Poplar potassium transporters capable of controlling K⁺ homeostasis and K⁺‐dependent xylogenesis

Abstract

The cambial K+ content of poplar increases during the growth period in a K+ supply dependent manner. Upon K+ starvation or application of tetraethylammoniumchloride (TEA+), a K+ channel blocker, the average vessel lumen and expansion zone area were significantly reduced. In search for the molecular basis of potassium-dependent xylogenesis in poplar, K+ transporters homologous to those of known function in Arabidopis phloem- and xylem-physiology were isolated from a poplar wood EST library. The expression profile of three distinct K+ channel types and one K+ transporter, Populus tremula K+ uptake transporter 1 (PtKUP1), was analysed by quantitative RT-PCR. Thereby, we found P. tremula outward rectifying K+ channel (PTORK) and P. tremula K+ channel 2 (PTK2) correlated with the seasonal wood production. K+ transporter P. tremula 1 (KPT1) was predominantly found in guard cells. Following the heterologous expression in Xenopus oocytes the biophysical properties of the different channels were determined. PTORK, upon membrane de-polarization mediates potassium release. PTK2 is almost voltage independent, carrying inward K+ flux at hyperpolarized potential and K+ release upon de-polarization. PtKUP1 was expressed in a K+ uptake-deficient Escherichia coli strain, where this K+ transporter rescued K+-dependent growth. In order to link the different K+ transporters to the cambial activity and wood production, we compared the expression profiles to seasonal changes in the K+ content of the bark as well as xylem vessel diameter. Thereby, we found PTORK and PTK2 transcripts to follow the annual K+ variations in poplar branches. PtKUP1 was expressed at a low level throughout the year, suggesting a housekeeping function. From these data, we conclude that K+ channels are involved in the regulation of K+-dependent wood production.