Before gene expression: early events in plant–insect interaction
2007, Trends in Plant Science
https://doi.org/10.1016/J.TPLANTS.2007.06.001Abstract
Successful defense depends on the ability of the plant to recognize an attacking 'enemy' as early as possible. Early defense responses require enemy-initiated signaling cascades. Their activation ensures an induced response that is quantitative, timely and coordinated with other activities of the host cells. Damage-induced ion imbalances and modulations of channel activities are the first events occurring in the plasma membrane and result in rapid perturbations of the plasma membrane potential (V m ) involving variations of cytosolic Ca 2+ concentrations. Interacting downstream networks of kinases and phytohormones mediate the signal and result in concerted gene activation. Here we review and discuss early events occurring before herbivore attack-related gene expression that are responsible for cascades of events and signal transductions, eventually leading to indirect and direct plant responses.
References (73)
- Reymond, P. et al. (2004) A conserved transcript pattern in response to a specialist and a generalist herbivore. Plant Cell 16, 3132- 3147
- Mitho ¨fer, A. et al. (2005) Effects of feeding Spodoptera littoralis on lima bean leaves. II. Continuous mechanical wounding resembling insect feeding is sufficient to elicit herbivory-related volatile emission. Plant Physiol. 137, 1160-1168
- Shabala, S. (2006) Non-invasive microelectrode ion flux measurements in plant stress physiology. In Plant Electrophysiology -Theory and Methods (Volkov, A., ed.), pp. 35-71, Springer-Verlag
- Ebel, J. and Mitho ¨fer, A. (1998) Early events in the elicitation of plant defence. Planta 206, 335-348
- Maffei, M. and Bossi, S. (2006) Electrophysiology and plant responses to biotic stress. In Plant Electrophysiology -Theory and Methods (Volkov, A., ed.), pp. 461-481, Springer-Verlag
- Volkov, A. and Brown, C.L. (2006) Electrochemistry of plant life. In Plant Electrophysiology -Theory and Methods (Volkov, A., ed.), pp. 437-459, Springer-Verlag
- Wildon, D.C. et al. (1992) Electrical signalling and systemic proteinase inhibitor induction in the wounded plant. Nature 360, 62-65
- Musser, R.O. et al. (2005) Evidence that the caterpillar salivary enzyme glucose oxidase provides herbivore offense in Solanaceous plants. Arch. Insec. Biochem. 58, 128-137
- Peiffer, M. and Felton, G.W. (2005) The host plant as a factor in the synthesis and secretion of salivary glucose oxidase in larval Helicoverpa zea. Arch. Insec. Biochem. 58, 106-113
- Nu ¨rnberger, T. et al. (1994) High affinity binding of a fungal oligopeptide elicitor to parsley plasma membranes triggers multiple defense responses. Cell 78, 449-460
- Mitho ¨fer, A. et al. (2005) Cation fluxes cause plasma membrane depolarization involved in beta-glucan elicitor-signaling in soybean roots. Mol. Plant Microbe Interact. 18, 983-990
- Shibuya, N. and Minami, E. (2001) Oligosaccharide signalling for defence responses in plant. Physiol. Mol. Plant Pathol. 59, 223-233
- Maischak, H. et al. (2007) Oral secretions from herbivorous lepidopteran larvae exhibit ion channel-forming activities. FEBS Lett. 581, 898-904
- Maffei, M. et al. (2004) Effects of feeding Spodoptera littoralis on lima bean leaves. I. Membrane potentials, intracellular calcium variations, oral secretions, and regurgitate components. Plant Physiol. 134, 1752- 1762
- Alborn, H. et al. (1997) An elicitor of plant volatiles from beet armyworm oral secretion. Science 276, 945-949
- Schmelz, E.A. et al. (2006) Fragments of ATP synthase mediate plant perception of insect attack. Proc. Natl. Acad. Sci. U. S. A. 103, 8894- 8899
- White, P.J. (2000) Calcium channels in higher plants. BBA- Biomembranes 1465, 171-189
- Lecourieux, D. et al. (2006) Calcium in plant defence-signalling pathways. New Phytol. 171, 249-269
- Evans, N.H. et al. (2001) Calcium oscillations in higher plants. Curr. Opin. Plant Biol. 4, 415-420
- Sanders, D. et al. (2002) Calcium at the crossroads of signaling. Plant Cell 14, S401-S417
- Reddy, V.S. and Reddy, A.S.N. (2004) Proteomics of calcium-signaling components in plants. Phytochemistry 65, 1745-1776
- Jonak, C. et al. (2002) Complexity, cross talk and integration of plant MAP kinase signalling. Curr. Opin. Plant Biol. 5, 415-424
- Arimura, G. et al. (2002) Herbivore-induced volatiles induce the emission of ethylene in neighboring lima bean plants. Plant J. 29, 87-98
- Arimura, G. et al. (2000) Herbivory-induced volatiles elicit defence genes in lima bean leaves. Nature 406, 512-515
- Maffei, M.E. et al. (2006) Effects of feeding Spodoptera littoralis on lima bean leaves. III. Membrane depolarization and involvement of hydrogen peroxide. Plant Physiol. 140, 1022-1035
- Sathyanarayanan, P.V. and Poovaiah, B.W. (2004) Decoding Ca 2+ signals in plants. Crit. Rev. Plant Sci. 23, 1-11
- Foyer, C.H. and Noctor, G. (2005) Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ. 28, 1056-1071
- Foyer, C.H. and Noctor, G. (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17, 1866-1875
- Foyer, C.H. and Noctor, G. (2003) Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol. Plant. 119, 355-364
- Asada, K. (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol. 141, 391-396
- van Breusegem, F. and Dat, J.F. (2006) Reactive oxygen species in plant cell death. Plant Physiol. 141, 384-390
- Zaninotto, F. et al. (2006) Cross talk between reactive nitrogen and oxygen species during the hypersensitive disease resistance response. Plant Physiol. 141, 379-383
- Rhoads, D.M. et al. (2006) Mitochondrial reactive oxygen species. Contribution to oxidative stress and interorganellar signaling. Plant Physiol. 141, 357-366
- Watanabe, T. et al. (2001) Wound-induced expression of a gene for 1- aminocyclopropane-1-carboxylate synthase and ethylene production are regulated by both reactive oxygen species and jasmonic acid in Cucurbita maxima. Plant Physiol. Biochem. 39, 121-127
- Leitner, M. et al. (2005) Direct and indirect defences induced by piercing-sucking and chewing herbivores in Medicago truncatula. New Phytol. 167, 597-606
- Mitho ¨fer, A. et al. (2004) Biotic and heavy metal stress response in plants: evidence for common signals. FEBS Lett. 566, 1-5
- Orozco-Cardenas, M.L. et al. (2001) Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. Plant Cell 13, 179-191
- Overmyer, K. et al. (2003) Reactive oxygen species and hormonal control of cell death. Trends Plant Sci. 8, 335-342
- Musser, R.O. et al. (2006) Ablation of caterpillar labial salivary glands: technique for determining the role of saliva in insect-plant interactions. J. Chem. Ecol. 32, 981-992
- Neill, S.J. et al. (2002) Hydrogen peroxide and nitric oxide as signalling molecules in plants. J. Exp. Bot. 53, 1237-1247
- Delledonne, M. (2005) NO news is good news for plants. Curr. Opin. Plant Biol. 8, 390-396
- Orozco-Cardenas, M. and Ryan, C.A. (2002) Nitric oxide negatively modulates wound signaling in tomato plants. Plant Physiol. 130, 487- 493
- Seo, S. et al. (1995) Tobacco map kinase -a possible mediator in wound signal-transduction pathways. Science 270, 1988-1992
- Seo, S. et al. (1999) Jasmonate-based wound signal transduction requires activation of WIPK, a tobacco mitogen-activated protein kinase. Plant Cell 11, 289-298
- Kodama, H. et al. (2000) Possible involvement of protein phosphorylation in the wound-responsive expression of Arabidopsis plastid omega-3 fatty acid desaturase gene. Plant Sci. 155, 153-160
- Liu, Y.D. et al. (2003) Interaction between two mitogen-activated protein kinases during tobacco defense signaling. Plant J. 34, 149-160
- Yamakawa, H. et al. (2004) Plant MAPK phosphatase interacts with calmodulins. J. Biol. Chem. 279, 928-936
- Gomi, K. et al. (2005) A mitogen-activated protein kinase NtMPK4 activated by SIPKK is required for jasmonic acid signaling and involved in ozone tolerance via stomatal movement in tobacco. Plant Cell Physiol. 46, 1902-1914
- Waller, F. et al. (2006) Expression of a WIPK-activated transcription factor results in increase of endogenous salicylic acid and pathogen resistance in tobacco plants. Plant Cell Physiol. 47, 1169-1174
- Ludwig, A.A. et al. (2004) CDPK-mediated signalling pathways: specificity and cross-talk. J. Exp. Bot. 55, 181-188
- Cheng, S.H. et al. (2002) Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol. 129, 469-485
- Ulloa, R.M. et al. (2002) Jasmonic acid affects plant morphology and calcium-dependent protein kinase expression and activity in Solanum tuberosum. Physiol. Plantarum 115, 417-427
- Ludwig, A.A. et al. (2005) Ethylene-mediated cross-talk between calcium-dependent protein kinase and MAPK signaling controls stress responses in plants. Proc. Natl. Acad. Sci. U. S. A. 102, 10736-10741
- Schmidt, S. and Baldwin, I.T. (2006) Systemin in Solanum nigrum. The tomato-homologs polypeptide does not mediate direct defense responses. Plant Physiol. 142, 1751-1758
- Schmelz, E.A. et al. (2003) Simultaneous analysis of phytohormones, phytotoxins, and volatile organic compounds in plants. Proc. Natl. Acad. Sci. U. S. A. 100, 10552-10557
- Schulze, B. et al. (2006) Profiling of structurally labile oxylipins in plants by in situ derivatization with pentafluorobenzyl hydroxylamine. Anal. Biochem. 348, 269-283
- Baldwin, I.T. et al. (1997) Quantification, correlations and manipulations of wound-induced changes in jasmonic acid and nicotine in Nicotiana sylvestris. Planta 201, 397-404
- Schulze, B. et al. (2007) Rapid enzymatic isomerization of 12- oxophytodienoic acid in the gut of feeding Lepidopteran larvae. ChemBioChem 8, 208-216
- Kessler, A. et al. (2004) Silencing the jasmonate cascade: induced plant defenses and insect populations. Science 305, 665-668
- Stotz, H.U. et al. (2002) Evidence for regulation of resistance in Arabidopsis to Egyptian cotton worm by salicylic and jasmonic acid signaling pathways. Planta 214, 648-652
- Traw, M.B. et al. (2003) Negative cross-talk between salicylate-and jasmonate-mediated pathways in the Wassilewskija ecotype of Arabidopsis thaliana. Mol. Ecol. 12, 1125-1135
- Ruther, J. and Kleier, S. (2005) Plant-plant signaling: ethylene synergizes volatile emission in Zea mays induced by exposure to (Z)- 3-hexen-1-ol. J. Chem. Ecol. 31, 2217-2222
- Harfouche, A.L. et al. (2006) Ethylene signaling mediates a maize defense response to insect herbivory. Mol. Plant Microbe Interact. 19, 189-199
- Lorenzo, O. et al. (2003) Ethylene response factor1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 15, 165-178
- Baldwin, I.T. et al. (2006) Volatile signaling in plant-plant interactions: 'Talking trees' in the genomics era. Science 311, 812- 815
- Lorenzo, O. et al. (2004) JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell 16, 1938-1950
- Garcia-Brugger, A. et al. (2006) Early signaling events induced by elicitors of plant Defenses. Mol. Plant Microbe Interact. 19, 711- 724
- Felton, G.W. and Korth, K.L. (2000) Trade-offs between pathogen and herbivore resistance. Curr. Opin. Plant Biol. 3, 309-314
- Grant, M. and Mansfield, J. (1999) Early events in host-pathogen interactions. Curr. Opin. Plant Biol. 2, 312-319
- Torres, M.A. et al. (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiol. 141, 373-378
- Dixon, R.A. (2001) Natural products and plant disease resistance. Nature 411, 843-847
- Arimura, G. et al. (2005) Herbivore-induced, indirect plant defences. BBA-Mol. Cell Biol. L. 1734, 91-111
- Cardoza, Y.J. and Tumlinson, J.H. (2006) Compatible and incompatible Xanthomonas infections differentially affect herbivore- induced volatile emission by pepper plants. J. Chem. Ecol. 32, 1755- 1768