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Keywords:

  • allelopathy;
  • chemical defences;
  • disease resistance;
  • metabolic diversity;
  • natural products;
  • roots;
  • secretion;
  • vesicle trafficking

Abstract

  1. Top of page
  2. Abstract
  3. I. Introduction
  4. II. Natural product trafficking and plant disease resistance
  5. III. Allelopathy
  6. IV. Conclusions and future directions
  7. Acknowledgements
  8. References

Contents

  • Summary 193

  • I. 
    Introduction 194
  • II. 
    Natural product trafficking and plant disease resistance 195
  • III. 
    Allelopathy 199
  • VI. 
    Conclusions and future directions 203
  • Acknowledgements 204

  • References 204

Summary

Plant-derived natural products have important functions in ecological interactions. In some cases these compounds are deployed to sites of pathogen challenge by vesicle-mediated trafficking. Polar vesicle trafficking of natural products, proteins and other, as yet uncharacterized, cargo is emerging as a common theme in investigations of diverse disease resistance mechanisms in plants. Root-derived natural products can have marked effects on interactions between plants and soilborne organisms, for example by serving as signals for initiation of symbioses with rhizobia and mycorrhizal fungi. They may also contribute to competitiveness of invasive plant species by inhibiting the growth of neighbouring plants (allelopathy). Very little is known about the mechanisms of release of natural products from aerial plant parts or from roots, although there are likely to be commonalities in these processes. There is increasing evidence to indicate that pathogens and symbionts can manipulate plant endomembrane systems to suppress host defence responses and facilitate accommodation within plant cells. The relationship between secretory processes and plant interactions forms the focus of this review, which brings together different aspects of the deployment of defence-related natural products by plants.


I. Introduction

  1. Top of page
  2. Abstract
  3. I. Introduction
  4. II. Natural product trafficking and plant disease resistance
  5. III. Allelopathy
  6. IV. Conclusions and future directions
  7. Acknowledgements
  8. References

Collectively, plants synthesize a diverse range of natural products (Wink, 1999). Within individual members of the plant kingdom, metabolic specialization is evident and it is common to find that the ability to produce specific compounds is restricted to particular plant lineages. These specialized substances are often referred to as secondary metabolites. Primary metabolites are associated with essential functions of ‘housekeeping’ metabolism. Historically, secondary metabolites have been regarded as dispensable. Loss of ability to produce secondary metabolites does not usually result in obvious detrimental effects on plant growth and development under laboratory conditions, although some of these compounds have been implicated in primary physiological functions such as auxin transport, regulation of seed longevity, and dormancy (D’Auria & Gershenzon, 2005). However, the laboratory is not a natural environment. Plants, unlike animals, are sessile and depend on their chemical repertoire to influence interactions with other organisms and with the environment. Many secondary metabolites have been shown to have important ecological functions and so have profound effects on the fitness of plants under natural conditions. These compounds serve as attractants for pollinators and seed-dispersal agents, and play important roles in interactions with beneficial microbes and other higher organisms. They also provide protection against pests, pathogens and abiotic stresses. Roots are a rich source of natural products, many of which are root-specific (Flores et al., 1999). Root-derived natural products can have marked effects on positive and negative interactions between plants and soilborne organisms, either by acting within the root, or following exudation or release into the rhizosphere. Natural products released from roots may also contribute to competitiveness of invasive plant species (Flores et al., 1999; Bertin et al., 2003; Inderjit & Duke, 2003; Bais et al., 2006). Thus it is evident that specialized metabolites have important functions. The term ‘natural product’ is therefore preferable to ‘secondary metabolite’.

The huge amount of metabolic diversity that we see in the plant kingdom is likely to be a consequence of niche colonization and adaptive evolution (Osbourn et al., 2003). The significance of natural products and of metabolic diversity for the survival of the plant kingdom is highlighted by the marked representation of genes with predicted functions in natural product synthesis in plant genomes (e.g. The Arabidopsis Genome Initiative, 2000; The International Rice Genome Sequence Project, 2005). For example, approximately 25% of known Arabidopsis genes are implicated in natural product synthesis. Furthermore, over 170 natural products from seven major classes of compound have now been reported in Arabidopsis– an almost fivefold increase over the past 10 yr (D’Auria & Gershenzon, 2005). Thus the collective genomic and biochemical evidence indicates that individual plant genomes are likely to have the hitherto unappreciated potential to produce diverse repertoires of metabolites. The list of Arabidopsis genes that have been demonstrated to be involved in specific natural product pathways is also growing rapidly, but is by no means complete. Many more genes and enzymes await characterization. Furthermore, despite rapid and recent advances in the elucidation of natural product synthesis in this model plant, there are significant gaps in our understanding of the ecological significance of the products of these pathways. We have direct information about ecological function for only a handful of Arabidopsis natural products. These include the UV-B protectants kaempferol (a flavonoid) and sinapoylmalate (a sinapate ester) (Landry et al., 1995; Ormrod et al., 1995; Booij-James et al., 2000), and the defence-related antimicrobial compounds camalexin (an indole sulphur phytoalexin) and sulphoraphane (a glucosinolate breakdown product), which provide protection against a range of plant pathogens (Glazebrook & Ausubel, 1994; Glazebrook et al., 1997; Tierens et al., 2001; Kliebenstein et al., 2005b) (Fig. 1). Even when the role of a particular natural product has been well defined within a specific ecological context, one should be wary of making generalizations. We know that there can be large variations in biological activity between structurally similar compounds within the same class, and that single compounds may have multiple context-dependent activities (Harborne & Williams, 2000). It follows that experiments that used narrowly defined parameters to assess the ecological functions of natural products may not be of broad relevance under natural conditions.

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Figure 1. Defence-related natural products that are produced by Arabidopsis. Kaempferol (a flavonoid) and sinapoylmalate (a sinapate ester) are UV-B protectants (Landry et al., 1995; Ormrod et al., 1995; Booij-James et al., 2000). Flavonoids may also act as negative regulators of auxin transport (Brown et al., 2001; Peer et al., 2004). The antimicrobial compounds camalexin (an indole sulphur phytoalexin) and sulphoraphane (a glucosinolate breakdown product) provide protection against a range of plant pathogens (Glazebrook & Ausubel, 1994; Glazebrook et al., 1997; Tierens et al., 2001; Kliebenstein et al., 2005b).

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This review considers the influence of plant-derived natural products on ecological interactions, with particular emphasis on trafficking and deployment of defence-related compounds. It highlights examples of compounds and/or secretion processes that have been visualized by cytological means. The first section focuses on natural products and plant disease resistance. The second focuses on allelopathy, in particular on phytotoxic compounds that are released from plant roots. It should be noted that the groups of compounds associated with pest/pathogen resistance and with allelopathy are not mutually exclusive, and that some compounds may fall into both categories. Very little is known about the mechanisms of release of natural products from roots and, as yet, there have been no direct tests of the roles of specific compounds in suppressing the growth of neighbouring plants. Nevertheless there have been important recent advances in this area, and it merits inclusion alongside the section on natural products and disease resistance, as both topics are ultimately concerned with deployment of defence-related and other signalling compounds by plants. We do not intend to provide exhaustive coverage of the huge amount of literature that has been published on phytochemicals and plant interactions, and we have not gone into the comprehensive body of work on volatiles. The reader is referred to other reviews for further information on these areas (Osbourn, 1996a, 1996b; Morrissey & Osbourn, 1999; Wink, 1999; Mansfield, 2000; Dixon, 2001; Kessler & Baldwin, 2001; Bouwmeester et al., 2003; Chen et al., 2003; D’Auria & Gershenzon, 2005; Kliebenstein et al., 2005a; Bais et al., 2006; Baldwin et al., 2006). Inevitably, this review focuses on abundant compounds that can be readily detected and analysed. However, it is important to bear in mind that these are not necessarily the most biologically active compounds in the plant repertoire, and that much remains to be discovered about the nature, synthesis and function of less abundant plant-derived natural products.

II. Natural product trafficking and plant disease resistance

  1. Top of page
  2. Abstract
  3. I. Introduction
  4. II. Natural product trafficking and plant disease resistance
  5. III. Allelopathy
  6. IV. Conclusions and future directions
  7. Acknowledgements
  8. References

1. Accumulation of vesicles at sites of pathogen challenge

Plants have a variety of means of defending themselves against attack by pests and pathogens. Induced defence responses that are triggered in leaves commonly involve cell wall reinforcement at the site of challenge by deposition of callose and lignin. In several cases, these defence responses have been shown to be accompanied by trafficking of antimicrobial compounds to the target site. The best known example for this comes from work with sorghum leaves, where pigmented vesicles containing antimicrobial flavonoids (3-deoxyanthocyanidins) (Fig. 2a) have been observed moving towards the site of attempted fungal infection in an incompatible interaction (Fig. 3a) (Snyder & Nicholson, 1990; Snyder et al., 1991). This example is particularly striking because of the vivid colour of the compounds. Similarly, the pigmented antimicrobial napthoquinones (shikonin derivatives) are secreted into the apoplast of boraginaceous plants such as Lithospermum erythrorhizon by a vesicle-mediated mechanism in response to fungal elicitation (Tabata, 1996; Yazaki et al., 2001, 2002). Accumulation of phenolic compounds at the challenge site is a common feature of cell wall reinforcement in plant–microbe interactions. Figure 3b shows vesicle-mediated delivery of autofluorescent phenolics in onion epidermis in response to challenge by the necrotrophic fungus Botrytis allii (Stewart & Mansfield, 1985; McLusky et al., 1999). These compounds, which are produced as a consequence of redirection of normal flavonoid and anthocyanin biosynthesis, are not antimicrobial but are thought to be secreted into the apoplast to provide precursors for cell wall reinforcement (McLusky et al., 1999). Cell wall reinforcements are generally accompanied by localized production of reactive oxygen species (ROS), which drive cell wall cross-linking, have antimicrobial activity, and are involved in defence-related signalling (Bradley et al., 1992; Levine et al., 1994). Reactive oxygen species have also been detected in vesicles that migrate to the site of infection; for example, vesicles containing hydrogen peroxide accumulate at pathogen-challenge sites in the barley–powdery mildew interaction (Hückelhoven et al., 1999) (Fig. 3c).

image

Figure 2. Examples of defence-related natural products that are produced by other plants: (a) 3-deoxyanthocyanidins, pigmented flavonoids produced by sorghum leaves in response to challenge with pathogens (R = H, apigenidin; R = OH, luteolinidin); (b) avenacin A-1, an antifungal triterpene glycoside that accumulates in the epidermal cells of oat roots and provides protection against attack by soil fungi; (c) 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA), a hydroxamic acid implicated in disease resistance and allelopathy in maize and wheat; (d) the allelochemical quinone sorgoleone, which is produced by sorghum root hairs; (e) the diterpene momilactone B, a compound that has been implicated in allelopathy in rice; (f) (–)-Catechin, the spotted knapweed allelochemical; (g) α-Tomatine, a tomato steroidal alkaloid implicated in plant defence.

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image

Figure 3. Vesicle trafficking in plants in response to pathogen challenge. (a) Pigmented vesicles containing antimicrobial flavonoids (3-deoxyanthocyanidins) moving towards the site of pathogen challenge in the epidermis of a sorghum leaf. The brown structure (app) is an appressorium (fungal penetration structure) produced by the pathogen Colletotrichum graminicola. Reproduced from Morrissey & Osbourn (1999), with permission of the American Society for Microbiology. (b) Vesicles containing autofluorescent phenolics accumulating at the cell wall (cw) in onion epidermis in response to challenge by the necrotrophic fungus Botrytis allii. Reproduced from McLusky et al. (1999), with permission of Blackwell Publishing. (c) Accumulation of vesicles containing hydrogen peroxide in a barley leaf epidermal cell at the site of attempted penetration of the powdery mildew pathogen Blumeria graminis f.sp. hordei. The vesicles have been stained with the histochemical 3,3,-diaminobenzidine (DAB). app, Appressorium. Reproduced from Hückelhoven et al. (1999), with permission of the American Society of Plant Biology. (d) Peroxisomes containing the PEN2-GFP fusion protein are targeted to powdery mildew (B. graminis f.sp. hordei) penetration sites and are visualized as green fluorescent vesicles. Fungal structures have been stained red with propidium iodide. app, Appressorium. Reproduced from Lipka et al. (2005), with permission of the American Association for the Advancement of Science. Bars, 10 µm (a,c,d); 100 µm (b).

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2. Mechanisms of vesicle-mediated trafficking

Trafficking of proteins has been studied intensively in plants and other organisms. In contrast, the mechanisms of vesicle-mediated transport of phytochemicals are not well understood (Lin et al., 2003; Grotewald, 2004). In protein trafficking, specific fusion of vesicles is mediated by recognition of SNAP (soluble N-ethylmaleimide-sensitive-factor association protein) receptor (SNARE) proteins in the vesicle and target membranes, respectively. This mechanism, which is controlled by Rab family GTPases, is also likely to be relevant for secretion of membrane complex polysaccharides synthesized in the Golgi (Uhr & Staehelin, 2001). In these cases the process is initiated in the Golgi, the cargo passes through the Golgi and the trans-Golgi network (TGN), and from there to the cell membrane. Lin et al. (2003) carried out experiments in which synthesis of readily visualized phytochemicals (yellow and green autofluorescent flavonoids and phenylpropanoids) in maize cells was induced using a regulatory gene under the control of an estradiol-inducible promoter. They observed two different kinds of subcellular trafficking. The yellow fluorescent compounds were targeted to the vacuole, where they accumulated as inclusions. In contrast, the green fluorescent compounds were secreted from the cell and accumulated in the cell wall. Trafficking of the green compounds was not affected by drugs that block protein secretion by promoting disassembly of the Golgi apparatus, suggesting that, in this case, the secretion process is distinct from that used for most proteins.

Are phytochemicals transported by SNARE-mediated processes or, as Lin et al. (2003) ask, have plants evolved novel trafficking pathways to accommodate their diverse range of metabolites? Evidence emerging from studies of disease-resistance mutants suggests that there may be overlap in the mechanisms employed for trafficking of proteins, membranes and natural products. Conserved SNARE proteins have been implicated in focal vesicle transport and vesicle fusion events associated with nonhost and basal resistance in Arabidopsis and barley [PENETRATION1 (PEN1) and REQUIRED FOR MLO RESISTANCE 2 (ROR2), respectively] (Collins et al., 2003; Assaad et al., 2004; Bhat et al., 2005). PEN1 and ROR2 belong to a subgroup of SNARE proteins known as syntaxins. ROR2 and a second barley disease-resistance component, REQUIRED FOR MLO RESISTANCE 1 (ROR1), were identified in a mutant screen as genes required for mlo-mediated broad-spectrum mildew resistance and also for basal penetration resistance (Freialdenhoven et al., 1996). The incidence of H2O2-containing vesicles of the kind shown in Fig. 3c is influenced by mutations at MLO, ROR1 and ROR2 (Collins et al., 2003). This evidence, along with the plasma membrane localization of the PEN1 and ROR2 syntaxins, and the demonstration that a SNAP protein that interacts with ROR2 is also required for disease resistance in barley (Collins et al., 2003), all implicate SNARE complex-mediated vesicle fusion events in disease resistance. It remains to be established whether trafficking of 3-deoxyanthocyanidins in sorghum leaves and shikimate derivatives in L. erythrorhizon are also dependent on SNARE protein-mediated mechanisms.

PENETRATION2 (PEN2), which is also required for nonhost resistance in Arabidopsis, was recently cloned (Lipka et al., 2005). This gene encodes an enzyme belonging to the family 1 group of glycosyl hydrolases, enzymes associated with hydrolysis of natural products in plants (D’Auria & Gershenzon, 2005). PEN2–green fluorescent protein (GFP) fusion protein localizes to mobile vesicle-like bodies that accumulate at fungal entry sites (Fig. 3d). Co-expression of fluorophore-tagged marker proteins for different subcellular compartments has identified these vesicle-like bodies as peroxisomes (Lipka et al., 2005). Mutation of presumed catalytic residues of PEN2 suggests that catalytic activity is required for disease resistance. It has been proposed that the congregation of PEN2-containing peroxisomes at fungal entry sites might provide a mechanism for the activation and release of a small molecule at high local concentrations, although it is not clear whether this small molecule would be cotransported in the peroxisomes, or whether it would encounter the PEN2 enzyme at the target site. In plants, PEN2 inhibits invasion by a diverse range of pathogens and so the product generated by this enzyme might be expected to exert broad-spectrum toxic activity, either directly or indirectly. PEN2 confers resistance to a wider range of pathogens than PEN1 (see above). This observation, plus the fact that pen1 pen2 double mutants are more susceptible than either of the single mutants alone, suggest that PEN1 and PEN2 represent components of two distinct resistance mechanisms. These pathogen-triggered focal processes, including PEN1 syntaxin and concentration of the PEN2 glycosyl hydrolase at fungal entry sites, are reminiscent of the polar secretion machinery in cytotoxic T-cells that is induced on T-cell receptor recognition, leading to targeted release of lytic proteins and killing of target cells (Lipka et al., 2005).

3. The broader significance of vesicle trafficking

PEN1, ROR2 and PEN2 are not required for specific disease resistance determined by gene-for-gene interactions, and are proposed to represent an ancient vesicle-associated defence response (Collins et al., 2003; Schulze-Lefert, 2004; Lipka et al., 2005). The Nicotiana benthamiana plasma membrane-localized SNARE protein NbSyp132 has recently been shown to be required for multiple forms of resistance to bacteria, including basal, gene-for-gene and systemic acquired resistance (SAR), suggesting a broader involvement of vesicle trafficking in diverse resistance mechanisms (M. Kalde, T. Nühse, K. Findlay and S. Peck, personal communication). NbSYP132 is likely to mediate secretion of antimicrobial pathogenesis-related (PR) proteins and/or antimicrobial compounds. These findings are consistent with those of Wang et al. (2005), who have shown that induction of plant protein-secretion machinery is required for SAR. Establishment of SAR in Arabidopsis is dependent on the key defence-response regulator NONEXPRESSOR OF PATHOGENESIS-RELATED GENES 1 (NPR1), which regulates expression of PR genes (Dong, 2004). Gene expression profiling experiments indicate that NPR1 also coordinately regulates expression of genes for the protein secretion machinery required for secretion of PR proteins (Wang et al., 2005), although it is not clear whether synthesis/secretion of natural products is concomitantly increased. Again, there are parallels with the mammalian immune system, where the secretory machinery in B cells is upregulated before the cells begin to secrete antibodies (Van Anken et al., 2003). If vesicle-anchored SNARE partners for PEN1, ROR2, NbSyp132 and other defence-related SNARE proteins can be identified, this should allow isolation of defence-related vesicles and systematic characterization of their cargo (Collins et al., 2003; M. Kalde, T. Nühse, K. Findlay and S. Peck, personal communication).

4. Constitutive chemical defences

The above are all examples of responses that are induced in plants following challenge with biotic or abiotic stresses. Many phytochemicals are synthesized by unchallenged plants as part of normal growth and development, and accumulate in specific tissues, organs or specialized structures (e.g. epidermal cells or glandular trichomes). Within these locations they are usually sequestered in the vacuole or other subcellular compartments (Morrissey & Osbourn, 1999). Sequestration implies the involvement of specific transport processes. For example, the defence-related triterpene glycoside avenacin A-1 (Crombie et al., 1986) (Fig. 2b) is synthesized by unchallenged oat plants and accumulates in the epidermal cells of the root tip, compartmentalized in the vacuoles (Osbourn et al., 1994) (Fig. 4). Avenacin A-1 has potent antifungal activity and confers resistance to a range of soil fungi (Bowyer et al., 1995; Papadopoulou et al., 1999; Haralampidis et al., 2001; Osbourn, 2003; Qi et al., 2004). In addition to forming a chemical barrier in the epidermal cell layer of the roots, it is also released into the soil around the roots at biologically active concentrations by unknown mechanisms (Carter et al., 1999). Avenacin A-1 is just one (very visual) example of a specialized metabolite that is produced constitutively in specific plant cells – in this case, the root epidermis.

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Figure 4. Localization of the defence-related triterpene avenacin A-1 in oat roots. (a) Cross-section of an oat root showing fluorescence of avenacin A-1 under UV illumination. This compound, which is the major UV-fluorescent component present in young oat roots, is localized in the epidermal cell layer (e) of the root tips. Bar, 50 µm. Reproduced from Osbourn (1996b), with permission of Elsevier. (b) Longitudinal view of oat root epidermal cells by confocal microscopy. Avenacin A-1 is localized in the vacuole (v). Bar, 10 µm.

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Other defence-related natural products may be stored as inactive precursors and are converted into biologically active antibiotics by plant enzymes in response to challenge. The glucosinolate–myrosinase system is a well known example of this. In Arabidopsis, glucosinolates can be stored in the vacuoles of specialized cells known as S-cells (Koroleva et al., 2000), while the enzymes that activate them (myrosinases) are sequestered in myrosin cells (Rask et al., 2000). Tissue damage caused by pest or pathogen attack leads to breakdown of compartmentalization and hydrolysis of glucosinolates to unstable aglucones by myrosinases. These unstable intermediates are then converted to toxic products such as isothiocyanates and nitriles (Wittstock & Halkier, 2002) (e.g. sulphoraphane, Fig. 1). Myrosinases, like PEN2, belong to the family 1 glucosyl hydrolase family (Xu, Z. et al., 2004). A connection between glucosinolates and SNARE proteins has emerged recently. The syntaxin AtVAM3 (Ohtomo et al., 2005) has been shown to be required for normal specification of myrosin cells (Ueda et al., 2006). The precise role of the AtVAM3 protein has not yet been established. However, it does not appear to be required for normal protein trafficking: Ueda et al. (2006) suggest that AtVAM3 may function as a negative regulator of cell differentiation and/or division during the formation of myrosin cells.

5. ATP-binding cassette (ABC) and multidrug and toxic compound extrusion (MATE) transporters

So far this review has focused on vesicle-mediated trafficking in leaves, as this is emerging as a major theme in plant–microbe interactions and, in at least some cases, has been linked with deployment of natural products. There are, however, other mechanisms of transport of defence-related natural products within and out of plant cells. These include ATP-binding cassette (ABC) and multidrug and toxic compound extrusion (MATE) transporters (Yazaki, 2005). The former involve directly energized primary transport, and the latter H+-gradient-dependent secondary transport. Both ABC and MATE transporters have been implicated in transport of flavonoids to the vacuole (Debeaujon et al., 2001; Goodman et al., 2004; Yazaki, 2005). Direct evidence for involvement of transporters in secretion of defence-related natural products has emerged from work with Nicotiana plumbaginifolia, where a plasma membrane-localized ABC transporter has been demonstrated to be required for secretion of sclareol and other antifungal terpenoids (Jasinski et al., 2001). Functional analysis has confirmed a role for this transporter in disease resistance (Stukkens et al., 2005). Further data linking trafficking of natural products with plant defence have been furnished by characterization of Arabidopsis pen3 mutants (Stein et al., 2006). These mutants, like the pen1 and pen2 mutants referred to above, were identified in screens for Arabidopsis mutants that are compromised in resistance to the barley powdery mildew fungus Blumeria graminis f.sp. hordei (i.e. affected in nonhost resistance). PEN3 has been cloned and characterized, and encodes a plasma membrane-localized ABC transporter (Stein et al., 2006). GFP-tagged PEN3 localizes to the plasma membrane in uninfected cells and concentrates at infection sites in response to pathogen challenge. These data suggest that the PEN3 transporter is involved in focused secretion of antimicrobial natural products into the apoplast at sites of attempted invasion. The pen3 and pen2 mutants have similar phenotypes, and genetic evidence suggests that the PEN3 and PEN2 proteins function in the same pathway. It is possible that the PEN2 enzyme is required for activation of nontoxic precursor metabolites prior to PEN3-mediated export of the active compounds into the apoplast. Metabolite profiling will confirm whether this is indeed the case.

III. Allelopathy

  1. Top of page
  2. Abstract
  3. I. Introduction
  4. II. Natural product trafficking and plant disease resistance
  5. III. Allelopathy
  6. IV. Conclusions and future directions
  7. Acknowledgements
  8. References

A second major area in which plant-derived natural products have been linked with defence is concerned with invasive plants and the rather controversial area of allelopathy. Invasive plants include species such as wild oat (Avena fatua) (Fig. 5a), a persistent weed of cereal crops; and spotted knapweed (Centaurea maculosa), an exotic species that is aggressively displacing native plants in the western USA (Fig. 5b). Plants like these pose a threat to agricultural systems and natural environments throughout the world. Establishing the factors that determine invasiveness is not trivial, as resource availability, the physical environment and interactions with native plants, animals and microbes (both detrimental and beneficial) will all have an impact on competitiveness (Shea & Chesson, 2002; Fitter, 2003). Invasive species may be particularly successful at establishing and spreading in alien environments because they have escaped competition from their natural neighbours. However, it has also been argued that the ability to produce allelopathic chemicals may contribute to their success (Whittaker & Feeney, 1971; Rice, 1984; Williamson, 1990; Callaway & Aschehoug, 2000; Inderjit & Duke, 2003). At this point it may be helpful to consider some definitions, as interpretations of the term ‘allelopathy’ vary.

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Figure 5. Invasive plant species. (a) Wild oats (Avena fatua) invading a wheat crop (photograph courtesy of the Agricultural Development and Advisory Service, Boxworth, Cambridge, UK). (b) Spotted knapweed (Centaurea maculosa), an exotic species that is aggressively displacing native plants in the western USA (photograph courtesy of Ray Callaway, University of Montana, Missoula, MT, USA).

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1. What is allelopathy?

The term ‘allelopathy’ was originally defined by the plant physiologist Hans Molísch as follows (Molísch, 1937; Inderjit & Duke, 2003):

‘The described phenomenon that one plant can influence another plays an important role in physiology, so it deserves an appropriate term. For this I coin the word allelopathy from the Greek words “allelon” meaning mutual and “pathos” meaning harm or affection.’

Note that this definition encompasses both positive and negative effects. The definition of allelopathy was subsequently broadened further by Rice (1984) to cover the effects of plants and their associated microorganisms on growth of other plants through the release of chemical compounds into the environment. As Inderjit & Duke (2003) point out, this extends the term to include almost all aspects of chemical ecology. The current working definition of the term ‘allelopathy’ tends to focus specifically on the negative effects of plant compounds – the suppression of the growth of neighbouring plants by the release of toxic compounds into the environment (Baldwin, 2003; Fitter, 2003; Inderjit & Duke, 2003).

2. Release of phytotoxic compounds from plants

Phytotoxic (potentially allelopathic) chemicals can originate from aboveground parts of plants and be released into the environment through foliar leaching, volatilization, residue decomposition and debris incorporation. However, many phytotoxic compounds of plant origin are produced by roots and are released directly into the soil (Inderjit & Duke, 2003). As emphasized previously, roots of different plant species produce a diverse array of natural products, and these compounds are often organ- and/or species-specific (Flores et al., 1999; Inderjit & Duke, 2003; Narasimhan et al., 2003; Walker et al., 2003a; Tan et al., 2004; D’Auria & Gershenzon, 2005; Bais et al., 2006). The production and/or release of these root-derived natural products is commonly constitutive, but may be induced by biotic or abiotic stresses (Lydon & Duke 1993; Bais et al., 2002; Bertin et al., 2003). Mechanisms of release of biologically active compounds from roots are not well understood, but are likely to include both diffusion and controlled release via transporters and vesicles (Neumann & Römheld, 2001; Bertin et al., 2003; Walker et al., 2003a). Improved methods for analysis of the natural product content of root exudates in Arabidopsis and other plant species are now opening up new opportunities for identification of root-derived compounds and for investigation of their synthesis, regulation, release and function (Fan et al., 1997; Narasimhan et al., 2003; Walker et al., 2003a, 2003b; Steeghs et al., 2004; Tan et al., 2004; Bais et al., 2006).

Various crop plants and weeds are known to release phytotoxic compounds into the soil at bioactive concentrations (Niemeyer, 1988; Minorsky, 2002; Inderjit & Duke, 2003). Once outside the plant, the biological activity of chemicals that are released into the rhizosphere may be altered by chemical oxidation, microbial degradation or immobilization by irreversible binding to soil particles (Bertin et al., 2003). Assessment of the effective concentration of individual phytotoxic chemicals in the rhizosphere, and of the impact of these compounds on plants, therefore represents a substantial challenge (Weidenhamer, 2005). To date there are few cases in which specific compounds have been identified as allelopathic agents (Duke et al., 2001), and there are no definitive tests of the contribution of specific compounds to the ability of invasive plant species to suppress the growth of susceptible plants (Baldwin, 2003). Nevertheless, considerable progress has been made in various aspects of allelopathy research. Some examples of this are outlined below.

3. Allelopathy in cereals

Within the past 50 yr, weed management has become almost completely dependent on herbicides (Duke et al., 2001). The development of crops with enhanced allelopathic properties, through traditional breeding or genetic modification, has potential for controlling weeds and improving yield and may represent a promising alternative to the application of chemicals (Duke et al., 2001; Minorsky, 2002). Examples of natural products that have been implicated in allelopathy in cereals include the benzoxazinoids, defence-related compounds that occur constitutively as glucosides in certain members of the Gramineae and in some dicots. The primary hydroxamic acid in rye is 2,4-dihydroxy-1,4-benzoxazin-3-one (DIBOA), while its methoxy derivative 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA) (Fig. 2c) is predominant in maize and wheat (Barnes & Putnam, 1987; Niemeyer, 1988; Sicker et al., 2000; Wu et al., 2001a). These compounds have also been associated with chemical defence against pests and pathogens (Niemeyer, 1988; Gierl & Frey, 2001). The allelochemical quinone sorgoleone (Fig. 2d) is released from sorghum roots (Duke et al., 2001), while the diterpene momilactone B has been proposed to act as an allelopathic compound in rice (Fig. 2e) (Kato-Noguchi et al., 2002). This list is by no means exhaustive, and a variety of other compounds including phenolics have also been implicated in allelopathy in these and other cereals (Minorsky, 2002; Inderjit & Duke, 2003; Kong et al., 2004). Oats are particularly invasive when compared with other cereals. Phenolics and l-tryptophan have been identified as potential allelopathic agents in this cereal (Guenzi & McCalla, 1966; Guenzi et al., 1967; Schumacher et al., 1983; Pérez & Ormeño-Nuñez, 1991; Kato-Noguchi et al., 1994a, 1994b; Fay & Duke, 1977). The antimicrobial triterpene glycoside avenacin A-1 (Fig. 2b) is also released from oat roots into the soil (Carter et al., 1999). Triterpene glycosides have a diverse range of biological activities, and may contribute to allelopathy (Hostettmann & Marston, 1995).

Characterization of the genes and enzymes required for the synthesis of compounds that are implicated in allelopathy should allow the biosynthetic pathways to be manipulated, so enabling direct tests of the contribution of these compounds to suppress the growth of weeds and other plants in laboratory-, glasshouse- and field-based experiments. It may then be possible to use this knowledge to enhance production of allelochemicals in plants that already produce them, or to transfer the ability to synthesize these allelopathic compounds into other important crop species (Duke et al., 2001; Bertin et al., 2003; Dayan et al., 2003; Wilderman et al., 2004; Xu, M. et al., 2004; Yang et al., 2004a, 2004b). The genes for the pathway leading to the synthesis of DIBOA and DIMBOA have been cloned from maize (Frey et al., 1997; Sicker et al., 2000; Gierl & Frey, 2001). Corresponding mutants are available for a number of these genes, although the effects of mutation on the ability to suppress other plants have not been reported. It is intriguing that the genes for the DIBOA/DIMBOA and avenacin biosynthetic pathways exist as module-like clusters in maize and oats, respectively (Frey et al., 1997; Papadopoulou et al., 1999; Haralampidis et al., 2001; Osbourn et al., 2003; Qi et al., 2004). Terpene synthases involved in the synthesis of rice momilactones also exist as functional clusters (Wilderman et al., 2004). The reasons for this clustering are unclear. Mechanisms that act to disperse genes (translocation, inversion and unequal crossing over) are well known in eukaryotes, and genes associated with other well characterized secondary metabolic pathways, such as anthocyanin biosynthesis, are generally unlinked. Horizontal transfer of gene clusters from other organisms cannot be the sole explanation for the existence of the clusters, as there is clear evidence of recruitment of cluster components from plant primary metabolism (Gierl & Frey, 2001; Qi et al., 2004). It seems that, in some cases, physical clustering of genes for the synthesis of protective chemicals is favoured because it will enable pathway genes to be inherited as a functional unit (Qi et al., 2004). Clustering also has the potential to facilitate coordinate regulation of gene expression at the chromatin level, a factor that may be important for stringent regulation of the synthesis of potentially phytotoxic plant compounds (Qi et al., 2004). The intriguing question of how these gene clusters came into being remains to be addressed. Regardless of this, the idea of transferring these chemical defence clusters between species via classical or GM-based approaches is tantalizing.

Germplasm of various crop plants, including barley, wheat, rice, sorghum, maize and oats, has been screened for allelopathic potential, and significant variation has been identified in each of these crops (Lovett & Hoult, 1995; Nimbal et al., 1996; Fay & Duke, 1997; Wu et al., 2000, 2001b; Minorsky, 2002; Olofsdotter et al., 2002; Sánchez-Moreiras et al., 2003). Although commercial crops with enhanced allelopathic potential have not yet been developed, these findings provide opportunities for improving allelopathy in rice through conventional breeding strategies by using marker-assisted selection.

A general caveat associated with the development of crop plants with enhanced allelopathic traits is that they are likely to be more competitive in natural ecosystems, although it may be possible to circumvent this problem by employing appropriate agronomic practices in order to minimize the risk of escape (Duke et al., 2001).

4. Sorghum and sorgoleone

Sorghum leaves synthesize and secrete red pigmented anthocyanidins as part of the induced defence response (Section II). The roots of sorghum produce a different pigmented natural product, the quinone sorgoleone (2-hydroxy-5-methoxy-3-[(8′z,11′z)-8′,11′,14′-pentadecatriene]-p-benzoquinone) (Fig. 2d), which is exuded from the root hairs in golden brown droplets (Nimbal et al., 1996; Czarnota et al., 2001; Czarnota et al., 2003) (Fig. 6a). Synthesis of sorgoleone is tissue-specific and occurs only in the root hairs (Czarnota et al., 2001; Yang et al., 2004b). Sorghum species are often used as cover crops because of their ability to suppress weeds, and evidence suggests that sorgoleone may contribute to this suppressive activity (Duke et al., 2001). Sorgoleone has potent phytotoxic activity and inhibits the germination and growth of susceptible weeds at concentrations as low as 10 µm (Einhellig & Souza, 1992; Nimbal et al., 1996). Root hairs can represent up to 80% of the root surface of cultivated crops, so release of sorgoleone into the rhizosphere is likely to be favoured (Dittmer, 1937; Yang et al., 2004b). Indeed, sorgoleone concentrations in soil under sorghum crops can easily reach 10–100 µm (Netzley et al., 1988). The compound has been reported to have a variety of effects on plant metabolism, including inhibition of photosynthesis and respiration (reviewed by Inderjit & Duke, 2003; Hejl & Koster, 2004).

image

Figure 6. Secretion of sorgoleone. (a) Droplets containing sorgoleone exuding from root hairs. Bar, 50 µm (b,c) Transmission electron micrographs showing longitudinal sections of Sorghum root hairs. Root exudates (stained black) are deposited between the plasma membrane and the cell wall. Bars, 1 µm. CW, cell wall; ER, endoplasmic reticulum; Mt, mitochondria; S, root exudates; So, root exudates at various stages of secretion; V, vacuole. Reproduced from Czarnota et al. (2003), with permission of University of Chicago Press.

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Characterization of the sorgoleone biosynthetic pathway and cloning of the cognate genes are currently under way (Duke et al., 2001; Dayan et al., 2003; Yang et al., 2004a, 2004b). The precise mechanism of secretion of sorgoleone is not understood, although a detailed study of the anatomy of sorgoleone-secreting root hairs suggests that this process is likely to involve vesicle trafficking (Czarnota et al., 2003). Transmission electron microscope studies suggest that the compound is synthesized in association with the ER, transported through the root-hair cells in lipophilic vesicles, then deposited between the plasma membrane and the cell wall (Czarnota et al., 2003) (Fig. 6b,c). Although these studies did not involve specific detection of sorgoleone, this compound and its analogues comprise approx. 90% of the content of root hair exudate. It is therefore reasonable to assume that the globules that are visible in Fig. 6b,c contain sorgoleone.

5. Spotted knapweed and (–)-catechin

Recent data from work with spotted knapweed (C. maculosa) has provided a solid base of evidence linking production of a specific root-derived compound with allelopathy, and has made inroads into addressing the mechanism of toxicity of this compound to susceptible plants. Vivanco and coworkers have identified the flavonol (–)-catechin (Fig. 2f) as the primary phytotoxic compound that is released into the soil from the roots of spotted knapweed (Bais et al., 2002, 2003). Although spotted knapweed roots exude a racemic mix of (±)-catechin, only (–)-catechin is phytotoxic. Interestingly, (+)-catechin (but not (–)-catechin) has antimicrobial activity towards root-infecting pathogens, leading to speculation that the enantiomers may have complementary functions in root protection (Bais et al., 2002); the observation that (±)-catechin also appears to play an autoinhibitory role in regulating conspecific seedling establishment is intriguing (Perry et al., 2005). The mechanism of release of these compounds into the soil is not yet known.

Recent experiments have provided insights into the mechanism of phytotoxicity of (–)-catechin. (–)-Catechin inhibits the germination and growth of other sensitive plant species at concentrations that occur naturally in soils, and causes cell death when applied to roots of Arabidopsis and the sensitive knapweed species Centurea diffusa at concentrations of 100 µg ml−1 (300 µm). Further analysis has revealed that (–)-catechin-induced cell death is preceded by production of ROS and a transient elevation in Ca2+ levels (Bais et al., 2003). These data suggest that ROS-induced Ca2+-dependent signal transduction triggers cell death. The tools and resources available for Arabidopsis now offer an opportunity to dissect the mechanism of (–)-catechin-induced cell death in more detail.

6. Living together

Plant species that normally coexist together are likely to have developed mechanisms of tolerating each other's toxins (Fitter, 2003). Examples are known in which resistant species detoxify allelochemicals by oxidation, carbohydrate conjugation or sequestration (Wieland et al., 1998; Sicker et al., 2001; Inderjit & Duke, 2003). Weir et al. (2006) suggest that resistance to the spotted knapweed allelochemical (±)-catechin may be conferred by increased secretion of oxalate, which is believed to protect against damage incurred by ROS. A number of allelochemicals have toxicity rivalling that of synthetic herbicides (Weidenhamer, 2005). As resistance in plants evolves rapidly in response to man-made herbicides (Powles & Holtum, 1994), resistance to allelochemicals of exotic invaders may therefore also be expected to evolve rapidly in native plant populations (Callaway et al., 2005). Unravelling the significance and consequences of production of allelochemicals by plants, and putting this into the broader context of plant competition and plant–microbe interactions, represents a substantial challenge for the future.

IV. Conclusions and future directions

  1. Top of page
  2. Abstract
  3. I. Introduction
  4. II. Natural product trafficking and plant disease resistance
  5. III. Allelopathy
  6. IV. Conclusions and future directions
  7. Acknowledgements
  8. References

Exciting trends are emerging from different but interconnected strands of research in the fields of plant–microbe interactions and allelopathy. From studies of plant disease, it is becoming increasingly clear that host cells undergo major cytoskeletal reorganization in response to challenge with pathogens, and that these events are often accompanied by site-directed secretion of proteins and/or natural products (Heath et al., 1997; Škalamera & Heath, 1998; Schulze-Lefert, 2004; Takemoto & Hardham, 2004; Lipka & Panstruga, 2005; Koh & Somerville, 2006). At the moment we do not know whether trafficking of defence-related proteins and natural products is mediated by the same or different kinds of vesicles. Isolation of the vesicles, and characterization of the nature of these structures and of their cargo, will help to resolve this question. The Arabidopsis genome is rich in genes that are predicted to encode SNARE proteins when compared with other nonplant eukaryotes (Sanderfoot et al., 2000; Schmelzer, 2002; Surpin & Raikhel, 2004). This representation is likely to reflect the complexity of plant endomembrane systems, about which we still have a huge amount to learn.

Collectively, the emerging data have implicated focused vesicle trafficking in a broad range of different disease-resistance mechanisms. It has been proposed that induction of pathogen-triggered cell polarization represents an ancient vesicle-associated resistance response, and that biotrophic pathogens such as the barley powdery mildew fungus may have evolved mechanisms of subverting this resistance machinery for pathogenesis by coaxing the host to form specialized invaginated membranes around the fungal feeding structures (haustoria) (Schulze-Lefert, 2004; Koh et al., 2005). These fungi may therefore be able to manipulate the endomembrane systems of their hosts. More recently, the Pseudomonas syringae effector protein HopM1 has been shown to interfere with an Arabidopis protein implicated in vesicle trafficking, suggesting that bacterial pathogens also target cell wall-associated host defence mechanisms (S.-Y. He, personal communication). These experiments were carried out on Arabidopsis leaves. In an interesting twist, it turns out that the ability of P. syringae to infect Arabidopsis roots is dependent, in part, on effector-mediated suppression of production of uncharacterized root-derived antimicrobial metabolites (Bais et al., 2005).

There are intriguing parallels between the changes in host membrane systems outlined above and those that take place during colonization of roots by symbionts (mycorrhizal fungi or symbiotic bacteria), where cytoskeletal rearrangements also occur in response to challenge followed by accommodation of the symbiont within structures bounded by specialized host plasma membranes. Symbiosis is likely to predate pathogenesis, again suggesting that pathogens have recruited existing plant machinery in order to colonize their hosts (Parniske, 2000). This is supported by comparative transcriptomics data indicating substantial overlap in the response of roots to colonization by symbionts and biotrophs (Sesma & Osbourn, 2004; Güimil et al., 2005). The significance of SNARE proteins for the establishment of symbiosis remains to be addressed, although a syntaxin has been identified as a component of the symbiosome membrane in nitrogen-fixing root nodules (Catalano et al., 2004).

Symbioses are initiated by the release of plant-derived natural products into the rhizosphere. In the case of rhizobia these signals are flavonoids (Long, 1996), while strigolactone (5-deoxy-strigol) has recently been shown to stimulate hyphal branching of mycorrhizal fungi (Akiyama et al., 2005). How are these compounds secreted from roots? Is there overlap with mechanisms used to secrete allelochemicals? Have ancient vesicle-trafficking processes been exploited by symbionts to enable accommodation within host cells? Intensification of research effort in these areas is likely to yield some very important insights.

A major challenge in plant biology is to understand the factors that determine plant invasiveness and competitive ability. This is a huge and complex area that encompasses many aspects in addition to the potential contribution of allelochemicals. The generation of plant mutants with altered ability to produce natural products that have been implicated in allelopathy should now allow direct tests of the roles of individual compounds and pathways in suppression of susceptible plant species in glasshouse and field experiments. These experiments, coupled with unbiased, genetics-based approaches to mapping and characterizing loci that contribute to allelopathic potential and competitiveness, will provide a fuller picture of the relationship between plant-derived natural products and suppressive ability.

In conclusion, we are certainly making progress in exploring the tip of the metabolic iceberg in plants, and in learning about how this chemical repertoire is deployed for plant defence. In symbiosis, deployment of plant signalling compounds is the first step in a dialogue. We have to be careful, then, not to assume that deployment of individual compounds into the apoplast or the environment is the end of the story. There are certainly indications that plant-derived natural products are involved in complex interplays between plants and other organisms. For example, various fungal pathogens of tomato hydrolyse sugars from the tomato steroidal glycoalkaloid α-tomatine during infection (Morrissey & Osbourn, 1999). Superficially these modifications represent simple detoxification events. However, there is more to it than that, since as α-tomatine hydrolysis products are able to suppress induced plant defence responses (Bouarab et al., 2002; Ito et al., 2004). Significantly, the aglycone of α-tomatine (but not α-tomatine itself) has been shown to inhibit sterol biosynthesis in yeast (Simons et al., 2006). A key question now is whether processing of α-tomatine in the plant leads to interference with plant sterol metabolism, with associated consequences for induced plant defence mechanisms.

Dialogues (or perhaps more appropriately multiple conversations) are likely to be even more complicated in the soil. As already highlighted, roots are a rich source of metabolic diversity. Natural products that are released from roots into the rhizosphere are available for modification by soil microbes and other organisms. This will lead to an even greater array of metabolic diversity. Understanding the fate and biological activity of this spectrum of compounds once they are released into the environment represents a formidable challenge. There is extensive natural product networking going on in nature.

Acknowledgements

  1. Top of page
  2. Abstract
  3. I. Introduction
  4. II. Natural product trafficking and plant disease resistance
  5. III. Allelopathy
  6. IV. Conclusions and future directions
  7. Acknowledgements
  8. References

We would like to thank Helen Ghirardello for assistance with manuscript preparation, Scott Peck and Sheng-Yang He for permission to refer to unpublished work, and colleagues for helpful comments. A.O. and B.F. receive funding from the BBSRC. A.O. and F.J. would also like to acknowledge the support of the Society in Science Foundation.

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  5. III. Allelopathy
  6. IV. Conclusions and future directions
  7. Acknowledgements
  8. References
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