Intercellular communication in plants: electrical stimulation of proteinase inhibitor gene expression in tomato

Abstract

Tomato (Lycopersicon esculentum L.) plants accumulate proteinase inhibitor ( pin) mRNA in response to various stimuli in leaves distant from those treated. Most earlier work suggests that the intercellular wound signals are chemical; we have tried to determine whether electrical or hydraulic signals can also evoke systemic pin expression. We used a mild¯ame to evoke a hydraulic signal and its local electrical aftermath, the variation potential (VP), and an electric stimulus to trigger an action potential. Under medium light, wounding evoked a 3-to 5-fold systemic increase in pin mRNA within 15 min, suggesting involvement of a rapidly transmitted signal. Wounding also triggered a transient systemic increase in calmodulin (cal ) mRNA, under medium light conditions. Wounded plants exhibited electrical responses (VP) and yielded 5-to 15-fold increases in pin mRNA within 1 h. Electrically stimulated plants that transmitted an action potential to the analyzed leaf exhibited similarly large, rapid increases in pin transcript. Plants which generated no signal had unchanged levels of pin mRNA. Thus, in addition to the previously shown chemical signals, both hydraulically induced VPs and electrically induced action potentials can elicit systemic pin expression.

Variation potential in higher plants: Mechanisms of generation and propagation

“…First, it was shown in several studies that local damage induced changes in stem or leaf thickness that reflected hydraulic wave propagation through the plant. 4,47,53,60,61 Changes in thickness started before the electrical reaction was initiated 4,40,47,51 thus supporting their key role in VP induction. Additionally, artificially increasing xylem hydraulic pressure in the positive direction 7,49,53 induces electrical reactions that are similar to VP.…”

Herbivory Rapidly Activates MAPK Signaling in Attacked and Unattacked Leaf Regions but Not between Leaves ofNicotiana attenuata

“…Several studies have found that systemic leaves orthostichous to the wounded leaf accumulate markedly higher levels of PI transcripts and activity than do nonorthostichous leaves, suggesting that the signal is transported by the vascular system (Jones et al, 1993;Orians et al, 2000;Schittko and Baldwin, 2003;Orians, 2005). The involvement of electric and hydraulic signals in mediating the systemic responses has also been proposed Stankovic and Davies, 1997). More importantly, an elegant genetic study strongly argues that JA plays important roles in mediating systemic PI response: either JA or a JA-elicited mobile signal is responsible for systemic PI induction (Li et al, 2002).…”

Recognition of Herbivory-Associated Molecular Patterns

“…Electrical waves that propagate from the point of injury through the tissue are more likely early and fast signals (Maffei et al, 2007b). Such signals are indeed able to trigger defenses, for example, the up-regulation of proteinase inhibitor genes (Wildon et al, 1992;Stankovic and Davies, 1997;Herde et al, 1998), a response obviously following wounding (Graham et al, 1986). Recently, action potentials in plants have been correlated with defense responses upon herbivore attack (Maffei et al, 2004) and they also have been demonstrated to be released by various compounds (e.g.…”