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Dissection of heat-induced systemic signals: superiority of ion fluxes to voltage changes in substomatal cavities

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Abstract

Using non-invasive ion-selective microprobes, that were placed in substomatal cavities, long-distance signalling has been investigated in intact Hordeum vulgare and Vicia faba seedlings. Heat (flame), applied to one leaf (S-leaf), triggers apoplastic ion activity (pH, pCa, pCl) transients in a distant leaf (T-leaf), all largely independent of simultaneously occurring action potential-like voltage changes. While apoplastic pCa and pH increase (Ca2+-, H+-activities decrease), pCl decreases (Cl−-activity increases). As the signal transfer from the S- to the T-leaf is too fast to account for mass flow, the heat-induced pressure change is primarily responsible for changes in voltage (H+ pump deactivation) as well as for the ion fluxes. The pCa transient precedes the pCl- and pH responses, but not the voltage change. Since the apoplastic pCl decrease (Cl− increase) occurs after the pCa increase (Ca2+ decrease) and after the depolarization, we argue that the Cl− efflux is a consequence of the Ca2+ response, but has no part in the depolarization. Kinetic analysis reveals that pH- and pCl changes are interrelated, indicated by the action of the anion channel antagonist NPPB, which inhibits both pCl- and pH changes. It is suggested that efflux of organic anions into the apoplast causes the pH increase rather than the deactivation of the plasma membrane H+ pump. Since there is considerably more information in ion activity changes than in a single action- or variation potential and heat-induced ion fluxes occur more reliably than voltage changes, released by milder stimuli, they are considered systemic signalling components superior to voltage.

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Abbreviations

AP:

Action potential

NPPB:

5-Nitro-2-(3-phenylpropylamino)benzoic acid

S-leaf:

Stimulated leaf

T-leaf:

Target leaf

VP:

Variation potential

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Acknowledgments

The financial support of this work by the “Deutsche Forschungsgemeinschaft” (Fe 213/15-1,2) is gratefully acknowledged.

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  1. Botanisches Institut I, Justus-Liebig-Universität, Senckenbergstraße 17, 35390, Gießen, Germany

    Mathias R. Zimmermann & Hubert H. Felle

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  1. Mathias R. Zimmermann
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  2. Hubert H. Felle
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Correspondence to Hubert H. Felle.

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Zimmermann, M.R., Felle, H.H. Dissection of heat-induced systemic signals: superiority of ion fluxes to voltage changes in substomatal cavities. Planta 229, 539–547 (2009). https://doi.org/10.1007/s00425-008-0850-x

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