Herbivores, Vascular Pathways, and Systemic Induction: Facts and Artifacts
Article First Online: 28 September 2005 Received: 22 March 2004 Revised: 01 December 2004 Accepted: 18 May 2005 Abstract
Over the past 10 years there has been tremendous growth in our understanding of molecular, chemical, and morphological induction of traits involved in the resistance of plants to herbivores. Although it is well established that the patterns of induction can be constrained by a plant's vascular architecture, studies often fail to account for these constraints. Failure to do so has the potential to severely underestimate both the patterns and extent of induction. Here I review (1) the evidence for vascular control of induced responses, (2) how interspecific variation in phyllotaxy influences spatial patterning of induction, (3) the factors, phloem transport and volatile production, that may break down vascular constraints and lead to more widespread induction, and (4) the experimental approaches that could be compromised when vascular architecture is not considered. I show that vascular constraints in systemic induction are commonplace, but vary among species. I suggest that when induction is more widespread than expected from patterns of phyllotaxy, differences in vascular connectivity and volatile production may be responsible. I argue that advances in the mechanisms of systemic induction, cross-talk between different signal transduction pathways, specificity of induction, costs and benefits of systemic induction, and the effects of induced changes on herbivores and their natural enemies require that experiments be designed to examine and/or control for vascular constraints in systemic induction.
Key Words Systemic induction vascular architecture sectoriality long-distance transport source–sink dynamics volatiles experimental design References Agrawal, A. A. 2000 Specificity of induced resistance in wild radish: causes and consequences for two specialist and two generalist caterpillars Oikos 89 493 500 CrossRef Google Scholar Agrawal, A. A., Karban, R. 1999 Why induced defenses may be favored over constitutive strategies in plants Tollrian, R. Harvell, C. D. eds. The Ecology and Evolution of Inducible Defenses Princeton University Press Princeton 45 61 Google Scholar Agrawal, A. A., Gorski, P. M., Tallamy, D. W. 1999 Polymorphism in plant defense against herbivory: Constitutive and induced resistance in Cucumis sativus J. Chem. Ecol. 25 2285 2304 CrossRef Google Scholar Arnold, T. M., Schultz, J. C. 2002 Induced sink strength as a prerequisite for induced tannin biosynthesis in developing leaves of Populus Oecologia 130 585 593 CrossRef Google Scholar Arnold, T. M., Appel, H., Patel, V., Stocum, E., Kavalier, A., Schultz, J. 2004 Carbohydrate translocation determines the phenolic content of Populus foliage: a test of the sink–source model of plant defense New Phytol. 164 157 164 CrossRef Google Scholar Baldwin, I. T. 1988 The alkaloidal responses of wild tobacco to real and simulated herbivory Oecologia 77 378 381 CrossRef Google Scholar Baldwin, I. T., Sims, C. L., Kean, S. E. 1990 The reproductive consequences associated with inducible alkaloidal responses in wild tobacco Ecology 71 252 262 Google Scholar Baldwin, I. T., Gorham, D., Schmelz, E. A., Lewandowski, C. A., Lynds, G. Y. 1998 Allocation of nitrogen to an inducible defense and seed production in Nicotiana attenuata Oecologia 115 541 552 CrossRef Google Scholar Cipollini, D. 2002 Does competition magnify the fitness costs of induced responses in Arabidopsis thaliana? A manipulative approach Oecologia 131 514 520 CrossRef Google Scholar Cipollini, D. F., Redman, A. M. 1999 Age-dependent effects of jasmonic acid treatment and wind exposure on foliar oxidase activity and insect resistance in tomato J. Chem. Ecol. 25 271 281 CrossRef Google Scholar Constabel, C. P., Yip, L., Patton, J. J., Christopher, M. E. 2000 Polyphenol oxidase from hybrid poplar. Cloning and expression in response to wounding and herbivory Plant Physiol. 124 285 295 CrossRef PubMed Google Scholar Davis, M. A., Gordon, M. P., Smit, B. A. 1991 Assimilate movement dictates remote sites ofwound-induced gene expression in poplar leaves Proc. Natl. Acad. Sci. USA 88 2393 2396 PubMed Google Scholar Moraes, C. M., Mescher, M. C., Tumlinson, J. H. 2001 Caterpillar-induced nocturnal plant volatiles repel conspecific females Nature 419 531 577 Google Scholar Denno, R. F. McClure, M. S. eds. 1983Variable Plants and Herbivores in Natural and Managed Systems Academic Press New York Google Scholar Dicke, M., Agrawal, A. A., Bruin, J. 2003 Plants talk, but are they deaf? Trends Plant Sci. 8 403 405 CrossRef PubMed Google Scholar Dickson, R. 1991 Carbon fixation and distribution in young Populus trees Raghavendra, A. S. eds. Physiology of Trees John Wiley and Sons, Inc. New York 51 85 Google Scholar Dickson, R. E., Isebrands, J. G. 1991 Leaves as regulators of stress response Mooney, H. A. Winner, W. E. Pell, E. J. eds. Response of Plants to Multiple Stresses Academic Press Inc. San Diego 3 34 Google Scholar Farmer, E. E. 2001 Surface-to-air signals Nature 411 854 856 Google Scholar Fisher, D. B. 2000 Long-distance transport Buchanan, B. B. Gruissem, W. Jones, R. L. eds. Biochemistry and Molecular Biology of Plants American Society of Plant Physiologists Rockville, MD 730 784 Google Scholar Haukioja, E. 1990 Induction of defenses in trees Annu. Rev. Entomol. 36 25 42 CrossRef Google Scholar Heil, M., Baldwin, I. T. 2002 Fitness costs of induced resistance: Emerging experimental support for a slippery concept Trends Plant Sci. 7 61 67 CrossRef PubMed Google Scholar Ishiwatari, Y., Fujiwara, T., McFarland, K. C., Nemoto, K., Hayashi, H., Chino, M., Lucas, W. J. 1998 Rice phloem thioredoxin h has the capacity to mediate its own cell-to cell transport through plasmodesmata Planta 205 12 22 CrossRef PubMed Google Scholar Jones, C. G., Hopper, R. F., Coleman, J. S., Krischik, V. A. 1993 Control of systematically induced herbivore resistance by plant vascular architecture Oecologia 93 452 456 CrossRef Google Scholar Karban, R. 1986 Induced resistance against spider mites in cotton: Field verification Entomol. Exp. Appl. 42 239 242 CrossRef Google Scholar Karban, R. 1987 Environmental conditions affecting the strength of induced resistance against mites in cotton Oecologia 73 414 419 CrossRef Google Scholar Karban, R., Baldwin, I. T. 1997Induced Responses to Herbivory University of Chicago Press Chicago Google Scholar Karban, R., Myers, J. H. 1989 Induced plant responses to herbivory Annu. Rev. Ecol. Syst. 20 331 348 CrossRef Google Scholar Karban, R., Baldwin, I. T., Baxter, K. J., Laue, G., Felton, G. W. 1997 Communication between plants: induced resistance in wild tobacco plants following clipping of neighboring sagebrush Oecologia 125 66 71 Google Scholar Kessler, A., Baldwin, I. T. 2001 Defensive function of herbivore-induced plant volatile emissions in nature Science 291 2141 2144 CrossRef PubMed Google Scholar Kiefer, I. W., Slusarenko, A. J. 2003 The pattern if systemic acquired resistance induction within the Arabidopsis rosette in relation to the pattern of translocation Plant Physiol. 132 840 847 CrossRef PubMed Google Scholar Larson, P. R. 1977 Phyllotactic transitions in the vascular system of Populus deltoides Bartr. as determined by 14C labeling Planta 134 241 249 CrossRef Google Scholar Lerdau, M. 2002 Plants talk—but can they listen? Science 298 361 CrossRef Google Scholar Lucas, W. J. 1997 Application of microinjection techniques to plant nutrition Plant Soil 196 175 189 CrossRef Google Scholar Malone, M., Alarcon, J.-J. 1995 Only xylem-borne factors can account for systemic wound signaling in the tomato plant Planta 196 740 746 CrossRef Google Scholar Marshall, C. 1996 Sectoriality and physiological organisation in herbaceous plants: an overview Vegetatio 127 9 16 CrossRef Google Scholar Minchin, P. E. H., Thorpe, M. R. 1984 Apoplastic phloem unloading in the stem of bean Phaseolis-vulgaris J. Exp. Bot. 35 538 550 Google Scholar Minchin, P. E. H., Thorpe, M. R. 1987 Measurement of unloading and reloading of photo-assimilate within the stem of bean J. Exp. Bot. 38 211 220 Google Scholar
Moore, R., Clark, W. D., and Vodopich, D. S. 1998. pp. 314–315,
Botany, 2nd edn. WCB/McGraw-Hill, Dubuque, IA.
Google Scholar Moran, P. J., Thompson, G. A. 2001 Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways Plant Physiol. 125 1074 1085 CrossRef PubMed Google Scholar Murray, B. J., Mauk, C., NoodÉn, L. D. 1982 Restricted vascular pipelines (and orthostichies) in plants What's New Plant Physiol. 13 33 36 Google Scholar Mutikainen, P., Walls, M., Ovaska, J. 1996 Herbivore-induced resistance in Betula pendula: the role of plant vascular architecture Oecologia 108 723 727 CrossRef Google Scholar Orians, C. M., Jones, C. G. 2001 Plants as resource mosaics: a functional model for predicting patterns of within-plant resource heterogeneity to consumers based on vascular architecture and local environmental variability Oikos 94 493 504 CrossRef Google Scholar Orians, C. M., Pomerleau, J., Ricco, R. 2000 Vascular architecture generates fine scale variation in the systemic induction of proteinase inhibitors in tomato J. Chem. Ecol. 26 471 485 CrossRef Google Scholar Orians, C. M., Babst, B., Zanne, A. E. 2005 Vascular constraints and long-distance transport in dicots Holbrook, N. M. Zwieniecki, M. eds. Vascular Transport in Plants Elsevier/AP co-imprint Oxford Google Scholar Pate, J. S., Dieter Jeschke, W. 1995 Role of stems in transport, storage, and circulation of ions and metabolites by the whole plant Gartner, B. L. eds. Plant Stems: Physiology and Functional Morphology Academic Press San Diego 177 204 Google Scholar Preston, K. A. 1998 The effects of developmental stage and source leaf position on integration and sectorial patterns of carbohydrate movement in an annual plant, Perilla frutescens (Lamiaceae) Am. J. Bot. 85 1695 1703 Google Scholar Redman, A. M., Cipollini, D., Schultz, J. C. 2001 Fitness costs of jasmonic acid-induced defense in tomato, Lycopersicon esculentum Oecologia 126 380 385 CrossRef Google Scholar Rhodes, J. D., Thain, J. F., Wildon, D. C. 1999 Evidence for physically distinct systemic signaling pathways in the wounded tomato plant Ann. Bot. 84 109 116 CrossRef Google Scholar Ruiz-Medrano, R., Xoconostle-Cazares, B., Lucas, W. J. 1999 Phloem long-distance transport of CmNACP mRNA: implications for supracellular regulation in plants Development 126 4405 4419 PubMed Google Scholar Ruiz-Medrano, R., Xoconostle-Cazares, B., Kragler, F. 2004 The plasmodesmatal transport pathway for homeotic proteins, silencing signals and viruses Curr. Opin. Plant Biol. 7 641 650 CrossRef PubMed Google Scholar Sachs, T., Novoplansky, A., Cohen, D. 1993 Plants as competing population of redundant organs Plant Cell Environ. 16 765 770 Google Scholar Schittko, U., Baldwin, I. T. 2003 Constraints to herbivore-induced systemic responses: bidirectional signaling along orthostichies in Nicotiana attenuata J. Chem. Ecol. 29 763 770 CrossRef PubMed Google Scholar Schittko, U., Preston, C. A., Baldwin, I. T. 2000 Eating the evidence? Manduca sexta larvae cannot disrupt specific jasmonate induction in Nicotiana attenuata by rapid consumption Planta 21 343 346 Google Scholar Shea, M. M., Watson, M. A. 1989 Patterns of leaf and flower removal: their effect on fruit growth in Chamaenerion angustifolium (fireweed) Am. J. Bot. 76 884 890 Google Scholar Shulaev, V., Leon, J., Raskin, I. 1995 Is salicylic acid a translocated signal of systemic acquired resistance in tobacco? Plant Cell 7 1691 1701 CrossRef PubMed Google Scholar Stout, M. J., Workman, K. V., Duffey, S. S. 1996a Identity, spatial distribution, andvariability of induced chemical responses in tomato plants Entomol. Exp. Appl. 79 255 271 CrossRef Google Scholar Stout, M. J., Workman, K. V., Workman, J. S., Duffey, S. S. 1996b Temporal and ontogenetic aspects of protein induction in foliage of the tomato, Lycopersicon esculentum Biochem. Syst. Ecol. 24 1 16 CrossRef Google Scholar StratmaNn, J. W. 2003 Long-distance run in the wound response—jasmonic acid is pulling ahead Trends Plant Sci. 8 247 250 CrossRef PubMed Google Scholar Thaler, J. S. 1999 Induced resistance in agricultural crops: Effects of jasmonic acid on herbivory and yield in tomato plants Environ. Entomol. 28 30 37 Google Scholar Thaler, J. S. 1999 Jasmonate-inducible plant defences cause increased parasitism of herbivores Nature 399 686 688 CrossRef Google Scholar Thaler, J. S., Fidantsef, A. L., Duffey, S. S., Bostock, R. M. 1999 Trade-offs in plant defense against pathogens and herbivores: A field demonstration of chemical elicitors of induced resistance J. Chem. Ecol. 25 1597 1609 CrossRef Google Scholar Thaler, J. S., Karban, R., Ullman, D. E., Boege, K., Bostock, R. M. 2002 Cross-talk between jasmonate and salicylate plant defense pathways: effects on several plant parasites Oecologia 131 235 277 Google Scholar Thomma, B. P. H. J., Eggermont, K., Penninckx, I. A. M. A., Mauch-Mani, B., Vogelsang, R., Cammue, B. P. A., Broekaert, W. F. 1998 Separate jasmonate-dependent and salicylate-dependent defense–response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens Proc. Natl. Acad. Sci. USA 95 15107 15111 CrossRef PubMed Google Scholar Thorpe, M., Minchin, P., Gould, N., McQueen, J. 2005 The stem apoplast: A potential communication channel in plant growth regulation Holbrook, N. M. Zwieniecki, M. eds. Vascular Transport in Plants Elsevier/AP co-imprint Oxford Google Scholar Traw, M. B., Dawson, T. E. 2002 Differential induction of trichomes by three herbivores of black mustard Oecologia 131 526 532 CrossRef Google Scholar Bel, A. J. E., Ehlers, K., Knoblauch, M. 2002 Sieve elements caught in the act Trends Plant Sci. 7 126 132 CrossRef PubMed Google Scholar Bel, A. J. E. 2003 Transport phloem: Low profile, high impact Plant Physiol. 131 1509 1510 PubMed Google Scholar Dam, N. M., Horn, M., Mares, M., Baldwin, I. T. 2001 Ontogeny constrains systemic protease inhibitor response in Nicotiana attenuata J. Chem. Ecol. 27 547 568 CrossRef PubMed Google Scholar Poecke, R., Posthumus, M. P., Dicke, M. A. 2001 Herbivore-induced volatile production by Arabidopsis thaliana leads to attraction of the parasitoid Cotesia rebucula: chemical, behavioral, and gene-expression analysis J. Chem. Ecol. 27 1911 1928 CrossRef PubMed Google Scholar Viswanathan, D. V., Thaler, J. S. 2004 Plant vascular architecture and within-plant spatial patterns in resource quality following herbivory J. Chem. Ecol. 30 531 543 CrossRef PubMed Google Scholar Voelckel, C., Baldwin, I. T. 2004 Generalist and specialist lepidopteran larvae elicit different transcriptional responses in Nicotiana attenuata, which correlate with larval FAC profiles Ecol. Lett. 7 70 775 CrossRef Google Scholar Walling, L. L. 2000 The myriad plant responses to herbivores J. Plant Growth Regul. 19 195 216 PubMed Google Scholar Watson, M. A. 1986 Integrated physiological units in plants TREE 1 119 123 Google Scholar Watson, M. A., Casper, B. B. 1984 Morphogenetic constraints on patterns of carbon distribution in plants Annu. Rev. Ecol. Syst. 15 233 258 CrossRef Google Scholar Zavala, J. A., Baldwin, I. T. 2004 Fitness benefits of trypsin proteinase inhibitor expression in Nicotiana attenuata are greater than their costs when plants are attacked BMC Ecol. 4 1 15 CrossRef PubMed Google Scholar Zavala, J. A., Patankar, A., Gase, K., Baldwin, I. T. 2004 Constitutive and inducible trypsin proteinase inhibitor production incurs large fitness costs in Nicotiana attenuata Proc. Natl. Acad. Sci. USA 101 1607 1612 CrossRef PubMed Google Scholar Zhang, Z. P., Baldwin, I. T. 1997 Transport of [2-C-14]jasmonic acid from leaves to roots mimics wound-induced changes in endogenous jasmonic acid pools in Nicotiana sylvestris Planta 203 436 441 CrossRef Google Scholar Zwieniecki, M. A., Orians, C. M., Melcher, P. J., Holbrook, N. M. 2003 Ionic control of lateral exchange of water between vascular bundles in tomato J. Exp. Bot. 54 1399 1406 CrossRef PubMed Google Scholar Copyright information
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