associated with limonene and myr- pothesis that neosynthesis is from cells dif- concentrations (Smith, 1966); limo- cene ferent from those responsible for the syn- is the most toxic monoterpene to this nene thesis of constitutive resin. This is in beetle, followed by Δ3-carene and myr- agreement with the ideas of Reid et al cene (Smith, 1965). In our P ponderosa (1967), Berryman (1969), Cheniclet et al samples, however, myrcene and Δ3- (1988) and Lieutier and Berryman (1988), increased while limonene de- carene who suggested that parenchymal cells creased. Raffa and Berryman (1982b) were responsible for neosynthesis. Our re- found that the percentages of α-pinene sults can be explained by the intervention and limonene increase while Δ3-carene of an elicitor whose "message" could be decreases in the response of P contorta to read by any target cell. Indeed, Cheniclet O clavigerum while in our experiment con- et al (1988) suggested that the neosynthe- centrations of α-pinene and Δ3-carene sis against a beetle-associated fungus in both increased. These results suggest that Pinus pinaster is preceded by the reactiva- between-tree variability in monoterpene tion of previously inactive cells. composition is the rule in the response of P contorta, as is also true for P abies (Schuck, 1982) and P sylvestris (Delorme Comparison between trees and Lieutier, 1990). Consequently, the qualitative monoter- In response to aggressors, each tree re- pene response of conifers does not seem sponded in a different manner. There were to be adapted to the species of aggressor. no between-tree similarities in the mono- Instead, the role of monoterpene in the in- terpene response. Indeed, only one ter- duced reponse of conifers to aggression is pene varied in the same direction (de- probably quantitative and dose-dependent, crease) in the 3 trees. The modification of as previously suggested (Raffa and Berry- the monoterpene ratio in response to O man, 1982a, b; Delorme and Lieutier, clavigerum was thus different in each tree 1990). although they are all hosts of D pondero- sae and O clavigerum. Berryman (1976), Bordasch Russel and ACKNOWLEDGMENTS (1977) and Raffa and Berry- and Berryman man (1982a) have reported that the de- This work conducted part of Ac- was as fense reactions of A grandis to T symbioti- CNRS-INRA tion Thématique Programmée higher relative contain No 4320. F Lieutier’s visit to the USA was sup- cum a ported by a grant from the Ministry of Industry concentration of the terpenes which are and Research of France. The authors thank Y least favorable to Scolytus ventralis Hiratsuka, Northern Forest Research Centre, LeConte, the beetle associated with Edmonton, Alberta, Canada, LA Hadwiger of the T symbioticum. Conversely, the monoter- department of plant pathology, and CA Ryan of penes least repellent to this beetle decline the Institute of Biological Chemistry, Washington in the defense reaction (Bordasch and State University, Pullman, for kindly providing
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