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A developmental gradient in the mechanism of K+ uptake during light-stimulated leaf growth in Nicotiana tabacum L.

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Abstract

Light causes growth of dicotyledonous leaves by stimulating proton efflux, cell wall acidification and loosening, and solute accumulation for turgor maintenance. For cells still undergoing cell division at the base of expanding tobacco (Nicotiana tabacum L. cv. Xanthi) leaves, light-stimulated growth depends on K+ uptake, and is inhibited by the potassium channel blocker tetraethylammonium (TEA). The generality of this mechanism has been tested by comparing the effect of light on the growth-associated physiology of dividing and expanding cells in the base with cells at the tip growing by cell expansion only. The magnitude of the light-induced growth response of excised leaf discs is greatest at the leaf base and declines as cells mature. Basal tissue is more sensitive to exogenous potassium, which enhances light-stimulated growth at <1 mM, whereas tip tissue requires higher levels (>10 mM). Growth is inhibited by TEA similarly in tip and base. However, light-stimulated K+ uptake and proton efflux respond differently to TEA in tip and basal tissue. In basal tissue, TEA reduces light-stimulated K+ uptake by 60% and inhibits light-stimulated proton efflux. These results agree with those presented by M. Claussen et al. (1997, Planta 201:227–234) showing that auxin-stimulated H+ pump activity and growth in coleoptiles require K+ uptake as an electrical counterbalance to H+ efflux. In contrast, in tip tissue, TEA inhibits light-stimulated K+ uptake by only 17% and does not inhibit proton efflux. Our results suggest that the basipetal gradient in the effect of TEA on light-regulated growth physiology can be explained by TEA effects on K+ uptake: TEA inhibits light-stimulated H+ pump activity, wall acidification and membrane hyperpolarization only in cells dependent on TEA-sensitive channels for light-stimulated K+ uptake. Further, our data suggest that younger, basal tissue is dependent on TEA-sensitive, sucrose-stimulatable channels for light-stimulated K+ uptake whereas older, tip tissue is able to use an additional, TEA-insensitive K+ transporter to mediate light-stimulated K+ uptake.

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Abbreviations

ABP-1:

auxin-binding protein

DCMU:

3-(3,4-dichlorophenyl)-1,1-dimethylurea

Em :

membrane potential

TEA:

tetraethylammonium

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Authors and Affiliations

  1. Botany Department, University of Washington, Box 35-5325, Seattle, WA 98195-5325, USA

    Kari A. Stiles, Anna McClintick & Elizabeth Van Volkenburgh

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  1. Kari A. Stiles
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  2. Anna McClintick
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  3. Elizabeth Van Volkenburgh
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Correspondence to Elizabeth Van Volkenburgh.

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Stiles, K.A., McClintick, A. & Van Volkenburgh, E. A developmental gradient in the mechanism of K+ uptake during light-stimulated leaf growth in Nicotiana tabacum L.. Planta 217, 587–596 (2003). https://doi.org/10.1007/s00425-003-1023-6

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  • DOI: https://doi.org/10.1007/s00425-003-1023-6

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