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Micro-Organism-Plant Interactions As Influencers of Secondary Metabolism in Medicinal Plants

Posted on: Sunday, 20 November 2005, 03:02 CST

By Bruni, R; Sacchetti, G

Over the last few decades, trends in herbal cropping have led to increased cultivation of medicinal plants, herbs and spices. With these new particular crops, however, unique diseases and pest problems are emerging. In terms of production, it is well known that plant pathologies can cause considerable losses in gross medicinal plant yield. Nevertheless, raw harvesting yield is not the sole key factor in determining the quality (and hence market value) of herbs intended for the phytotherapic market. The quality and therapeutic value of the products are, in fact, also determined by the abundance of specific secondary metabolites reputed responsible for the pharmacological activity of medicinal plants. As a direct consequence of its raison d'tre, it is generally known that secondary metabolism in plants can be altered in response to biotic and abiotic factors, including exposure of individual plants to pathologies. However, only in few cases has the extent of such changes been investigated. This review summarizes the known relationships between phytopathological status and secondary metabolism of medicinal plants, with a specific overview on its biotechnological relapses.

KEY WORDS: Plants * Micro-organisms * Metabolism.

Secondary plant metabolism, a source of active principles of interest for herbal medicine (and other fields), offers more degrees of freedom than modern-day manufacturing would like. In fact, while commercial manufacturing seeks, and requires, standardized processes which are as steadfast and repeatable as possible, nature responds with the instrument that best functioned throughout evolutionary adaptation: dynamic complexity. The characteristic biosynthetic pathways and physiological dynamics do not resemble interstate highways with just a few exits; they are more like an intricate, interdependent web of country roads where the specific needs of the moment make the pursuit of certain paths and certain destinations a priority to the detriment of those traveled under normal conditions. What one normally tends to see as a useful, substantially monolithic source of healthy substances is, in reality, an elaborate, nearly rhizomatic system of ecological communication, defense and interaction between the plant and its environment. As such it tends to adapt by changing in response to the stimuli it receives. If, on the one hand, these events can even lead to marked infraspecies variability in secondary metabolism, they also offer an interpretative key and this can prove useful in determining the ecological meaning of secondary metabolism. And yet, above all, they offer effective, plastic instruments for maximizing biotechnological processes (optimization of extraction, induction, production) both in vitro and in vivo.

In defining the quality of a herbal product (whether it is raw material or final processed product obtained through biotech or traditional means), one needs to identify, recognize and constantly monitor all those events that can modulate secondary metabolism. Culture and climate conditions, soil and genetic characteristics are the onto- and phylo-genetic factors that can usually affect the abundance and variety of the active principles. Hence they constitute the variables one works on to increase or optimize the production of those substances that determine the quality-and consequently the therapeutic and commercial value-of herbal products to be placed on the market. Nevertheless, as in the more traditional sector of cash crops (for food, fiber, etc.), the production yield and commercial value of the crop can also be affected by other biotic stress-related factors: phytopathological status and symbiotic interaction with various types of microorganisms (fungi, bacteria, viruses, phytoplasms).

Phytopathy and polar metabolites

Medicinal herbs are increasingly being cultivated side-by-side with traditional food plants; species which were once only found wild are now being cultivated and the increase in phytosanitary controls performed on herbs and medicinal plants has revealed a significant increase in the incidence of phytopathies which were once the realm solely of plants grown through traditional agriculture. Fungal and bacterial attacks, infections caused by phytoplasms and viruses-until a few decades ago a source of concern solely in intensive cultivation of food crops and ornamental plants- have begun to spread even to species grown for the herbal medicine and cosmetics markets. This is not only detrimental to the quantitative yield of such herbs but even affects the intrinsic quality of the final product.1

Beside the macroscopic damage that can be intuitively correlated with decreased raw material production yield (due to plant death, induced nanism and proliferation of axillary buds (witches' broom), missed flowering and/or fructification, decrease in the development of useful biomass, etc.), various phytopathies can also alter the morphology of structures that secrete and accumulate secondary metabolites and this, in turn, makes it necessary for them to fall back on synthetic pathways and to change both the chemical structure of the active principles as well as their absolute and relative abundance. This can lead to a significant drop in the pharmacognostic and organoleptic load of the herbal product and its therapeutic potential. The fact that biotic stress can lead to such variations is not surprising. The production of defensive, communications substances is, in fact, one of the primary purposes of plant secondary metabolism and the main reason for the existence of many of what we consider active principles.2 The rationale behind the final outcome of the plant-pathogen interaction is to modulate the physiological response of the species under attack. Moreover, in time, this interaction can follow different pathways, modulating the plant biochemistry in various ways.

Generally, the initial response is the onset of a cascade of passive defense mechanisms aimed at isolating the aggressor, segregating it in a specific area of the organism so as to prevent propagation from becoming systemic. This process occurs through the selective obstruction of vessels, thickening of the walls and apoptotic cell sacrifice, achieved for example through hyperproduction of phenols 3 and their subsequent polymerization or animation.4 A possible consequence is an increase in the amount of cinnamic, caffeic and ferulic polyphenols (monomeric or polymerized) in drugs obtained from diseased individuals and this has indeed been found in some medicinal plant species.5

In some cases this phenomenon translates into a true and proper inversion of normal biosynthesis. For example, when Allium species are the object of fungal and bacterial aggression, we find increased synthesis of cinnamic and ferulic derivatives with a corresponding decrease in the production of fiavonoids (often responsible for their pharmacological activity) in those individuals exposed to pathogenic microorganisms.6 On the contrary, in other cases, the phenols, segregated at the vacuolar level and released by cell lysis, undergo rapid oxidation and polymerization which decreases both their abundance and availability for extraction. This type of strategy appears quite widespread in nature 7 and can most likely be extended to medicinal plant species, particularly those, such as Hypericumperforatum, which accumulate polyphenols in specific sites adjacent to the epidermis (e.g. in zones which are sensitive to attacks). Recent studies 8 have, in fact, demonstrated the effects of a phytoplasm infection on the flavonoid and naphthodiantrone components of St. John's Wort, highlighting the marked effect pathogens have on the content of active principles. Indeed, healthy plants have a markedly higher total flavonoid content (12.55 mg/g) than found in infected plants (6.74 mg/g). In particular, rutin and isoquercitrin contents differ in healthy (4.69 mg/g and 3.5 mg/g, respectively) and infected (1.96 mg/g and 1.47 mg/g) plants. Moreover, less pseudohypericin is present in the infected plants (2.29 mg/g vs 1.41 mg/g) while the hypericin content does not appear affected by the presence of pathogens. On the other hand, the amount of chlorogenic acid increases considerably in the presence of pathogens (0.77 mg/g vs 1.56 mg/g). Although one is dealing with a phytoplasm infection, the trend appears in line with what has been described for fungal infections in Allium species: decreased flavonoids and increased phenolic derivatives. The specific mechanisms envisaged involve the inhibition of certain enzyme pools rather than an effective conversion of the substrates.

A different strategy, instead, involves the biosynthesis of phytoalexins or their precursors (phytoanticipins) as an active defensive response to microbiological aggression.9 In these cases, the biosynthetic reaction has more active overtones since the substances involved act directly on the pathogen, limiting replication or damaging its cell membranes.10 It must be pointed out that, in numerous cases, the active principles of commercial interest are de facto phytoalexins and the abundance in the plant matrix is directly dependent on the degree of exposure to pathogenic aggression. This is, for example, the case of stilbene resveratrol, one of the active principles responsible for the anti-oxidizing, healing-preventativeaction ascribed to red wine ( Vitis vinifera) and the by-products of its production chain. Its presence is greater in plants exposed to modest fungal attacks while it is drastically reduced under massive attacks as a consequence of the pathogen's enzymatic pool detoxifying effect that can overcome the plant's chemical defenses-the resveratrol-and thus infect the plant.11. 12 In recent decades, similar observations have been made regarding numerous classes of chemicals of interest for their medicinal or food properties: e.g. the isoflavones in Leguminosae and the glucosinolates and indolic alkaloids in Cruciferae.13 In particular, the extreme chemodiversity developed in these molecular structures- the fruit of ongoing dynamic fine-tuning of the relationship between plant and pathogenic microorganisms-clearly gives a glimpse of the capital importance the study of such relationships has in the identification and evaluation of new active principles. In fact, the study of the metabolites produced as a result of biotic stress makes it possible to expand the arsenal of bioactive substances, drawing on species which are not directly known as "medicinal". This was the case for the cystatin isolated from Castanea sativa 14 and the phenyl-phenalanon isolated from Musa acuminata.15

It must be noted that not only is this information of great importance because of its physiological and ecological relapses, but also because understanding this is extremely useful when one wishes to optimize the biotechnological processes used in the production of secondary metabolites with plant cells or tissues. Correct interpretation of this information makes it possible to identify strategies for dedicated extraction or to draw indications for hemisynthetic modification of natural molecular nuclei.

Despite the observations reported, there is very little specific information on medicinal species and even fewer studies have been performed that directly correlate phytopathological status with the quali-quantitative yield of active principles of commercial interest, perhaps because they require an interdisciplinary approach that correlates agronomy, genomics, physiology, pharmaceutical biology and phytochemistry. There have not been many publications on the effect phytopathologies have on the production of secondary polar metabolites (Table I) 6-10-12, 14-25 and no specific trends can be identified although these studies do indicate that they affect various classes of chemicals (alkaloids, phenols, saponins, triterpenes). Particular study has been focused on how Catharanthus roseus responds to phytoplasm infection. Using a metabolomic (^sup 1^H-NMR) approach an explanation has been found on how aggression leads to variations in both primary metabolism (increased synthesis of carbohydrates: glucose, saccharose) and secondary metabolism where an increase in the biosynthesis of polyphenols (chlorogenic acid) and indolic alkaloid precursors (loganic acid, secologanin) have been found with a consequent increase in the final levels of ajmalicin and vindolin.26 Using more traditional analytical techniques analogous results have been reported quantifying this increase at as much as 4 times the values found in healthy plants.18

Finally, species attacked by pathogens can present greater quantities of other substances and these play an important role as activators of the defensive response to infection; this is the case of salicylic acid which, even in medicinal species, peaks in the phase immediately following aggression.27,28

On the whole, the research performed has been sporadic and isolated. A true systematic, integrated handling of the question is clearly needed. A great deal is taken from the more prolific works on food and ornamental plant species of prime commercial interest.29 Moreover, these works are, in particular, limited to observations regarding the effects of viruses and phytoplasms.

TABLE I.-Influence of phytopathies on medicinal plants.

Phytopathies and apolar metabolites

The above is particularly true in the essential oil sector. In fact, while there is a great deal of information regarding the effects of pathologies of microbial origin, there is a relative dearth of data regarding the consequences of viral infections and phytoplasms on the extraction yield and chemical composition of essential oils. Indeed there is more evidence regarding the effects fungi and bacterial phytopathogens have on the composition of this type of secretion (Table II).3o-4i Terpenes, phenylpropanoids and other volatile compounds are of prime importance in a plant's defense against pathogens and can, therefore, easily be the object of variations as a result of both plant adaptation and pathogen- induced modifications that weaken the plant's chemical defenses.42

In many cases there are drastic decreases in the total yield of essential oils in plants attacked by fungi and bacteria as a result of the damage caused to the secretory and epidermal structures 36 and of the scarcity in development of secretory tissues. Frequently, however, the variations can also be qualitative as in the case of P. crispum infected by C. petroselini where a marked increase in myristicin is recorded (from 40% to 80%) against a net decrease in the biosynthesis of myrcene (dropping from 24% to 5%).37 Likewise, in Mentha spp., the synthesis of menthol and other terpenic alcohols can be inhibited to boost the production of related chetones and terpene hydrocarbons, although it is not clear whether this phenomenon is induced directly by the pathogen or by a fine-tuning of the plant's defenses.

Infections from phytoplasms and viruses appear to provide a remarkable effect. In this case, the limited development of the internal and external secretory structures and the repercussions the pathology has on the plant's physiological development lead to a dramatic decline in total yield and a uniform response pattern through qualitative alterations as has been described for various species. For example, a comparative study of essential oils obtained from Lavandula vera DC and from five different cultivars of Lavandula angustifolia Miller affected by alfalfa mosaic virus has highlighted a definite pattern. In all 6 cases, in fact, there was a decrease in yield (of up to 25%) and in oxygenated terpenes (including linalol) plus a net increase in esters (including linalil acetate). In particular, the value of the esters revealed peaks of +26% in L. vera and L. angustifolia cv. Abrialis, while the oxygenated terpenes were more highly affected in L. vera (-14%), Abrialis (-9%) and Super A (-8%). One must recall that the abundance, both absolute and relative, of linalol, linalil acetate and esters is one of the markers that defines the quality of lavender and French lavender. Besides these modifications, in some cases, a slight increase was observed in the abundance of sesquiterpenes (Super A, Maime) along with a decrease in the presence of hydrocarburic monoterpenes (Z. Vera, Maime, Grosso, Super A). The only cultivar which showed no significant qualitative variation was one that had no linalil acetate, thus suggesting that enzymatic esterification may come into play.43

TABLE II.-Influence of phytopathies on medicinal plants.

Previously, a significant variation in the gas chromatographic profile of essential oils obtained from anise hyssop (Agastache anethiodora Kuntze) affected by the cucumber mosaic virus was observed and studied. In particular, drastically reduced levels of estragol (-80.5%) and pulegon (-40.2%) were observed. At the same time, higher levels appeared in the first oil from limonene (+76.3%), field mint (+50.8%) and iso-field mint (+38.5%). Levels of monoterpene hydrocarbons and oxygenated moterpenes rose (from the "infected" to the "healthy" plants) from 3.07% to 13.35% and from 66.13% to 73-95%, respectively, while sesquiterpenes decreased from 9-7% to 5.49%. The oil extraction yield decreased by 80% and the hint of anise characteristic of the oil obtained from healthy plants was missing from the product generated by diseased plants.43

Finally, a different behavior was seen in Hypericum perforatum L. cv. Godet Derborance infected by phytoplasms belonging to the "stolbur" group.44 Again in this case the essential oil obtained from infected plants showed a marked decrease in distillation yield (-50%). In terms of chemical composition, as compared with oils obtained from healthy plants grown under the same conditions, the variations were mainly quantitative. Although the same compounds were identified, there was a marked fluctuation in the abundance of the principal components. It is also worth noting that this oscillation was seen in the entire class of compounds represented and not in individual components. In fact, the infected sample showed a monoterpenic fraction which was 51.25% lower and a greater abundance of sesquiterpenes (+12.7%). The modifications in β- caryophyllene (+15.5%), β-elemene (+15.7%) and germacrene D (+12.1%) were particularly evident.8 On the whole, the behavior of Hypericum and Lavender appear analogous to what was found in various essential oil plants under hydric stress or attack by microbial pathogens.39, 45 This behavior could stem from a lack of adequate nutrients at the floral tip as a result of obstruction in the vessels which, in turn, may be due both to the phytoplasms and the passive defenses of the plant itself. In fact, it is known that such pathogens tend to insert themselves in the phloem of the affected plant, blocking the vessels and consequently interrupting the transport of processed lymph.46

Conclusions

If, on the one hand, development of genetic fingerprinting techniques has made it possible to at least partially resolve the problem of identification of elusive pathologies such as viruses and phytoplasms and to obtain a taxonomic characterization of endophytic species, two problems of scientif\ic and commercial interest remain partially unresolved: to provide complete information on the possible modifications that are to be found in the final product as well as indirect indication of what type of biochemical relationship exists between microorganism and plant. In particular, we need greater knowledge on the seasonal repeatability of the observations and the existence of any species-specific responses. Moreover we need to be able to identify clear behavioral trends in the response of medicinal plants exposed to phytopathies from viruses or phytoplasms.

Although preliminary, the analyses reported through direct experimentation or through bibliographic indications support the hypothesis that these pathogens really do affect the yield and composition of essential oils and polar extracts of medicinal species. This suggests that secondary metabolism may be affected, thus leading to a subsequent drop in production yield and the commercial or therapeutic quality of the marketed product. At the same time, knowledge of a plant's defensive response and the modifications induced by the interaction between plant and microorganism provides an indispensable reservoir of information for optimizing elicitation and managing controls throughout the biosynthetic process in cell cultures.

Acknowledgements.-A special thanks goes to Prof. Maria Grazia Bellardi for kindly sharing her knowledge on plant virosis and phytoplasma diseases and to Mrs. Eileen Cartoon for the English translation.

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R. BRUNI1, G. SACCHETTI2

1 Section of Vegetable Biology and Botanical Garden Department of Evolutive and Functional Biology University of Parma, Parma, Italy

2 Department of Natural and Cultural Resources University of Ferrara, Ferrara, Italy

Address reprint requests to: Dr. R. Bruni, Dipartimento di Biologi\a Evolutiva e Funzionale-Sezione di Biologia Vegetale, Viale delle Scienze, 1-43100, Universit degli Stucli di Parma, Italy. E- mail: bruni@biol.unipr.it

Copyright Edizioni Minerva Medica Sep 2005

Source: Minerva Biotecnologica

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