SPIK: a K + channel for Arabidopsis pollen

Abstract

Channel proteins form aqueous pores that allow ions to cross membranes down their electrochemical gradients. ‘Highly-selective’ K+ channels are characterized by the amino acid sequence Gly-Tyr-Gly-Asp (GYGD) in their pore structure. There are 15 genes encoding such K+ channels in Arabidopsis thaliana, which includes those for channels facilitating K+ influx (KIR) and K+ efflux (KOR) across the plasma membrane belonging to the ‘Shaker’ channel family. Plasma membrane K+ channels serve both to generate the osmotic changes required for turgor regulation, nastic movements or growth, and to balance the charge of other ions moving across the plasma membrane during, for example, nutrient uptake or cell signalling. The seven KIR channels in Arabidopsis can be divided into proteins that possess an ankyrin domain at their C-terminal (AKT1, AKT2/3, AKT5 and AKT6), which allows interactions with the cytoskeleton, and those that do not (KAT1, KAT2 and KAT3). The physiological roles of these channels are being elucidated through studies of their expression patterns, electrophysiological characteristics (following expression in heterologous systems and corroboration in appropriate plant cell types), and through the use of mutants lacking, or expressing mutant, channel proteins. From many such studies it has been suggested that (1) AKT1 is the dominant KIR channel expressed in roots and is responsible for K+ uptake from ammoniacal solutions, (2) AKT2/3 is expressed in the leaf vasculature, where it can provide a counter K+ current that facilitates sucrose loading into the phloem, and (3) KAT1 and KAT2 are co-expressed in guard cells where they form an oligomeric channel responsible for K+ uptake during stomatal opening. Now, in a most comprehensive study, Karine Mouline and colleagues have elucidated the function of AKT6 [1xPollen tube development and competitive ability are impaired by disruption of a Shaker K+ channel in Arabidopsis. Mouline, K et al. Genes Dev. 2002; 16: 339–350Crossref | PubMed | Scopus (138)See all References][1].Because AKT6 is expressed solely in pollen tubes, Mouline et al. have called its gene product SPIK, for Shaker pollen inward K+ channel. When expressed in mammalian COS cells, SPIK behaves as a typical KIR channel. It opens at extremely negative voltages and is blocked by extracellular Cs+ at mm concentrations. It is insensitive to extracellular Ca2+ in the range 1–10 mm, but is activated at more positive voltages when the extracellular medium is acidified. Mouline et al. confirmed that this electrophysiological behaviour corresponded to the KIR channels recorded in native pollen grains and argue that, because the membrane potential of pollen tubes is sufficiently negative for SPIK to open, this channel could drive pollen tube elongation by catalysing K+ uptake. Consistent with their argument, was the demonstration that pollen tubes of mutants lacking AKT6 (spick-1) had reduced KIR currents and restricted growth, resulting in a decline in pollen competitive ability and reproductive success.It is noteworthy that the expression of AKT6 is restricted to a particular cell type. Indeed, it is startling that each KIR-channel gene in Arabidopsis encodes a protein with unique biophysical properties that is expressed in specific cell types or at certain stages of development. The reason for this functional differentiation of KIR channels has yet to be resolved. Perhaps the answer lies in a necessity for precisely controlled cation fluxes, or the strict coordination of KIR channel expression in cells experiencing contrasting extracellular ionic conditions or conflicting environmental or developmental cues. The answer might also lie in the exact role of the KIR channel in cellular or plant physiology. Whatever the reason, it is nevertheless clear that many cell types possess a unique complement of KIR channels and that the K+ transport capabilities of different cell types can never be assumed.