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Plant Physiology 146:801-803 (2008)
© 2008 American Society of Plant Biologists

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EDITORIALS - FOCUS ISSUE

Plant Interactions with Arthropod Herbivores: State of the Field

Georg Jander and Gregg Howe

Monitoring Editors
Plant Physiology

Interactions between plants and their arthropod herbivores dominate the terrestrial ecology of our planet. The survival of an estimated one million or more phytophagous insect species depends on plants as a source of food. Plant-eating arthropods employ sophisticated feeding strategies to obtain nutrients from all aboveground and belowground plant parts. Rather than being passive victims in these interactions, plants cope with herbivory through the production of myriad specialized metabolites and proteins that exert toxic, repellent, or antinutritive effects on their animal attackers (see Zhu-Salzman et al., 2008Go). The co-evolutionary struggle between arthropod herbivores and plants to consume or not to be consumed, respectively, has shaped not only the extraordinary diversity of plant metabolism, but also the genetic diversity of plants.

The central role of plant chemicals in mediating interactions with arthropod herbivores has attracted the attention of insect physiologists and population ecologists for more than 50 years (see Berenbaum and Zangerl, 2008Go). Widespread interest in this field among plant biologists, however, can be traced back to 1972, when Clarence "Bud" Ryan (Fig. 1 ) and colleagues at Washington State University reported that insect feeding on potato and tomato plants activates local and systemic expression of proteinase inhibitors that disrupt the activity of digestive proteases in the insect gut (Green and Ryan, 1972Go). This seminal discovery was instrumental in establishing the paradigm that plant defense responses to herbivore attack are rapid and highly dynamic. The general theme of induced resistance runs through much, if not most, plant-insect interaction research published in Plant Physiology. Remarkable progress in understanding plant relations with arthropod herbivores has been achieved in the recent past; these advances were the genesis of this Focus Issue.


Figure 1
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  		Figure 1. Clarence "Bud" Ryan (1931–2007). Photograph courtesy of Washington State University.

 
Plant-herbivore interaction research is arguably one of the most multidisciplinary endeavors in plant biology. Like all research concerned with inter-species relationships, numerous disciplines are required to accurately describe the range of chemical and ecological processes that influence the outcome of plant-herbivore interactions. A defining aspect of the field has been its focus on animals as the "other organism." The complexity of animal behavior, together with the technical difficulties associated with genetic manipulation of plant-eating animals, poses unique but not insurmountable challenges. As discussed in Updates by Zheng and Dicke (2008)Go and by Schwachtje and Baldwin (2008)Go, an important research trend is the use of plant-insect systems to address questions of ecological relevance. The merging of molecular and ecological disciplines offers a powerful approach to understand gene function and evolution in an ecological context.

Much of contemporary plant-herbivore interaction research is focused on understanding the molecular mechanisms and ecological consequences of induced plant responses to herbivory. In their Update, Mithöfer and Boland (2008)Go discuss the early signaling events at the plant-herbivore interface. Wu et al. (2008)Go show that there can be significant within-species differences in these early signaling responses. Frost et al. (2008)Go describe molecular and ecological aspects of defense "priming," which has become an important area of research. In her Update, Walling (2008)Go describes various mechanisms by which insects evade host defense responses, thereby highlighting the co-evolutionary nature of plant-herbivore relations.

It is now clear that the jasmonate (JA) family of lipid-derived signals plays a prominent and conserved role in promoting plant resistance to herbivores. Browse and Howe (2008)Go discuss these roles, as well as recent progress in elucidating the mechanism of JA signaling. One notable recent discovery is that an amino acid-conjugated form of JA, JA-Ile, is a bioactive signal for defense responses and a potential ligand for the JA receptor. An article by Wang et al. (2008)Go indicates that JA and JA-Ile serve distinct (but overlapping) roles in defense. Chung et al. (2008)Go show that the levels of both JA and JA-Ile increase within 5 min of mechanical tissue damage, and provide genetic evidence that the JAZ proteins, which negatively regulate JA responses, play a role in regulating host plant resistance to herbivory. An article by Arimura et al. (2008)Go shows that the temporal pattern of leaf damage plays a critical role in the emission of plant volatiles that attract natural enemies of the herbivore, and that JA is likely involved in the control of this response. Lin et al. (2008)Go in this issue show how genome duplication allowed neofunctionalization of a terpene synthase that contributes to herbivore-induced volatile release. In an article by Jassbi et al. (2008)Go, direct antifeedant effects of diterpenoids are demonstrated through insect bioassays involving plants that are silenced in the expression of these compounds. Koornneef and Pieterse (2008)Go discuss recent progress in our understanding of how JA and other signaling pathways influence the outcome of plant-pest interactions. The phenomenon of signal cross talk in plant biology has gained increased attention as scientists seek to understand how plants respond to simultaneous attack by multiple herbivores and pathogens. A novel example of signal cross talk is described in an article by Runyon et al. (2008)Go, who examined how the parasitic plant Cuscuta pentagona affects induced defenses of tomato to insect attack.

Model plant systems, together with the increasing use of mutants that are affected in their interactions with arthropod herbivores, have contributed greatly to recent progress in the field. An article by de Vos et al. (2008)Go in this issue illustrates the value of Arabidopsis thaliana mutants for studying the role of small molecules in plant-insect interactions. In their forward-looking view of the future of plant-insect interaction research, Berenbaum and Zangerl (2008)Go argue convincingly that a deep understanding of chemical-mediated plant-insect interactions will require analysis of phylogenetically diverse species that extends beyond the current repertoire of model plant systems. It will also be important to learn more about the interaction of arthropod attackers with belowground plant tissues. Two Updates, one by Erb et al. (2008)Go and the other by Rasmann and Agrawal (2008)Go, are devoted to the theme of belowground herbivory.

As is the case with all areas of plant biology, modern "omics" approaches have also facilitated rapid progress in research on plant-arthropod interactions. These tools have provided an unprecedented opportunity to study large-scale changes in herbivore-induced plant processes in a relatively unbiased manner. An article by Gao et al. (2008)Go in this issue is the first report on a plant insect-interaction where both organisms, in this case, Acyrthosiphon pisum (pea aphid) and Medicago truncatula, are the subject of ongoing genome sequencing projects. Rapid advances in DNA sequencing technology will bring research on this and other plant-herbivore model systems to a new level by making it possible to do genetic and genomic studies on both sides of the interaction.

Another important theme in research on plant-arthropod interactions is the control of herbivory on crop plants. An Update by Gatehouse (2008)Go in this issue highlights advances in transgenic approaches for creating insect-resistant crops. Enthusiasm for the use of plant proteinase inhibitors for crop protection has been tempered by the realization that insects have the capacity to synthesize, on demand, gut proteases that are insensitive to plant-derived inhibitors. A research article by Goulet et al. (2008)Go describes targeted engineering of plant cystatins to provide greater efficacy against insect digestive proteases. Major and Constabel (2008)Go describe the functional and biochemical variability of Kunitz trypsin inhibitor genes of hybrid poplar, which may provide a starting point for similar engineering efforts in tree species.

We hope that this Focus Issue conveys to readers the fact that plant-herbivore interaction research, while still in its infancy, is a rapidly moving multidisciplinary field with strong roots and a bright future. For that, we owe much to Bud Ryan, a founding father of this field, and we are deeply saddened by his recent passing. Bud's pioneering work on plant proteinase inhibitors (Ryan, 1990Go), induced resistance to herbivory (Green and Ryan, 1972Go), and peptide-signaled defense responses (Pearce et al., 1991Go) inspired several generations of biologists to pursue the study of plant-insect interactions. The impact of Bud's work is readily discernible in each of the articles contributed to this Focus Issue. For these reasons, we would like to dedicate this Focus Issue to the memory of Bud Ryan.

Finally, we would like to thank the many authors, reviewers, and Plant Physiology staff who were involved in the publication of this Focus Issue.


   FOOTNOTES
 
www.plantphysiol.org/cgi/doi/10.1104/pp.104.900247


   LITERATURE CITED
TOP
 LITERATURE CITED
 
Arimura G-I, Köpke S, Kunert M, Volpe V, David A, Brand P, Dabrowska P, Maffei ME, Boland W (2008) Effects of feeding Spodoptera littoralis on lima bean leaves: IV. Diurnal and nocturnal damage differentially initiate plant volatile emission. Plant Physiol 146: 965–973

Berenbaum MR, Zangerl AR (2008) Facing the future of plant-insect interaction research: le retour à la "raison d'être". Plant Physiol 146: 804–811

Browse J, Howe GA (2008) New weapons and a rapid response against insect attack. Plant Physiol 146: 832–838

Chung HS, Koo AJK, Gao X, Jayanty S, Thines B, Jones AD, Howe GA (2008) Regulation and function of Arabidopsis JASMONATE ZIM-domain genes in response to wounding and herbivory. Plant Physiol 146: 952–964

de Vos M, Kriksunov KL, Jander G (2008) Indole-3-acetonitrile production from indole glucosinolates deters oviposition by Pieris rapae. Plant Physiol 146: 916–926

Erb M, Ton J, Degenhardt J, Turlings TCJ (2008) Interactions between arthropod-induced aboveground and belowground defenses in plants. Plant Physiol 146: 867–874

Frost CJ, Mescher MC, Carlson JE, De Moraes CM (2008) Plant defense priming against herbivores: getting ready for a different battle. Plant Physiol 146: 818–824

Gao L-L, Klingler JP, Anderson JP, Edwards OR, Singh KB (2008) Characterization of pea aphid resistance in Medicago truncatula. Plant Physiol 146: 996–1009

Gatehouse JA (2008) Biotechnological prospects for engineering insect-resistant plants. Plant Physiol 146: 881–887

Goulet M-C, Dallaire C, Vaillancourt L-P, Khalf M, Badri AM, Preradov A, Duceppe M-O, Goulet C, Cloutier C, Michaud D (2008) Tailoring the specificity of a plant cystatin toward herbivorous insect digestive cysteine proteases by single mutations at positively selected amino acid sites. Plant Physiol 146: 1010–1019

Green TR, Ryan CA (1972) Wound-induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects. Science 175: 776–777[Abstract/Free Full Text]

Jassbi AR, Gase K, Hettenhausen C, Schmidt A, Baldwin IT (2008) Silencing geranylgeranyl diphosphate synthase in Nicotiana attenuata dramatically impairs resistance to tobacco hornworm. Plant Physiol 146: 974–986

Koornneef A, Pieterse CMJ (2008) Cross talk in defense signaling. Plant Physiol 146: 839–844

Lin C, Shen B, Xu Z, Kollner TG, Degenhardt J, Dooner HK (2008) Characterization of the monoterpene synthase gene tps26, the ortholog of a gene induced by insect herbivory in maize. Plant Physiol 146: 940–951

Major IT, Constabel CP (2008) Functional analysis of the Kunitz trypsin inhibitor family in poplar reveals biochemical diversity and multiplicity in defense against herbivores. Plant Physiol 146: 888–903

Mithöfer A, Boland W (2008) Recognition of herbivory-associated molecular patterns. Plant Physiol 146: 825–831

Pearce G, Strydom D, Johnson S, Ryan CA (1991) A polypeptide from tomato leaves induces wound-inducible proteinase-inhibitor proteins. Science 253: 895–898[Abstract/Free Full Text]

Rasmann S, Agrawal AA (2008) In defense of roots: a research agenda for studying plant resistance to belowground herbivory. Plant Physiol 146: 875–880

Runyon JB, Mescher MC, De Moraes CM (2008) Parasitism by Cuscuta pentagona attenuates host plant defenses against insect herbivores. Plant Physiol 146: 987–995

Ryan CA (1990) Protease inhibitors in plants: genes for improving defenses against insects and pathogens. Annu Rev Phytopathol 28: 425–449[Web of Science]

Schwachtje J, Baldwin IT (2008) Why does herbivore attack reconfigure primary metabolism? Plant Physiol 146: 845–851

Walling LL (2008) Avoiding effective defenses: strategies employed by phloem-feeding insects. Plant Physiol 146: 859–866

Wang L, Allmann S, Wu J, Baldwin IT (2008) Comparisons of LIPOXYGENASE3- and JASMONATE-RESISTANT4/6-silenced plants reveal that jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore resistance of Nicotiana attenuata. Plant Physiol 146: 904–915

Wu J, Hettenhausen C, Schuman MC, Baldwin IT (2008) A comparison of two Nicotiana attenuata accessions reveals large differences in signaling induced by oral secretions of the specialist herbivore Manduca sexta. Plant Physiol 146: 927–939

Zheng S-J, Dicke M (2008) Ecological genomics of plant-insect interactions: from gene to community. Plant Physiol 146: 812–817

Zhu-Salzman K, Luthe DS, Felton GW (2008) Arthropod-inducible proteins: broad spectrum defenses against multiple herbivores. Plant Physiol 146: 852–858





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