Vaccinations in agriculture
Vaccinations are the mainstay of western preventive medicine, and there are many parallels between the use of vaccinations in medicine and agriculture. Plant pathologists have been aware that plants can become more resistant to pathogens following exposure to avirulent strains for over 100 years (Beauverie, Reference Beauverie1901; Ray, Reference Ray1901; Chester, Reference Chester1933) although entomologists have discovered induced resistance much more recently (Green & Ryan, Reference Green and Ryan1972; Haukioja & Hakala, Reference Haukioja and Hakala1975). The activity of the inducing agent is not due to antibiotic activity per se by killing or harming the attackers; rather, the inducing agent makes the plant more resistant to subsequent challenges (Kuc, Reference Kuc1982). Induced resistance in this review refers to changes in the host plant in response to attacks or treatment that cause the plant to become less preferred or less favourable for insects compared to an uninduced plant (Karban & Baldwin, Reference Karban and Baldwin1997).
Vaccination techniques have been developed to protect crop plants against economically important diseases and arthropods, although these have been used commercially in only a small percentage of the plant systems where they seem effective (Campbell, Reference Campbell, Campbell and Macdonald1989; Karban & Baldwin, Reference Karban and Baldwin1997). As was true in medicine, early attempts to induce resistance in agriculture relied upon introducing mild, economically benign insects and mites to induce resistance against economically important arthropod pests. Although it is possible to achieve induced resistance in this way, this technique poses several hurdles.
The following characteristics will increase the feasibility of using induced resistance in specific agricultural systems (following Karban & Baldwin, Reference Karban and Baldwin1997): (i) the pest must be destructive (costly) and difficult to control by other means; (ii) the inducer must not be a pest itself or cause significant losses in yield; (iii) it must be feasible to introduce the inducer into the system; (iv) the inducer should be sustainable (perhaps self-replicating); and (v) the plant must have some tolerance of the pest and of the inducer since vaccinations are unlikely to provide complete control, by themselves. All of these conditions contribute to the cost effectiveness of induced resistance. In many markets, use of vaccination techniques will also require that some corporation or governmental agency finds commercialization of the vaccine profitable, financially and politically (Kuc, Reference Kuc, Hammerschmidt and Kuc1995). In the past this has been the biggest hurdle to overcome in adopting induced resistance in commercial agriculture.
We envision three strategies that use induced resistance to protect crop plants.
(1) Avirulent organisms can be introduced to protect crops against economically damaging pests. This is the most straight-forward method of vaccinating plants although it is also the most difficult to use effectively.
(2) As we learn about the chemical pathways that lead to induced resistance, it may become feasible to use natural or synthetic chemical elicitors of induced responses.
(3) Similarly, as we learn more about the genetics and molecular control of resistance, it may become feasible for us to selectively express resistance traits that are naturally inducible. By using genetic manipulations, we can over-express or control the expression of genes conferring resistance traits that were naturally only expressed following attack. Genetic manipulations enable us to move induced resistance traits from resistant varieties and species into susceptible varieties that have desirable agronomic characteristics.
In the following sections, we will present rice (Oryza sativa L.) as a model system for work on induced resistance against insect pests. The sequencing of the rice genome has opened the door to a wealth of genomic and biochemical information about the resistance pathways of rice; the biology of the insects are well-studied, and unlike other models (e.g. Arabidopsis), rice is the most important staple for close to a quarter of the world's population. We will describe our current knowledge of the mechanistic basis of induced resistance in rice, strategies for increasing resistance in rice to insect pests, the relationship between induced resistance and other integrated pest management (IPM) strategies in rice, and finally prospects for the future.
Insect pests of rice
In this review, we focus on the insect pests found in Asia. While the majority of insects on rice cause very little damage (Dale, Reference Dale and Heinrichs1994), there are several widespread and abundant pests that attack rice throughout Asia. For induced resistance to be useful in an IPM context, it is important to understand the biology of rice insects, particularly when they attack, and the frequency and severity of attack. Detailed information about the timing, specificity and physiology of the organisms involved is critical if induced resistance techniques are to be successful.
The rice leaffolder, Cnaphalocrocis medinalis (Guenée) (Lepidoptera: Pyralidae), attacks the rice plant during the vegetative stage. Enclosed by a leaf, larvae scrape away at the surface of leaves. Leaffolders rarely cause significant yield loss, because the rice plant is capable of tolerating serious defoliation. For example, abnormally high infestation levels, or the loss of 67% of leaves, did not cause a significant yield loss (Miyashita, Reference Miyashita1985). Leaffolders are normally controlled by a wide range of natural enemies (Khan et al., Reference Khan, Barrion, Litsinger, Castilla and Joshi1988; Barrion et al., Reference Barrion, Litsinger, Medina, Aguda, Bandong, Pantua, Viajante, de la Cruz and Vega1991); however, outbreaks have been reported resulting from excessive fertilizer and pesticide use throughout Asia (Yadava et al., Reference Yadava, Santaram, Israel and Kalode1972; Chatterjee, Reference Chatterjee1979; Dhaliwal et al., Reference Dhaliwal, Shahi, Gill and Maskina1979).
Lepidopteran borers are considered major pests of rice because they attack from seedling to maturity and are very destructive (Khan et al., Reference Khan, Litsinger, Barrion, Villaneuva, Fernandez and Taylor1991; Bandong & Litsinger, Reference Bandong and Litsinger2005). There are about fifty species that attack rice (Khan et al., Reference Khan, Litsinger, Barrion, Villaneuva, Fernandez and Taylor1991). The two most important in Asia are the striped stem borer, Chilo suppressalis (Walker) (Lepidoptera: Pyralidae), and the yellow stem borer, Scirpophaga incertulas (Walker) (Lepidoptera: Pyralidae). The insects tunnel into the stems and kill part of the plant. During the vegetative stage, stem borer damage results in dead hearts, or discoloured apical shoots. Feeding during the reproductive stage can result in white heads, or unfilled spikelets. Stem borers are difficult to control by existing methods.
Several important insect pests feed on phloem sap of rice. The brown planthopper, Nilaparvata lugens (Stål) (Hemiptera: Delphacidae), is the most common of these species. It feeds on the phloem in leaf sheaths, causing wilting and drying of the leaves. Under severe infestations, planthoppers can kill entire plants. Nilaparvata lugens can be found at all stages of plant development (Dale, Reference Dale and Heinrichs1994). It became a major threat to rice production in the early 1970s, when new high-yielding varieties were introduced with insecticides. There is considerable evidence that N. lugens outbreaks are associated with overuse of insecticides (Kenmore et al., Reference Kenmore, Cariño, Perez, Dyck and Gutierrez1984; Gallagher et al., Reference Gallagher, Kenmore, Sogawa and Perfect1994).
The Asian gall midge, Orseolia oryzae (Wood-Mason) (Diptera: Cecidomyiidae), is found primarily in lowland irrigated rice. It attacks rice from the seedling stage until the end of the tillering stage. Orseolia oryzae is only found in cultivated rice near perennial wild rice, which provides an alternate habitat during the dry season (Shepard et al., Reference Shepard, Barrion and Litsinger1995). Attack by this insect results in a profuse tillering and stunting of rice plants (Dale, Reference Dale and Heinrichs1994).
Mechanistic basis of induced resistance in rice
Early work on dicotyledonous plants revealed that induced resistance against pathogens and insects was systemic in some species, such that plant tissues on attacked plants distant from the site of attack were protected (Ross, Reference Ross1961; Green & Ryan, Reference Green and Ryan1972; Kuc, Reference Kuc1982; Karban & Carey, Reference Karban and Carey1984). Plants use chemical signals to coordinate their responses to attack. Knowledge about these signals will allow us to understand and manipulate plant defences. Careful examination of the signalling events related to systemic-induced resistance revealed that chemical cascades involving salicylic acid (SA) were responsible for many induced reactions against pathogens (Malamy et al., Reference Malamy, Carr, Klesig and Raskin1990; Metraux et al., 1990), and cascades involving jasmonic acid (JA) were involved in many induced responses against wounding and insect attack (Farmer et al., Reference Farmer, Johnson and Ryan1992). Other signalling molecules have also been identified, such as abscisic acid and ethylene, although the important role of jasmonates in signalling responses to herbivory has been highly conserved among plants families (Thaler & Bostock, Reference Thaler and Bostock2004; Stout et al., Reference Stout, Thaler and Thomma2006). However, since most of this pioneering work was done with dicotyledonous plants, the role that these signalling molecules might play in cereals such as rice has been poorly understood until recently (Schweizer et al., Reference Schweizer, Buchala, Budler and Metraux1998; Kogel & Langen, Reference Kogel and Langen2005).
Signalling in rice has been found to differ from the model that was developed for dicotyledonous plants. Rice contains relatively high background levels of endogenous SA that do not increase after infection by pathogens (Silverman et al., Reference Silverman, Seskar, Kanter, Schweizer, Metraux and Raskin1995). This result sheds doubt on the possibility that SA is the mobile signal for induced resistance in rice (Yang et al., Reference Yang, Qi and Mei2004). Even if SA is not the signal in rice, the high endogenous levels of SA appear to function as an antioxidant, protecting the plant against oxidative stress and plant pathogens. SA-deficient transgenic plants had elevated levels of H2O2 and superoxide and suffered a higher incidence of lesions under intense sunlight (Yang et al., Reference Yang, Qi and Mei2004). Furthermore, blast fungus infection led to more pathogenic lesions on SA-deficient transgenic plants than on control plants.
Even if SA does not play a role as a signalling compound for induced defence pathways in this system, rice appears to share other subsequent, ‘downstream’, steps of the induction pathway with dicotyledonous plants (Chern et al., Reference Chern, Fitzgerald, Canlas, Navarre and Ronald2005; Kogel & Langen, Reference Kogel and Langen2005). It is quite possible that monocots use an additional signalling chemical since the currently known signals cannot account for all of the responses that have been observed (Schweizer et al., Reference Schweizer, Buchala and Metraux1997; Yang et al., Reference Yang, Qi and Mei2004).
Some of the genes involved in induced resistance against blast fungus have been identified and expression of gene products conferring resistance have been found to be mediated by JA, and not SA (Lee et al., Reference Lee, Qi and Yang2001). Wounding in rice caused levels of JA to increase immediately in the wounded leaf and to accumulate with a delay of several hours in leaves that were not directly wounded (Schweizer et al., Reference Schweizer, Buchala, Budler and Metraux1998; Lee et al., Reference Lee, Cho, Jang, Rakwal, Iwahashi, Agrawal, Shim and Han2004). The SA and JA pathways may be antagonistic, and endogenous SA levels decreased during the initial JA burst (Lee et al., Reference Lee, Cho, Jang, Rakwal, Iwahashi, Agrawal, Shim and Han2004). The increase in JA caused greater production of gene products normally associated with induced responses to pathogens rather than wounding or insect damage and provided induced resistance against rice blast fungus.
Induced responses in rice appear to vary in response to different pest species. Chewing damage caused by armyworm or cluster caterpillars, Spodoptera litura (Fabricus) (Lepidoptera: Noctuidae), caused signal cascades and expression of genes normally associated with induced resistance against herbivores, such as the JA pathway, phenyl propanoid pathway and terpene biosynthesis (Xu et al., Reference Xu, Zhou, Chen, Zhang, He, Gu and Zhang2003). This result suggests that the JA signalling pathway in rice is involved with induced resistance against caterpillars. This result contrasts with plant responses to phloem-feeding insects.
In general, phloem-feeding insects appear to be perceived by plants as pathogens and induce either SA or JA/ethylene signalling pathways, resulting in the production of pathogenesis-related proteins (Walling, Reference Walling2000). Gene expression studies show that N. lugens feeding in rice probably induces the SA rather than the JA pathway (Xu et al., Reference Xu, Zhou, Chen, Zhang, He, Gu and Zhang2003; Zhang et al., Reference Zhang, Zhu and He2004). Genes for pathogenesis-related proteins were significantly overexpressed when planthoppers fed on rice (Kanno et al., Reference Kanno, Satoh, Kimura and Fujita2005; Wang et al., Reference Wang, He and He2005). The redundancy in plant responses may allow cross-protection between planthoppers and fungal pathogens. For example, rice plants previously inoculated with white-backed planthoppers, Sogatella furcifera (Horvath) (Homoptera: Delphacidae), had fewer lesions from the rice blast fungus (Kanno et al., Reference Kanno, Satoh, Kimura and Fujita2005). The SA pathway also produces other defensive chemicals, such as phenols and flavonoids (Dixon et al., Reference Dixon, Achine, Kota, Liu, Reddy and Wang2002); increases in rice phenolics following infection by rice blast pathogens or gall midges may also be controlled by the SA pathway (Bentur & Kalode, Reference Bentur and Kalode1996; Babu et al., Reference Babu, Sajeena, Samundeeswarf, Sreedhar, Vidhyasekeran and Reddy2003a).
Planthopper feeding induces the expression of a variety of other defence genes (Wang et al., Reference Wang, Ren, Zhu and He2004, Reference Wang, He and He2005; Yuan et al., Reference Yuan, Chen, Zhu and He2004; Zhang et al., Reference Zhang, Zhu and He2004). For instance, Yuan et al. (Reference Yuan, Chen, Zhu and He2004) found that mechanical damage, ethylene, and N. lugens feeding induced expression of a novel rice gene, although its role in defence has not yet been established. Nilaparvata lugens feeding induced expression of protease-inhibitor (PI) genes such as oryzacystatin (Zhang et al., Reference Zhang, Zhu and He2004; Wang et al., Reference Wang, He and He2005). These are thought to interfere with insect protein digestion in the midgut (Broadway & Duffey, Reference Broadway and Duffey1986, Jongsman & Bolter, Reference Jongsma and Bolter1997). Nilaparvata lugens feeding also induced the expression of β-glucosidase, which is thought to be involved with release of volatile terpenoids (Wang et al., Reference Wang, He and He2005). The pathways controlling these other defence genes are unclear, but they could be induced by a common signalling molecule from the SA pathway.
Gene expression studies indicate that induced responses can be both rapid and persistent. Although the precise timing of induced responses has not been studied, some responses can occur within 24 h (Xu et al., Reference Xu, Zhou, Xia, Zhang and Gu2002). Induced resistance can also last for quite a long time. For example, induction by white-backed planthoppers protected the rice plant for more than 15 days against rice blast (Kanno et al., Reference Kanno, Satoh, Kimura and Fujita2005).
Strategies for increasing resistance in rice
Insects as elicitors
Induced resistance can be rapid, acting directly upon the insect that causes the initial damage, or delayed, acting upon insects that subsequently attack the plant. Some cultivars of Japonica rice produce watery lesions rapidly at the site of oviposition in response to whitebacked planthopper eggs (Suzuki et al., Reference Suzuki, Sogawa and Seino1996) and to a lesser degree to brown planthopper eggs (Yamasaki et al., Reference Yamasaki, Yoshimura and Yasui2000). These watery lesions contain an ovicidal compound, benzyl benzoate, which causes high rates of egg mortality (up to 80% depending upon cultivar, developmental stage and other factors). No ovicidal substance was detected in undamaged plants or in locations away from oviposition sites on damaged plants (Seino et al., Reference Seino, Suzuki and Sogawa1996). A single plant gene conferring ovicidal activity has recently been identified (Yamasaki et al., Reference Yamasaki, Yoshimura and Yasui2003).
All crops, including rice, serve as hosts for a wide range of herbivores (see above for a discussion of insects on rice). Some of these herbivore species and biotypes within species are far more damaging to the crop than are others. Herbivores differ in their abilities to build up large populations. Plants also vary greatly in their tolerance as hosts of different herbivores; some pests cause much more economic loss per capita than others. These generalizations apply well to rice (Way & Heong, Reference Way and Heong1994; Matteson, Reference Matteson2000). For instance, rice seedlings of a resistant variety Phalguna exhibit a hypersensitive response including localized necrosis immediately surrounding the oviposition sites in reaction to several biotypes of the Asian rice gall midge, Orseolia oryzae (Bentur & Kalode, Reference Bentur and Kalode1996; Sardesai et al., Reference Sardesai, Rajyashri, Behura, Nair and Mohan2001). This hypersensitive response caused 100% mortality of first instar maggots within four days. Tillers that were produced subsequently by these induced plants were well protected against avirulent biotypes. In addition, seedlings that had been exposed to an avirulent biotype gained resistance against more damaging biotypes of the rice gall midge; resistance induced by the avirulent midges continued to protect plants for several weeks (Bentur & Kalode, Reference Bentur and Kalode1996). This suggested that releases of the avirulent biotype could protect plants against the spread of more damaging biotypes. Efforts are underway to map and clone the genes responsible for this delayed induced resistance against gall midges (Sardesai et al., Reference Sardesai, Rajyashri, Behura, Nair and Mohan2001; Harris et al., Reference Harris, Stuart, Mohan, Nair, Lamb and Rohfritsch2003).
Rice plants that are attacked early in development can become more resistant to subsequent attacks. For example, young plants that were fed on by early instar caterpillars of Spodoptera frugiperda (the fall armyworm of North America) became locally and systemically more resistant to growth by subsequent caterpillars compared to controls (M.J. Stout, unpublished). Similarly, prior feeding by two species of planthoppers reduced the quality of rice plants as food for subsequent planthoppers (Matsumura & Suzuki, Reference Matsumura and Suzuki2003).
Rice plants that are attacked by armyworm or cluster caterpillars (Spodoptera litura) release blends of volatile compounds that are repellent to brown planthoppers (Xu et al., Reference Xu, Zhou, Xia, Zhang and Gu2002). Adult brown planthopper females were less likely to choose rice plants damaged by caterpillars compared with undamaged plants, mechanically damaged plants or plants infested with brown planthoppers in dual-choice experiments conducted in flight tunnels. This result indicates that induced plant volatiles could be used to make plants less attractive to important pests such as brown planthoppers although caterpillar numbers are difficult to manipulate at agricultural scales and unlikely to be useful as actual inducers. Recent work has attempted to identify the active volatiles in tests combining y-tube olfactometers with chemical techniques to examine the pathways that produced elevated plant emissions (Xu et al., Reference Xu, Zhou, Chen, Zhang, He, Gu and Zhang2003; Zhou et al., Reference Zhou, Xu, Zhang, Gu and Zhang2003).
Chemicals as elicitors
Inoculating plants with avirulent strains or species of insects to gain protection against damaging ones is conceptually straightforward although this strategy faces several practical problems. It must be possible (and cost effective) to acquire, transport and introduce the avirulent inducer. This often requires considerable labour, expertise to distinguish the virulent and avirulent insects, and trust on the part of the farmers. Some of these problems can be solved by applying chemicals that induce resistance against pest insects. These chemical inducers are not directly toxic or inhibitory to the pest insects but cause the plant to increase its level of resistance. In some cases, the chemical inducers are ‘botanicals’ or plant extracts. For example, leaf extracts from Datura metel (Solanaceae) have been used to induce systemic resistance against several economically important pathogens of rice in India (Kagale et al., Reference Kagale, Marimuthu, Thayumanavan, Nandakumar and Samiyappan2004). Some plant-derived substances are inexpensive and readily available in developing countries although we are not aware of their commercial use to control pathogens or insect pests of rice anywhere. Similarly, treating rice seeds before planting with chemical ‘sensitizers’ stimulated phytoalexin responses and other defensive responses when the seedlings were challenged subsequently by pathogens (Cartwright et al., Reference Cartwright, Langcake, Pryce, Leworthy and Ride1977; Sinha & Hait, Reference Sinha and Hait1982; Hait & Sinha, Reference Hait and Sinha1987; Munusamy et al., Reference Munusamy, Selvaraj, Murugaiyan, Sundaram, Chung, Yang, Subbiah and Sa2004). Various fertilizers and growth stimulants have been reported to also increase plant resistance to insects. For example, several zinc or iron based soil additives have the additional effects of reducing insect populations. Rice plants receiving applications of these fertilizers had approximately half the populations of whitebacked planthoppers as untreated controls and produced higher grain yields (Rath & Misra, Reference Rath and Misra1998). Several authors have questioned the potential of strategies relying on chemicals to boost induced responses because the resistance has been relatively short-lived and may not be cost effective in some instances (Deacon, Reference Deacon1988; Hedin, Reference Hedin1990; Isman, Reference Isman2006).
Some cultural practices change the rice plant so that it becomes more susceptible, rather than more resistant, to pests. For example, several widely used pesticides have been found to increase populations of planthoppers (Wu et al., Reference Wu, Xu, Yuan, Liu, Jiang and Xu2001, Reference Wu, Hui-Min, Yang, Liu, Liu and Wilkins2004). The mechanisms responsible varied depending upon the pesticide and the insect although they involved changes in numerous plant traits.
An understanding of the signalling process has gone hand in hand with developing artificial elicitors of resistance that can be used to control levels of plant resistance under agricultural conditions. Several synthetic mimics of SA were developed that caused plants to react much as they would when they were attacked by pathogens (Gorlach et al., Reference Gorlach, Volrath, Knauf-Bleter, Hengy, Beckhove, Kogel, Oostendorp, Staub, Ward, Kessmann and Ryals1996). One of these, benzothiadiazole, has been marketed commercially (as Bion) and registered for control of many diseases in cereal crops. It protects rice against fungal and bacterial infections more effectively than SA (Schweizer et al., Reference Schweizer, Schlagenhauf, Schaffrath and Dudler1999; Babu et al., Reference Babu, Sajeena, Samundeeswarf, Sreedhar, Vidhyasekeran and Reddy2003b). We are not aware of rice farmers using benzothiadiazole successfully in commercial field situations.
As mentioned above, JA is generally regarded as a key component of the signalling pathway involved with induced plant resistance to insects with chewing mouthparts, such as caterpillars. Synthetic analogues of jasmonates are more potent elicitors of plant responses associated with the JA pathway than are naturally occurring compounds (Schuler et al., Reference Schuler, Gorls and Boland2001). Although the signalling process is not well understood in rice, the JA pathway appears to be involved in induced responses caused by wounding or by chewing herbivores (see above). Plants sprayed with JA at 1 mm had approximately half as many larvae of rice water weevil, Lissorhoptrus oryzophilus Kuschel (Coleoptera: Curculionidae), as untreated controls in trials in North America (M.J. Stout, unpublished). Similarly, relative growth rates of S. frugiperda caterpillars were reduced by the application of 0.5 mm JA (M.J. Stout, unpublished). No chemical elicitors have been marketed commercially for control of insect pests of rice although this strategy holds considerable promise.
Genetic techniques to incorporate induced resistance
Classical breeding programmes for plant resistance to diseases and herbivores have been limited by the existing heritable variation present in the species (or closely related species). Genetic engineering offers the exciting possibility of incorporating novel resistance traits from other species, families, and even phyla into rice varieties that show desirable traits. For example, rice varieties in China have been transformed using Agrobacterium to incorporate inducible cowpea trypsin inhibitors. These transformed plants showed enhanced resistance against stem borers (Hu-Qi et al., Reference Hu-Qi, Li-Yue, Zheng-Yu, Zhang-Xaio and Li-Ben2005). Transformed plants supported smaller populations of several caterpillars including stem borers and rice leaffolders and reduced levels of damage compared to untransformed controls in field trials (Li-Yue et al., Reference Li-Yue, Hu-Qi, Zheng-Yu, Zhang-Xiao and Li-Ben2005). Other resistance traits (e.g. a gene that provides resistance against planthoppers) that are not inducible have also been incorporated into agronomically desirable rice varieties (Nagadhara et al., Reference Nagadhara, Ramesh, Pasalu, Kondala Rao, Sarma, Reddy and Rao2004). Other inducible traits that have been characterized genetically, such as genes associated with ovicidal responses to planthopper eggs, may be amenable to genetic engineering in the near future (Yamasaki et al., Reference Yamasaki, Yoshimura and Yasui2003).
In addition, it should be possible to make a trait that is now constitutively expressed inducible by fusing it with an inducible promoter. It would then only be expressed following insect attack or following activation by a chemical elicitor. Such specificity would reduce impacts of genetically modified plants on non-target organisms. Recently, a gene involved in pathogen resistance in rice has been linked successfully to an inducible promoter (Mei et al., Reference Mei, Qi, Sheng and Yang2006). Attempts are underway at several laboratories around the world to develop such tools to genetically improve rice by increasing resistance against insects as well as pathogens (Kogel & Langen, Reference Kogel and Langen2005).
Induced resistance and integrated pest management
Relationships between insect control and disease control
Resistance to insects is influenced by many factors including the plant's nutritional state, its constitutive and induced traits and its environment. Integrated pest management is an attempt to manipulate the plant and its environment so as to manage losses to insects and pathogens and to maximize economic return to the growers. There has been a growing realization that managing plants for resistance to insect herbivores is both strongly affected by and also strongly influences resistance to pathogens (Karban & Baldwin, Reference Karban and Baldwin1997; Stout et al., Reference Stout, Thaler and Thomma2006). As mentioned above, for many plant species, responses to pathogens are thought to be mediated by the SA pathway, while responses to herbivores are mediated by the JA pathway. However, for rice and perhaps other cereals, the processes controlled by these two pathways are interrelated in complex ways. For example, treatment of rice plants with JA has been found to make them more attractive to some herbivores, such as brown planthoppers, in addition to deterring others (Lou et al., Reference Lou, Du, Turlings, Cheng and Shan2005). This is consistent with the observation that brown planthopper damage causes responses associated with the SA pathway rather than the JA pathway (Xu et al., Reference Xu, Zhou, Chen, Zhang, He, Gu and Zhang2003). Because these two pathways interact, attempts to manage pathogens can have strong effects on insect pests, and vice versa.
In rice, responses against insects and pathogens are clearly not always independent. For example, plants that have hosted white-backed planthoppers are strongly protected against symptoms of rice blast fungus (Kanno & Fujita, Reference Kanno and Fujita2003; Kanno et al., Reference Kanno, Satoh, Kimura and Fujita2005). This negative interaction was found to occur even if the planthopper and the fungus did not overlap precisely in time and space. On a larger scale, in agricultural paddies, the application of insecticides to control white-backed planthopper numbers increased the incidence of rice blast disease (Satoh et al., Reference Satoh, Nakajima and Kanno2005). Levels of plant parasites (both insects and pathogens), as well as tactics used to control them, are likely to have complex and far-reaching affects on plant resistance.
Relationships between herbivores and their predators and parasites
Plant responses to attack by insects may also have effects on other organisms in the agroecosystem, such as the predators and parasites of herbivores. Certainly, insecticides targeted at rice pests also reduce populations of beneficial insects (Way & Heong, Reference Way and Heong1994; Matteson, Reference Matteson2000). If induced plant responses increase rates of predation or parasitism of herbivores, these changes may provide indirect defences for the plants. For example, rice plants that were infested with Spodoptera litura caterpillars or with brown planthoppers emitted volatiles that were repellent, under some circumstances, to other planthoppers that arrived subsequently (Xu et al., Reference Xu, Zhou, Xia, Zhang and Gu2002, although see also Lou et al., Reference Lou, Du, Turlings, Cheng and Shan2005). Each specific herbivore species caused plants to emit a specific blend of volatiles. Volatiles released when plants were attacked by planthoppers also attracted parasitoid wasps that were specific for planthopper eggs (Lou et al., Reference Lou, Cheng, Ping, Tang, Ru and Du2002). Similarly, rice plants treated with JA released volatiles that were attractive to parasitoids (Lou et al., Reference Lou, Du, Turlings, Cheng and Shan2005). Plants near neighbours treated with JA experienced greater rates of parasitism of brown planthopper eggs in the greenhouse and the field. This suggests that chemical elicitors may be useful as inducers of direct defences in rice as well as indirect defences mediated by predators and parasitoids.
Future prospects for induced resistance in rice IPM
Although induced resistance has played relatively little role in managing insect pests of rice, it holds great promise as a management tool for the future. Below, we consider the prospects for employing the three strategies discussed above. This may be an excellent system in which to allow early season pests to induce resistance against later ones. As discussed above, early ‘vaccinations’ may protect plants against later infestations of the same insect species. Rice varieties have been identified that have high levels of induced resistance against the rice gall midge and against white and brown planthoppers. Since the rice genome is so well characterized, it should be possible in the near future to incorporate induced resistance against these important pests into rice varieties that have other desirable traits.
Early attack by economically unimportant species may also provide resistance against more damaging species of rice insects. For example, leaffolders are common early season feeders although they rarely cause economic losses. Although leaffolders have often been targeted by growers using pesticides, encouraging small, natural populations may provide resistance against more damaging insects that attack later in the season. This possibility is currently being investigated by researchers in the Philippines, China and Malaysia. Although previous attempts to use early season insects to vaccinate against later season ones have not been adopted on a large scale, rice offers several advantages that were absent from attempts in other systems. For example, the rice leaffolder is easy to identify in the field, it has a wide natural distribution, and it can be easily introduced. Leaffolders are unlikely to become serious pests although they have the potential to help protect plants against more costly species. As noted above, using vaccinations for pest management is information intensive and labor intensive. Whereas governments and universities in North America are cutting back on field research and extension efforts, considerable infrastructure is in place in many Asian growing regions to provide information and assistance to rice farmers (Matteson, Reference Matteson2000; Huan et al., Reference Huan, Thiet, Chien and Heong2005).
Chemical elicitors of induced resistance may also allow rice farmers to manipulate the levels and timing of plant resistance. Several of the economically important rice pests have been found to be affected by host plant resistance that is mediated by plant hormones such as JA and SA. Experiments are currently underway to evaluate vaccinations using these elicitors as means of controlling levels of resistance of rice in production agriculture. Improved basic knowledge of the mechanisms, specificity, timing and natural history of plant hormones and their effects will make this effort more effective. Similarly, as we gain a more complete understanding of additional plant regulators and how they interact, it is likely that we will have more candidates that can be used in agriculture to manipulate plant defences.
Cereal grains were problematic candidates for improvement using biotechnology because transforming them by adding novel genes was not possible for many years. These difficulties have been solved to a large extent, and rice has become a particularly good candidate crop for biotechnological approaches since the genome has been relatively well characterized (Repellin et al., Reference Repellin, Baga, Jauhar and Chibbar2001). Biotechnological approaches require that traits providing induced resistance be identified, the genes controlling them must be mapped, and techniques for transferring them into desirable varieties be developed. Since biotechnological approaches can be extremely specific, they can theoretically provide greater safety in terms of minimizing environmental problems and undesirable secondary chemicals associated with inducers of more generalized plant responses. Additional control over expression of resistance traits may be possible if genes can be fused to inducible promoters so that the desired products can be switched on and off as needed. It remains unclear whether this potential can be realized and how many years in the future this realization may be.
Acknowledgements
The authors were supported by the Strategic Initiative Fund of the International Rice Research Institute. This review benefited from discussions with K.L. Heong, Merdelyn Lit, Nik Mohd Noor Nik Salleh and Lu Zhongxian and comments on an earlier draft by Mawsheng Chern, Larry Godfrey and Michael Stout.
