Academia.eduAcademia.edu

Outline

Before gene expression: early events in plant–insect interaction

2007, Trends in Plant Science

https://doi.org/10.1016/J.TPLANTS.2007.06.001

Abstract

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)

  1. Reymond, P. et al. (2004) A conserved transcript pattern in response to a specialist and a generalist herbivore. Plant Cell 16, 3132- 3147
  2. 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
  3. 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
  4. Ebel, J. and Mitho ¨fer, A. (1998) Early events in the elicitation of plant defence. Planta 206, 335-348
  5. 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
  6. 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
  7. Wildon, D.C. et al. (1992) Electrical signalling and systemic proteinase inhibitor induction in the wounded plant. Nature 360, 62-65
  8. 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
  9. 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
  10. 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
  11. 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
  12. Shibuya, N. and Minami, E. (2001) Oligosaccharide signalling for defence responses in plant. Physiol. Mol. Plant Pathol. 59, 223-233
  13. Maischak, H. et al. (2007) Oral secretions from herbivorous lepidopteran larvae exhibit ion channel-forming activities. FEBS Lett. 581, 898-904
  14. 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
  15. Alborn, H. et al. (1997) An elicitor of plant volatiles from beet armyworm oral secretion. Science 276, 945-949
  16. 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
  17. White, P.J. (2000) Calcium channels in higher plants. BBA- Biomembranes 1465, 171-189
  18. Lecourieux, D. et al. (2006) Calcium in plant defence-signalling pathways. New Phytol. 171, 249-269
  19. Evans, N.H. et al. (2001) Calcium oscillations in higher plants. Curr. Opin. Plant Biol. 4, 415-420
  20. Sanders, D. et al. (2002) Calcium at the crossroads of signaling. Plant Cell 14, S401-S417
  21. Reddy, V.S. and Reddy, A.S.N. (2004) Proteomics of calcium-signaling components in plants. Phytochemistry 65, 1745-1776
  22. Jonak, C. et al. (2002) Complexity, cross talk and integration of plant MAP kinase signalling. Curr. Opin. Plant Biol. 5, 415-424
  23. Arimura, G. et al. (2002) Herbivore-induced volatiles induce the emission of ethylene in neighboring lima bean plants. Plant J. 29, 87-98
  24. Arimura, G. et al. (2000) Herbivory-induced volatiles elicit defence genes in lima bean leaves. Nature 406, 512-515
  25. 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
  26. Sathyanarayanan, P.V. and Poovaiah, B.W. (2004) Decoding Ca 2+ signals in plants. Crit. Rev. Plant Sci. 23, 1-11
  27. 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
  28. 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
  29. 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
  30. Asada, K. (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol. 141, 391-396
  31. van Breusegem, F. and Dat, J.F. (2006) Reactive oxygen species in plant cell death. Plant Physiol. 141, 384-390
  32. Zaninotto, F. et al. (2006) Cross talk between reactive nitrogen and oxygen species during the hypersensitive disease resistance response. Plant Physiol. 141, 379-383
  33. Rhoads, D.M. et al. (2006) Mitochondrial reactive oxygen species. Contribution to oxidative stress and interorganellar signaling. Plant Physiol. 141, 357-366
  34. 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
  35. Leitner, M. et al. (2005) Direct and indirect defences induced by piercing-sucking and chewing herbivores in Medicago truncatula. New Phytol. 167, 597-606
  36. Mitho ¨fer, A. et al. (2004) Biotic and heavy metal stress response in plants: evidence for common signals. FEBS Lett. 566, 1-5
  37. 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
  38. Overmyer, K. et al. (2003) Reactive oxygen species and hormonal control of cell death. Trends Plant Sci. 8, 335-342
  39. 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
  40. Neill, S.J. et al. (2002) Hydrogen peroxide and nitric oxide as signalling molecules in plants. J. Exp. Bot. 53, 1237-1247
  41. Delledonne, M. (2005) NO news is good news for plants. Curr. Opin. Plant Biol. 8, 390-396
  42. Orozco-Cardenas, M. and Ryan, C.A. (2002) Nitric oxide negatively modulates wound signaling in tomato plants. Plant Physiol. 130, 487- 493
  43. Seo, S. et al. (1995) Tobacco map kinase -a possible mediator in wound signal-transduction pathways. Science 270, 1988-1992
  44. 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
  45. 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
  46. Liu, Y.D. et al. (2003) Interaction between two mitogen-activated protein kinases during tobacco defense signaling. Plant J. 34, 149-160
  47. Yamakawa, H. et al. (2004) Plant MAPK phosphatase interacts with calmodulins. J. Biol. Chem. 279, 928-936
  48. 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
  49. 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
  50. Ludwig, A.A. et al. (2004) CDPK-mediated signalling pathways: specificity and cross-talk. J. Exp. Bot. 55, 181-188
  51. Cheng, S.H. et al. (2002) Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol. 129, 469-485
  52. 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
  53. 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
  54. 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
  55. 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
  56. Schulze, B. et al. (2006) Profiling of structurally labile oxylipins in plants by in situ derivatization with pentafluorobenzyl hydroxylamine. Anal. Biochem. 348, 269-283
  57. 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
  58. Schulze, B. et al. (2007) Rapid enzymatic isomerization of 12- oxophytodienoic acid in the gut of feeding Lepidopteran larvae. ChemBioChem 8, 208-216
  59. Kessler, A. et al. (2004) Silencing the jasmonate cascade: induced plant defenses and insect populations. Science 305, 665-668
  60. 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
  61. 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
  62. 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
  63. Harfouche, A.L. et al. (2006) Ethylene signaling mediates a maize defense response to insect herbivory. Mol. Plant Microbe Interact. 19, 189-199
  64. Lorenzo, O. et al. (2003) Ethylene response factor1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 15, 165-178
  65. Baldwin, I.T. et al. (2006) Volatile signaling in plant-plant interactions: 'Talking trees' in the genomics era. Science 311, 812- 815
  66. 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
  67. Garcia-Brugger, A. et al. (2006) Early signaling events induced by elicitors of plant Defenses. Mol. Plant Microbe Interact. 19, 711- 724
  68. Felton, G.W. and Korth, K.L. (2000) Trade-offs between pathogen and herbivore resistance. Curr. Opin. Plant Biol. 3, 309-314
  69. Grant, M. and Mansfield, J. (1999) Early events in host-pathogen interactions. Curr. Opin. Plant Biol. 2, 312-319
  70. Torres, M.A. et al. (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiol. 141, 373-378
  71. Dixon, R.A. (2001) Natural products and plant disease resistance. Nature 411, 843-847
  72. Arimura, G. et al. (2005) Herbivore-induced, indirect plant defences. BBA-Mol. Cell Biol. L. 1734, 91-111
  73. 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