Abstract
The pathway of a systemic electrical signal possibly linking wounding and the systemic synthesis of proteinase inhibitor was investigated in tomato (Lycopersicon esculentumMill. cv. Moneymaker) plants. Heat, causing wounding to a cotyledon, was used to induce both a travelling electrical signal and systemic proteinase inhibitor activity. Intracellular recordings of changes in the membrane potential of different cell types were measured in the petiole of leaf 1, the first true leaf, and impaled cells were identified by injection of fluorescent dye (Lucifer Yellow CH). No difference was found between the membrane potentials of the different cell types; the mean membrane potential of all the cell types was -148 ± 3 mV. Only sieve-tube elements and companion cells produced large (79 ± 3.3 mV) action-potential-like depolarisations following wounding, although smaller (23 ± 1.6 mV) depolarisations were observed in other cell types. It was concluded that the electrical signal possibly linking a wound stimulus in a cotyledon with the induction of systemic proteinase inhibitor synthesis was propagated in the sieve-tube element/companion cell complex.
Similar content being viewed by others
Abbreviations
- LYCH:
-
Lucifer Yellow CH
- PI:
-
proteinase inhibitor
References
Bewies DJ (1990) Defence-related proteins in higher plants. Annu Rev Biochem 59: 873–907
Farmer EE, Ryan CA (1990) Interplant communication: Air-borne methyl jasmonate induces synthesis of proteinase inhibitor in plant leaves. Proc Natl Acad Sci USA 87: 713–716
Farmer EE, Ryan CA (1992) Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase-inhibitors. Plant Cell 4: 129–134
Findlay GP, Hope AB (1976) Electrical properties of plant cells: methods and findings. In: Lüttge U, Pitman MG (eds) Encyclopaedia of plant physiology (NS), vol II: Transport in plants: Part A. Cells. Springer-Verlag, Berlin, pp 53–92
Fromm J, Bauer T (1994) Action potentials in maize sieve tubes change phloem translocation. J Exp Bot 45: 463–469
Fromm J, Eschrich W (1988) Transport processes in stimulated and non-stimulated leaves of Mimosa pudica. Trees 2: 18–24
Fromm J, Eschrich W (1993) Electric signals released from roots of willow (Salix viminalis L.) change transpiration and photosynthesis. J Plant Physiol 141: 673–680
Fromm J, Spanswick R (1993) Characteristics of action potentials in willow (Salix viminalis L). J Exp Bot 44: 1119–1125
Herde O, Fuss H, Peña-Cortès H, Fisahn J (1995) Proteinase inhibitor II gene expression induced by electrical stimulation and control of photosynthetic activity in tomato plants. Plant Cell Physiol 36: 737–742
Julien JL, Frachisse JM (1992) Involvement of the proton pump and proton conductance change in the wave of depolarization induced by wounding in Bidens pilosa. Can J Bot 70: 1451–1458
Malone M, Alarcon J-J (1995) Only xylem-borne factors can account for systemic wound signalling in the tomato plant. Planta 196: 740–746
Malone M, Palumbo L, Boari F, Monteleone M, Jones HG (1994a) The relationship between wound-induced proteinase inhibitors and hydraulic signals in tomato seedlings. Plant Cell Environ 17: 81–87
Malone M, Alarcon J-J, Palumbo L (1994b) An hydraulic interpretation of rapid, long-distance wound signalling in the tomato. Planta 193: 181–185
Mobbs P, Becker D, Williamson R, Bate M, Warner A (1994) Techniques for dye injection and cell labelling. In: Ogden D (ed) The Plymouth workshop handbook. The Company of Biologists Ltd. Cambridge, UK, pp 361–388
Pearce G, Strydom D, Johnson S, Ryan CA (1991) A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science 253: 895–898
Jon H, Willmitzer L, Sanchez-Serrano JJ (1991) Abscisic acid mediates wound induction but not developmental-specific expression of the proteinase inhibitor II gene family. Plant Cell 3: 963–972
Pickard BG (1973) Action potentials in higher plants. Bot Rev 39: 172–201
Ryan CA (1990) Protease inhibitors in plants: Genes for improving defences against insects and pathogens. Annu Rev Phytopathol 28: 425–449
Ryan CA, Farmer EE (1991) Oligosaccharide signals in plants: A current assessment. Annu Rev Plant Physiol Plant Mol Biol 42: 651–674
Samejima M, Sibaoka T (1983) Identification of the excitable cells in the petiole of Mimosa pudica by intracellular injection of procion yellow. Plant Cell Physiol 24: 33–39
Shimmen T, Mimura T, Munehiro K, Tazawa M (1994) Characean cells as a tool for studying electrophysiological characteristics of plant cells. Cell Struct Funct 19: 263–278
Stankovic B, Davies E (1995) Direct electrical induction of gene expression in tomato plants. J Cellular Biochem suppl 21A: 503
Thain JF, Wildon DC (1993) Electrical signalling in plants. In: Schultz JC, Raskin I (eds) Plant signals in interactions with other organisms. American Society of Plant Physiologists, Maryland, pp 102–115
van Bel AJE, Kempers R (1990) Symplastic isolation of the sieve element-companion cell complex in the phloem of Ricinus communis and Salix alba stems. Planta 183: 69–76
van Bel AJE, van Rijen HVM (1994) Microelectrode-recorded development of the symplasmic autonomy of the sieve element/ companion cell complex in the stem phloem of Lupinus luteus L). Planta 192: 165–175
van der Schoot C, van Bel AJE (1989) Glass microelectrode measurements of sieve tube membrane potentials in internode discs and petiole strips of tomato (Solanum lycopersicum L). Protoplasma 149: 144–154
van der Schoot C, van Bel AJE (1990) Mapping membrane potenlial differences and dye-coupling in inlernodal tissues of tomato (Solanum lycopersicum L. Planta 182: 9–21
Wayne R (1994) The excitabilily of planl cells: with special emphasis on Characean internodal cells. Bol Rev 60: 265–367
Wildon DC, Doherly HM, Eagles G, Bowles DJ, Thain JF (1989) Systemic responses arising from localized heal stimuli in tomato plants. Ann Bot 64: 691–695
Wildon DC, Thain JF, Minchin PEH, Gubb IR, Reilly AJ, Skipper D, Doherty HM, O'Donnell PJ, Bowles DJ (1992) Electrical signalling and systemic proteinase inhibitor induction in the wounded plant. Nature 360: 62–65
Zawadzki T, Davies E, Dziubinska H, Trebacz K (1991) Characteristics of action potentials in Helianthus annuus. Physiol Planl 83: 601–604
Author information
Authors and Affiliations
Corresponding author
Additional information
This work was supported by the Biotechnology and Biological Sciences Research Council (UK).
Rights and permissions
About this article
Cite this article
Rhodes, J.D., Thain, J.F. & Wildon, D.C. The pathway for systemic electrical signal conduction in the wounded tomato plant. Planta 200, 50–57 (1996). https://doi.org/10.1007/BF00196648
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00196648