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1、ReviewTRENDS in Ecology and Evolution Vol.20 No.11 November 2005Linking aboveground andbelowground interactionsvia induced plant defensesT. Martijn Bezemer1,2,3 and Nicole M. van Dam31Laboratory of Nematology, Wageningen University and Research Centre, PO Box 8123, 6700 ES Wageningen, the Netherland
2、s2Laboratory of Entomology, Wageningen University and Research Centre, PO Box 8031, 6700 EH Wageningen, the Netherlands3Netherlands Institute of Ecology (NIOO-KNAW), PO Box 40, 6666 ZG Heteren, the NetherlandsPlants have a variety of chemical defenses that often increase in concentration following a
3、ttack by herbi-vores. Such induced plant responses can occur above-ground, in the leaves, and also belowground in the roots. We show here that belowground organisms can also induce defense responses aboveground and vice versa. Indirect defenses are particularly sensitive to interference by induced f
4、eeding activities in the other compartment, and this can disrupt multitrophic inter-actions. Unravelling the involvement of induced plant responses in the interactions between aboveground and belowground communities associated with plants is likely to benefit from comprehensive metabolomic analyses.
5、 Such analyses are likely to contribute to a better understanding of the costs and benefits involved in the selection for induced responses in plants.Despite being separated in space, aboveground and belowground organisms influence each other, either directly, for example via predation of soil insec
6、ts by predators that live aboveground, or indirectly, via changes in biomass and the nutritional quality of host plants 13. As primary producers that have belowground (roots) and aboveground (leaves, stems and flowers) organs, plants are an important link between most life above and below ground 4.
7、In response to the many organisms that feed on them, such as arthropods, nematodes, and pathogenic microorganisms 5, plants have evolved a variety of chemical defenses to repel, deter or kill their enemies 6. These defense strategies can be divided into direct defenses (directly impacting the enemy;
8、 e.g. trichomes and toxins; see Glossary) and indirect defenses (which include compounds that enable plants to recruit carnivores or enhance their effectiveness; e.g. extrafloral nectar and volatiles) (Box 1). Rather than maintaining high (con-stitutive) levels of these indirect defense chemicals, m
9、any plants increase their levels of defense only when they are attacked. Such induced defenses (Box 1) have been studied intensively, primarily in an aboveground context 6,7. Roots, however, also have direct and indirect induced defenses 8,9. Because many induced defenses are not restricted to the s
10、ite of attack, but result instead inCorresponding author: Bezemer, T.M. (martijn.bezemerwur.nl).Available online 29 August 2005systemic defense induction throughout the plant, root feeders can change shoot defense levels, and vice versa.In this themed issue of TREE, Bardgett et al. 10 review the tem
11、poral dynamics of soil communities and the implications for ecosystem functioning, whereas De Deyn and Van der Putten 11 discuss linkages between above-ground and belowground biodiversity. Here, we focus on the individual interactions that occur between plants and higher trophic levels and evaluate
12、how induced plant defense responses can mediate interactions between aboveground and belowground organisms.Recently published studies that explicitly analyzed root- and shoot-induced responses in different plant species show that root-induced responses in particular affect the effectiveness of shoot
13、-induced defense responses and that this can disrupt aboveground multitrophic interactions. Directly, because changes in plant quality can influence, via the herbivore, organisms at higher trophic levels 12, and indirectly via the efficiency of predation or parasitization. Although studies thus far
14、have focused specifically on changes in well-known plant defense compounds, such as terpenoids or glucosinolates, induced responses can also affect the levels of nutritional compounds (e.g. sugars and amino acids) or other compounds (e.g. hormones) that are involved in induced defense. A new technol
15、ogy, metabolomics, has recently emerged that enables a comprehensive analysis of all theGlossaryConstitutive defenses: plant defenses that are always expressed, independent of herbivore or pathogen attack.Direct defenses: plant structures, such as trichomes, or compounds, such as toxins, deterrents
16、or digestibility reducers, that directly reduce the preference or performance of a herbivore or pathogen.Indirect defenses: enable the plant to recruit carnivores or enhance the efficiency with which carnivores attack herbivores; can be plant-induced compounds for attraction (e.g. volatiles), plant-
17、provided food supplements for facilitation (e.g. extra-floral nectar), or plant structures for providing shelter to carnivores (e.g. domatia).Induced defenses: changes in the plant following herbivore damage or pathogen infestation that benefit the plant by decreasing herbivore or pathogen performan
18、ce or preference.Parasitoids: insects that lay their eggs in or near other invertebrates, usually other insects, and whose larvae feed on the host and eventually kill it. Only larval stages are parasitic, whereas adults are free living.Systemic induction: herbivore- or pathogen-induced changes in pl
19、ant defense levels in unchallenged plant 0169-5347/$ - see front matter Q 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2005.08.006618ReviewTRENDS in Ecology and Evolution Vol.20 No.11 November 2005Box 1. What are induced plant defenses?Induced plant responses occur in most studied plan
20、t species and are produced in response to a wide variety of organisms, such as bacteria, viruses, nematodes, insects and mammalian herbivores 6,7. The defense response can be limited to the site of attack (local induction), or can be expressed in remote, undamaged plant parts (systemic induction). T
21、he defenses range from structural defences, such as thorns and trichomes, to toxic chemical compounds, such as nicotine and terpenoids 6,7.The compounds that are produced in response to herbivory can either have a direct effect on the attacker itself (e.g. toxins or digestibility reducers), or serve
22、 as indirect defenses by attracting the natural enemies of the herbivores 59. Natural enemies of herbivores, such as parasitoids or predators, can be attracted to the plant by providing sugar (Box 3) or by specific volatile organic compounds (VOC) that plants emit in response to herbivore feeding. T
23、he volatile bouquet depends not only on the plant species involved, but also on the species of herbivore that is causing the damage 60. Components in the excretions or saliva of the herbivore, such as enzymes or amino acid conjugates, can trigger specific signaling cascades in the plant, resulting i
24、n the emission of a specific VOC blend that can attract a specific enemy to the herbivore 61,62.Plant hormones have an important role in shaping induced responses. Jasmonic acid (JA or its methylated form, MeJA), salicylic acid (SA or MeSA), ethylene (ET), and abscisic acid (ABA), are all involved i
25、n induced responses against insects or pathogens, and can change in response to other stresses, such as drought and competition for nutrients 25,63. Although JA is generally associ-ated with induced responses against chewing herbivores, and SA with responses against pathogens and spider mites 60,64,
26、 the pathways that are triggered by these hormones are not independent. In some species, such as Rumex spp., JA and SA-induced responses overlap 65, whereas in Lycopersicon esculentum tomato plants, SA-induced responses counteract the expression of JA-induced responses 64. ET and ABA are thought to
27、act as modulators, thus enabling the plant to fine-tune its response to its attacker 66,67. Transport of hormones or signaling molecules via the vascular system (e.g. JA and SA), or via the air (e.g. MeJA, MeSA and ET), can cause the systemic induction of defenses in undamaged parts of the plant 35.
28、metabolites of a plant 13 (Box 2). Future aboveground belowground studies should take advantage of this tech-nology, which could significantly improve our under-standing of the role of induced defenses in the complex multitrophic interactions associated with plants.Effects of belowground organisms o
29、n aboveground plant defenseWhen exposed to belowground organisms, plants can show several direct (e.g. production of toxins) and indirect (e.g. release of volatiles) defense responses in the foliage that can affect aboveground herbivores and disrupt multitrophic interactions.Direct defenseA range of
30、 belowground organisms that are directly associated with plant roots (e.g. insects, nematodes, root pathogens and mycorrhizal fungi) influence the concen-tration of plant defense compounds, such as terpenoids, glucosinolates or phenolics, in aboveground plant tissues 1421. Because these compounds fr
31、equently have a negative effect on aboveground herbivores, the action of belowground organisms can influence the performance of aboveground organisms via changes in plant defense levels. Increases and decreases in aboveground defenseBox 2. Metabolomics as a tool for ecologists?Metabolomics has been
32、defined as an unbiased way to identify and quantify comprehensively all metabolites of an organism 68, and is closely related to other fields in functional genomics, such as pro-teomics (the comprehensive analysis of all proteins in an organism) and transcriptomics (analysis of the entire gene expre
33、ssion profile of an organism) 13,69.Metabolomics enables the simultaneous analysis of primary com-pounds (such as amino acids and sugars, which are of nutritional importance to herbivores), and secondary plant compounds (such as phenolics or glucosinolates, which have a defensive function in the pla
34、nt) 13,69. The potency of certain defensive compounds is contingent on the nutritional quality of the plant. Together with multivariate statistical analysis techniques such as principal com-ponent analysis and hierarchical cluster analysis, metabolomics has been used to differentiate between differe
35、nt genotypes or cultivars of one species 70, diseased and healthy plants 71, and plants under different nutrient regimes 72. Although much effort has been put in to analyzing gene expression profiles of plants, metabolomics is a more valuable technique to ecologists than is transcriptomics, because
36、differences in gene expression profiles do not automatically translate in metabolic differences (i.e. on the phenotype level) 69. The disadvantage of metabolomic analyses is that it requires expen-sive high-throughput equipment, for example for nuclear magnetic resonance and gas-chromatography time-
37、of-flight mass spec-trometry, which is not readily available to evolutionary and ecologically oriented research groups. We are confident, however, that metabolomics will prove to be an important tool for the advancement of ecological studies of the multitrophic interactions associated with plants.as
38、 a result of belowground herbivory have been reported, suggesting that there is a range of interactions between aboveground and belowground herbivores. We argue here that these differences in responses of the plant to root-associated soil organisms are related to the differences in their feeding hab
39、its.Several studies have shown that root chewing by belowground insects causes an increase in plant defense compounds in aboveground plant parts that is similar to that observed for foliar-feeding chewing insect larvae 14,15,19,20. Studies that use artificial root damage or hormone applications as a
40、 substitute for root feeding show similar induction patterns 14,17,18. Root and shoot chewers thus elicit similar induction pathways. Interest-ingly, the distribution of defense compounds between leaves in response to damage by root chewers can differ from that observed after foliar feeding 14. Such
41、 spatial changes in plant defense can have major implications for aboveground organisms feeding from the plant and, thus, for plant fitness (Box 3).Plant responses to root-feeding nematodes are more variable, and decreases and increases in concentrations of aboveground defense compounds have both be
42、en observed 16,22. The response depends not only on the suscepti-bility of the plant to nematodes, but also on the type of feeding behaviour 16,23. For example, endoparasitic sedentary root-knot and cyst nematode species, such as Meloidogyne and Heterodera spp., establish a feeding cell, which elici
43、ts hormonal regulatory responses in the host plant; endoparasitic migratory and ectoparasitic plant-feeding nematodes, such as Pratylenchus and Tylenchorynchus, do not form a cell and are likely to influence the host plant to a lesser extent 23,ReviewTRENDS in Ecology and Evolution Vol.20 No.11 Nove
44、mber 2005619Box 3. Case study: abovegroundbelowground interactions via plant defenseIn Gossypium herbaceum cotton plants that are exposed to root-chewing insect larvae, concentrations of non-volatile terpenoid compounds (known to deter insect feeding) in the leaves increase. Terpenoid concentrations
45、 also increase after foliar feeding by insects, but only in the youngest leaves. By contrast, older leaves also show increases in terpenoid concentrations following root damage, but the level of increase per leaf is lower than after foliar feeding (Figure I, 14). Interestingly, this more-even distri
46、bution of defense compounds between leaves after root herbivory rather than after foliar herbivory is detrimental to insects feeding on the foliage. If the plant had been damaged previously by foliar feeders, insects preferentially feed on older leaves and avoid the young leaves with high terpenoid
47、levels, with little consequences for larval growth rates. However, if the plant had been previously damaged by root feeders, foliar-feeding insects feed less and have reduced growth rates 15.Cotton plants also show an aboveground indirect defense response to root herbivory and the spatial distributi
48、on also differs from the response observed after aboveground herbivory. Extrafloral nectar production (Figure II) of leaf glands increases following root herbivory. Extrafloral nectaries have an indirect defensive function because they attract ants that subsequently feed on herbivores present on the plant. Following foliar herbivory, the production of extrafloral nectar increases specifi-cally on the leaf that is under attack, possibly to direct ants to the source of that attack. After root herbivory, howeve