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Biotic interactions
Biotic interactions Ploy and counter-ploy in the biotic interactions of plants Editorial overview Maria J Harrison and Ian T Baldwin Current Opinion in Plant Biology 2004, 7:353–355 Available online 15th June 2004 1369-5266/$ – see front matter ß 2004 Elsevier Ltd. All rights reserved. DOI 10.1016/j.pbi.2004.05.012
Maria J Harrison Boyce Thompson Institute for Plant Research, Tower Road, Ithaca, New York 14853-1801, USA e-mail: [email protected]
Maria is a scientist at the Boyce Thompson Institute for Plant Research. The research in her laboratory focuses on the arbuscular mycorrhizal symbiosis and phosphate transport in plants. Her work integrates genomics, genetic and cell biology techniques to dissect the molecular basis of the development and functioning of the arbuscular mycorrhizal symbiosis in a model legume, Medicago truncatula.
Ian T Baldwin Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Hans-Kno¨llStrasse 8, Beutenberg Campus, 07745 Jena, Germany e-mail: [email protected]
The goal of the Baldwin group is to bring molecular biological tools to the study of plant–herbivore interactions so as to manipulate these interactions in nature and to identify traits that are demonstrably important for Darwinian fitness. We focus on signaling and defense responses in two native plant species (Nicotiana attenuata in North America and Solanum nigrum in Europe) that take part in a rich suite of ecological interactions. We have developed molecular (transformation systems, VIGS systems, cDNA and genomic libraries, cDNA and oligo microarrays and real-time RTPCR), analytical (high-throughput HPLCDAD-MS, GC-MS, ELISA and z-Nose) and ecological (natural history background, and field stations in Utah and Jena) tools to allow us to rigorously manipulate the genetic basis for ecological sophistication in these two systems. www.sciencedirect.com
Abbreviations AM arbuscular mycorrhizal JA jasmonic acid ROS reactive oxygen species SA salicylic acid
Throughout their lives, plants interact with a huge array of organisms, each with their own agenda. These interactions take many forms, including close encounters with mobile organisms, co-habitation with other plants and organisms in the rhizosphere, intimate associations with a diverse array of pathogens and sustained interactions with symbionts, all of which are potential selective forces for the plant. As a consequence, these interactions are best understood in the context of the evolutionary interplay that occurs between the genomes of the interacting partners. As each plant response evokes counter responses, the dynamics of the interaction are sometimes coevolutionary and always complicated. Interactions with simple outcomes (e.g. the complete domination of one partner) are no longer seen as part of the picture. The reviews in this issue focus on the mechanisms of plant interactions with other organisms, emphasizing the signals, signaling networks and cellular processes that underlie these interactions and the evolutionary dialog that emerges from the details. Plants have the capacity to produce a broad array of molecules that act as signals and elicit responses in other organisms: many mimic or inhibit the partner’s endogenous signals. All responses involve tradeoffs, compromises negotiated over evolutionary time between the interacting partners. These tradeoffs are most easily seen in the interactions that occur along the parasitic-mutualistic continuum. Plants have evolved complex, integrated defense-signaling pathways that allow them to tailor their responses to individual pathogens. Such tailoring maintains the delicate balance of restricting invaders while allowing plants to avoid collateral damage to themselves or their beneficial symbionts. Defense signaling, with its own suite of checks and balances, must be integrated with symbiotic signaling pathways as the latter may be open to exploitation. Studies of successful attackers (bacteria, virus, nematodes, fungi and insects) reveal the cellular mechanisms that are targeted by these biotrophic pathogens to manipulate defense pathways and develop a sustaining environment in the plant. The idea that successful pathogens suppress host defenses, and in some instances redirect cellular processes to create an environment that is favorable for their proliferation, is accepted. As outlined in a number of reviews Current Opinion in Plant Biology 2004, 7:353–355
354 Biotic interactions
(Abramovitch and Martin [pp. 356–364], Whitham and Wang [pp. 365–371], Bird [pp. 372–376], Schulze-Lefert [pp. 377–383], Hotson and Mudgett [pp. 384–390]), the molecular mechanisms that are involved in these processes are beginning to be revealed. Plant pathogenic bacteria initiate their attack by introducing an array of proteins termed ‘effectors’ into the cells of their plant hosts. As reviewed by Abramovitch and Martin, a surprising number of effector proteins function to suppress hypersensitive-response-based cell death and, in some cases, other plant defense responses. The effectors are diverse and their modes of action largely unknown but, as reviewed by Hotson and Mudgett, a number of effectors have cysteine protease activity. The manipulation of the host’s signaling pathways via proteolysis of host proteins appears to be common among a wide range of bacterial pathogens. Plant targets for proteolytic effectors, where known, include fundamental cellular processes such as sumoylation. The proteolysis of essential host targets may promote bacterial virulence, though it can also initiate the demise of bacteria. Plants have evolved a counter-attack strategy that involves monitoring the proteolytic action of the effectors. In appropriate hosts, proteolysis can trigger R-protein-mediated defense responses (reviewed by Belkhadir et al. [pp. 391–399]). As reviewed by van der Hoorn and Jones [pp. 400–407], plant proteases are currently viewed as having a central role in defense responses to pathogens and insects, not only in the execution of the response but also in surveillance and signaling pathways. Subversion of defense responses and the manipulation of host cellular processes to create a specialized environment is a strategy perfected by the biotrophic fungal pathogens. The first challenge faced by these pathogens is to control defenses that are triggered as they traverse the cell wall. As reviewed by Schulze-Lefert, recent findings support the presence of a surveillance system that enables the plant to monitor cell wall integrity, with a breach of security resulting in the activation of salicylic acid (SA)-dependent signaling pathways. A conserved SNARE-dependent vesicle-trafficking process is required for nonhost/basal resistance in both monocots and dicots. Some biotrophic fungal pathogens subvert the cell wall resistance mechanisms by disrupting this process. Altering trafficking and the balance between exocytotic and endocytotic processes could also allow the manipulation of the plant membrane at the biotrophic interface. In this regard, there are parallels between the biotrophic fungal pathogen interactions and the symbiotic arbuscular mycorrhizal (AM) associations. Both require basal defenses to be avoided and a polarized extension of the plasma membrane at the fungal–plant interface. The molecular and cellular events that underlie mutualistic interactions have long been thought to involve cooptions of existing cellular processes. Positional cloning of symbiosis genes in the model legumes Medicago truncatula Current Opinion in Plant Biology 2004, 7:353–355
and Lotus japonicus has provided exciting insights into symbiosis signaling pathways (reviewed by Riely et al. [pp. 408–413] and Parniske [pp. 414–421]) that further support this view. The long search for the elusive Nodfactor receptor(s) has concluded with the identification of receptor kinase proteins that have extracellular LysM domains, which have been implicated in Nod-factor binding. At least two receptor kinases were identified in each species, providing the next challenge: to determine how the receptor functions. Signaling components that are required for both nodulation and development of the AM symbiosis have also been uncovered. The AM symbiosis is the older of the two interactions, and consequently, it seems likely that rhizobia co-opted available mycorrhizal signaling pathways to facilitate nodulation. This shared symbiosis signaling pathway includes a novel channel protein, an leucine-rich repeat (LRR) receptorkinase and a calcium/calmodulin-dependent protein kinase, which place ion fluxes and calcium signals centrally in this pathway. A plant receptor that responds to signals from AM fungi has not yet been identified, but evidence of diffusible fungal signals that activate plant gene expression before physical contact with the host supports its existence. Rhizobia may not have been the only organisms to co-opt pathways that originally developed for other plant– microbe interactions. As Bird mentions, intriguing parallels exist between signals and developmental events that underlie the plant interactions with both nematodes and rhizobia. Although plants have evolved mechanisms to control pathogens, they may be less well equipped to avoid secondary exploitation by epiparasites. As described by Leake (pp. 422–428), the use of molecular taxonomy techniques has provided new insights into mycoheterophic interactions, revealing the identity of the fungi from which these achlorophyllous plants steal carbon. Surprisingly, the very specialized achlorophyllous plants have chosen to parasitize AM and ectomycorrhizal fungi, symbionts that have a direct carbon pipeline to their plant partners. Such are the hidden costs to the plant of developing mycorrhizal symbioses. Signal deception appears to be rampant in a plant’s interactions with bacteria and pollinators. Bauer and Mathesius (pp. 429–433) discuss how bacteria use quorum-sensing signals to orchestrate infections of multi-cellular organisms. Plants not only respond to these bacterial signals but produce their own quorum-sensing mimics, and actively disrupt these signals in a process called ‘quorum quenching’, presumably to disrupt the communication network in the surrounding bacterial communities. The remarkable achievements in this field have, to a large extent, been made possible by the remarkable convergence on a relatively small number of microbial signals. Deceptive signaling, albeit on a larger spatial scale, is lucidly illustrated in the first Current www.sciencedirect.com
Editorial overview Harrison and Baldwin 355
Opinion in Plant Biology review on plant–pollinator interactions by Raguso (pp. 434–440). He details how plant’s mimicry of the pheromones and posture of female wasps attracts male wasps to the flowers of particular orchids, and how the characteristic odors of decaying flesh attract carrion blowflies. The benefits of finding unmated females and carrion seem to overwhelm the costs of the occasional floral visit and are responsible for maintaining this resource-deception mechanism for pollination. Chemical fragrances are not the only signals involved in pollination signaling: the echo fingerprints of flowers provide valuable information to the sonar-based sensory system of bats. The simplistic view that plant responses to microbial interactors are mediated by a small number of smallmolecular-weight hormones (including SA, jasmonic acid [JA] and ethylene) has given way to a more inclusive view. According to this view, many of the signals and secondary messengers that are known from animal systems, including redox signals, are involved, as are a selection of novel plant-specific signals. Interest in jasmonates and other oxylipins that are produced by the enzymatic peroxidation of fatty acids erupted when these signals were found to profoundly mediate resistance against a wide range of chewing insects and certain microbial pathogens. The spectrum of potential signals has exploded with the recognition that many free-radical-produced nonenzymatic oxilipins, some of which are produced by reactive oxygen species (ROS)-mediated stress responses, are elicitors of defense responses (reviewed by Mueller [pp. 441–448]). Many of these nonenzymatically generated oxilipins are toxic. They not only may represent the first line of defense against microbial invasion but also have evolved a subsequent signaling function as indicators of membrane damage. Lipid signals are implicated in systemic acquired resistance (SAR) against pathogens and insects, and with the identification of the phytoprostanes, the array of possible signaling pathways that involve lipids is daunting. It is now established that NO signaling interacts with SA and JA signaling, two fundamental pathways that mediate pathogen and insect resistance (reviewed by Wendehenne et al. [pp. 449–455]). Three second
www.sciencedirect.com
messengers (i.e. guanylate cyclase, cyclic ADP ribose and Caþ2) are known to mediate NO signaling responses. NO signaling appears to inhibit the wound-induced H2O2 burst, and thereby inhibits the ROS-associated HR. When activated in conjunction with H2O2 production, however, NO signaling activates programmed cell death. In addition to NO’s role in mediating cross-talk between pathways involving the established phytohormones, NON-EXPRESSOR OF PATHOGENESISRELATED GENES1 (NPR1), which was previously shown to mediate SA signaling, is now known to play different roles in the nucleus and the cytosol in mediating SA signaling and SA–JA signal interactions, as reviewed by Pieterse and Van Loon (pp. 456–464). The AP2 family of transcription factors, which mediates many of the small phytohormone responses, particularly ethylene signaling, is reviewed by Gutterson and Reuber (pp. 465–471) from a phylogenetic perspective. Such a perspective highlights the structural elements that are likely to confer specialized function within plant lineages. ROS-mediated programmed cell death, which is so frequently invoked in both offensive and defense responses in plant–pathogen interactions, may also be involved in some plant–plant allelopathic interactions. As reviewed by Weir et al. (pp. 472–479), particular flavonoids that are secreted into the rhizosphere by allelopathic plants can elicit ROS-mediated cell death in susceptible plants, providing a potential mechanism for this form of chemical warfare between plants. Allelopathic interactions are immensely complicated, and mutant plants that are unable to secrete the putative allelochemicals are sorely needed to determine whether allelopathy occurs under ecologically realistic conditions. In short, the reviews in this issue portray a plant’s biotic interactions as comparable to a complicated espionage plot imagined by the best spy/thriller writers of the day. A valuable spin-off of the mechanism-focused research reviewed in this issue would be to generate mutants and to identify signals that could be used to manipulate these complicated interactions in nature. We might just learn that nature tells a tale more ripe with intrigue than the paranoid conspiracy-theory-evoking human mind could ever weave.
Current Opinion in Plant Biology 2004, 7:353–355
Maria J Harrison Boyce Thompson Institute for Plant Research, Tower Road, Ithaca, New York 14853-1801, USA e-mail: [email protected]
Maria is a scientist at the Boyce Thompson Institute for Plant Research. The research in her laboratory focuses on the arbuscular mycorrhizal symbiosis and phosphate transport in plants. Her work integrates genomics, genetic and cell biology techniques to dissect the molecular basis of the development and functioning of the arbuscular mycorrhizal symbiosis in a model legume, Medicago truncatula.
Ian T Baldwin Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Hans-Kno¨llStrasse 8, Beutenberg Campus, 07745 Jena, Germany e-mail: [email protected]
The goal of the Baldwin group is to bring molecular biological tools to the study of plant–herbivore interactions so as to manipulate these interactions in nature and to identify traits that are demonstrably important for Darwinian fitness. We focus on signaling and defense responses in two native plant species (Nicotiana attenuata in North America and Solanum nigrum in Europe) that take part in a rich suite of ecological interactions. We have developed molecular (transformation systems, VIGS systems, cDNA and genomic libraries, cDNA and oligo microarrays and real-time RTPCR), analytical (high-throughput HPLCDAD-MS, GC-MS, ELISA and z-Nose) and ecological (natural history background, and field stations in Utah and Jena) tools to allow us to rigorously manipulate the genetic basis for ecological sophistication in these two systems. www.sciencedirect.com
Abbreviations AM arbuscular mycorrhizal JA jasmonic acid ROS reactive oxygen species SA salicylic acid
Throughout their lives, plants interact with a huge array of organisms, each with their own agenda. These interactions take many forms, including close encounters with mobile organisms, co-habitation with other plants and organisms in the rhizosphere, intimate associations with a diverse array of pathogens and sustained interactions with symbionts, all of which are potential selective forces for the plant. As a consequence, these interactions are best understood in the context of the evolutionary interplay that occurs between the genomes of the interacting partners. As each plant response evokes counter responses, the dynamics of the interaction are sometimes coevolutionary and always complicated. Interactions with simple outcomes (e.g. the complete domination of one partner) are no longer seen as part of the picture. The reviews in this issue focus on the mechanisms of plant interactions with other organisms, emphasizing the signals, signaling networks and cellular processes that underlie these interactions and the evolutionary dialog that emerges from the details. Plants have the capacity to produce a broad array of molecules that act as signals and elicit responses in other organisms: many mimic or inhibit the partner’s endogenous signals. All responses involve tradeoffs, compromises negotiated over evolutionary time between the interacting partners. These tradeoffs are most easily seen in the interactions that occur along the parasitic-mutualistic continuum. Plants have evolved complex, integrated defense-signaling pathways that allow them to tailor their responses to individual pathogens. Such tailoring maintains the delicate balance of restricting invaders while allowing plants to avoid collateral damage to themselves or their beneficial symbionts. Defense signaling, with its own suite of checks and balances, must be integrated with symbiotic signaling pathways as the latter may be open to exploitation. Studies of successful attackers (bacteria, virus, nematodes, fungi and insects) reveal the cellular mechanisms that are targeted by these biotrophic pathogens to manipulate defense pathways and develop a sustaining environment in the plant. The idea that successful pathogens suppress host defenses, and in some instances redirect cellular processes to create an environment that is favorable for their proliferation, is accepted. As outlined in a number of reviews Current Opinion in Plant Biology 2004, 7:353–355
354 Biotic interactions
(Abramovitch and Martin [pp. 356–364], Whitham and Wang [pp. 365–371], Bird [pp. 372–376], Schulze-Lefert [pp. 377–383], Hotson and Mudgett [pp. 384–390]), the molecular mechanisms that are involved in these processes are beginning to be revealed. Plant pathogenic bacteria initiate their attack by introducing an array of proteins termed ‘effectors’ into the cells of their plant hosts. As reviewed by Abramovitch and Martin, a surprising number of effector proteins function to suppress hypersensitive-response-based cell death and, in some cases, other plant defense responses. The effectors are diverse and their modes of action largely unknown but, as reviewed by Hotson and Mudgett, a number of effectors have cysteine protease activity. The manipulation of the host’s signaling pathways via proteolysis of host proteins appears to be common among a wide range of bacterial pathogens. Plant targets for proteolytic effectors, where known, include fundamental cellular processes such as sumoylation. The proteolysis of essential host targets may promote bacterial virulence, though it can also initiate the demise of bacteria. Plants have evolved a counter-attack strategy that involves monitoring the proteolytic action of the effectors. In appropriate hosts, proteolysis can trigger R-protein-mediated defense responses (reviewed by Belkhadir et al. [pp. 391–399]). As reviewed by van der Hoorn and Jones [pp. 400–407], plant proteases are currently viewed as having a central role in defense responses to pathogens and insects, not only in the execution of the response but also in surveillance and signaling pathways. Subversion of defense responses and the manipulation of host cellular processes to create a specialized environment is a strategy perfected by the biotrophic fungal pathogens. The first challenge faced by these pathogens is to control defenses that are triggered as they traverse the cell wall. As reviewed by Schulze-Lefert, recent findings support the presence of a surveillance system that enables the plant to monitor cell wall integrity, with a breach of security resulting in the activation of salicylic acid (SA)-dependent signaling pathways. A conserved SNARE-dependent vesicle-trafficking process is required for nonhost/basal resistance in both monocots and dicots. Some biotrophic fungal pathogens subvert the cell wall resistance mechanisms by disrupting this process. Altering trafficking and the balance between exocytotic and endocytotic processes could also allow the manipulation of the plant membrane at the biotrophic interface. In this regard, there are parallels between the biotrophic fungal pathogen interactions and the symbiotic arbuscular mycorrhizal (AM) associations. Both require basal defenses to be avoided and a polarized extension of the plasma membrane at the fungal–plant interface. The molecular and cellular events that underlie mutualistic interactions have long been thought to involve cooptions of existing cellular processes. Positional cloning of symbiosis genes in the model legumes Medicago truncatula Current Opinion in Plant Biology 2004, 7:353–355
and Lotus japonicus has provided exciting insights into symbiosis signaling pathways (reviewed by Riely et al. [pp. 408–413] and Parniske [pp. 414–421]) that further support this view. The long search for the elusive Nodfactor receptor(s) has concluded with the identification of receptor kinase proteins that have extracellular LysM domains, which have been implicated in Nod-factor binding. At least two receptor kinases were identified in each species, providing the next challenge: to determine how the receptor functions. Signaling components that are required for both nodulation and development of the AM symbiosis have also been uncovered. The AM symbiosis is the older of the two interactions, and consequently, it seems likely that rhizobia co-opted available mycorrhizal signaling pathways to facilitate nodulation. This shared symbiosis signaling pathway includes a novel channel protein, an leucine-rich repeat (LRR) receptorkinase and a calcium/calmodulin-dependent protein kinase, which place ion fluxes and calcium signals centrally in this pathway. A plant receptor that responds to signals from AM fungi has not yet been identified, but evidence of diffusible fungal signals that activate plant gene expression before physical contact with the host supports its existence. Rhizobia may not have been the only organisms to co-opt pathways that originally developed for other plant– microbe interactions. As Bird mentions, intriguing parallels exist between signals and developmental events that underlie the plant interactions with both nematodes and rhizobia. Although plants have evolved mechanisms to control pathogens, they may be less well equipped to avoid secondary exploitation by epiparasites. As described by Leake (pp. 422–428), the use of molecular taxonomy techniques has provided new insights into mycoheterophic interactions, revealing the identity of the fungi from which these achlorophyllous plants steal carbon. Surprisingly, the very specialized achlorophyllous plants have chosen to parasitize AM and ectomycorrhizal fungi, symbionts that have a direct carbon pipeline to their plant partners. Such are the hidden costs to the plant of developing mycorrhizal symbioses. Signal deception appears to be rampant in a plant’s interactions with bacteria and pollinators. Bauer and Mathesius (pp. 429–433) discuss how bacteria use quorum-sensing signals to orchestrate infections of multi-cellular organisms. Plants not only respond to these bacterial signals but produce their own quorum-sensing mimics, and actively disrupt these signals in a process called ‘quorum quenching’, presumably to disrupt the communication network in the surrounding bacterial communities. The remarkable achievements in this field have, to a large extent, been made possible by the remarkable convergence on a relatively small number of microbial signals. Deceptive signaling, albeit on a larger spatial scale, is lucidly illustrated in the first Current www.sciencedirect.com
Editorial overview Harrison and Baldwin 355
Opinion in Plant Biology review on plant–pollinator interactions by Raguso (pp. 434–440). He details how plant’s mimicry of the pheromones and posture of female wasps attracts male wasps to the flowers of particular orchids, and how the characteristic odors of decaying flesh attract carrion blowflies. The benefits of finding unmated females and carrion seem to overwhelm the costs of the occasional floral visit and are responsible for maintaining this resource-deception mechanism for pollination. Chemical fragrances are not the only signals involved in pollination signaling: the echo fingerprints of flowers provide valuable information to the sonar-based sensory system of bats. The simplistic view that plant responses to microbial interactors are mediated by a small number of smallmolecular-weight hormones (including SA, jasmonic acid [JA] and ethylene) has given way to a more inclusive view. According to this view, many of the signals and secondary messengers that are known from animal systems, including redox signals, are involved, as are a selection of novel plant-specific signals. Interest in jasmonates and other oxylipins that are produced by the enzymatic peroxidation of fatty acids erupted when these signals were found to profoundly mediate resistance against a wide range of chewing insects and certain microbial pathogens. The spectrum of potential signals has exploded with the recognition that many free-radical-produced nonenzymatic oxilipins, some of which are produced by reactive oxygen species (ROS)-mediated stress responses, are elicitors of defense responses (reviewed by Mueller [pp. 441–448]). Many of these nonenzymatically generated oxilipins are toxic. They not only may represent the first line of defense against microbial invasion but also have evolved a subsequent signaling function as indicators of membrane damage. Lipid signals are implicated in systemic acquired resistance (SAR) against pathogens and insects, and with the identification of the phytoprostanes, the array of possible signaling pathways that involve lipids is daunting. It is now established that NO signaling interacts with SA and JA signaling, two fundamental pathways that mediate pathogen and insect resistance (reviewed by Wendehenne et al. [pp. 449–455]). Three second
www.sciencedirect.com
messengers (i.e. guanylate cyclase, cyclic ADP ribose and Caþ2) are known to mediate NO signaling responses. NO signaling appears to inhibit the wound-induced H2O2 burst, and thereby inhibits the ROS-associated HR. When activated in conjunction with H2O2 production, however, NO signaling activates programmed cell death. In addition to NO’s role in mediating cross-talk between pathways involving the established phytohormones, NON-EXPRESSOR OF PATHOGENESISRELATED GENES1 (NPR1), which was previously shown to mediate SA signaling, is now known to play different roles in the nucleus and the cytosol in mediating SA signaling and SA–JA signal interactions, as reviewed by Pieterse and Van Loon (pp. 456–464). The AP2 family of transcription factors, which mediates many of the small phytohormone responses, particularly ethylene signaling, is reviewed by Gutterson and Reuber (pp. 465–471) from a phylogenetic perspective. Such a perspective highlights the structural elements that are likely to confer specialized function within plant lineages. ROS-mediated programmed cell death, which is so frequently invoked in both offensive and defense responses in plant–pathogen interactions, may also be involved in some plant–plant allelopathic interactions. As reviewed by Weir et al. (pp. 472–479), particular flavonoids that are secreted into the rhizosphere by allelopathic plants can elicit ROS-mediated cell death in susceptible plants, providing a potential mechanism for this form of chemical warfare between plants. Allelopathic interactions are immensely complicated, and mutant plants that are unable to secrete the putative allelochemicals are sorely needed to determine whether allelopathy occurs under ecologically realistic conditions. In short, the reviews in this issue portray a plant’s biotic interactions as comparable to a complicated espionage plot imagined by the best spy/thriller writers of the day. A valuable spin-off of the mechanism-focused research reviewed in this issue would be to generate mutants and to identify signals that could be used to manipulate these complicated interactions in nature. We might just learn that nature tells a tale more ripe with intrigue than the paranoid conspiracy-theory-evoking human mind could ever weave.
Current Opinion in Plant Biology 2004, 7:353–355