Plant Physiol, February 2003, Vol. 131, pp. 583-594

Differences in Whole-Cell and Single-Channel Ion Currents across the Plasma Membrane of Mesophyll Cells from Two Closely Related Thlaspi Species

United States Plant, Soil, and Nutrition Laboratory, United States Department of Agriculture-Agricultural Research Service, Cornell University, Ithaca, New York 14853

The patch clamp technique was used to study the physiology of ion transport in mesophyll cells from two Thlaspi spp. that differ significantly in their physiology. In comparison with Thlaspi arvense, Thlaspi caerulescens (a heavy metal accumulator) can grow in, tolerate, and accumulate very high levels of certain heavy metals (primarily zinc [Zn] and cadmium) in their leaf cells. The membrane conductance of every T. arvense leaf cell was dominated by a slowly activating, time-dependent outward rectifying current (SKOR). In contrast, only 23% of T. caerulescens cells showed SKOR activity, whereas the remaining 77% exhibit a rapidly developing instantaneous K⁺ outward rectifier (RKOR) current. In contrast to RKOR, the channels underlying the SKOR current were sensitive to changes in the extracellular ion activity. Single-channel recordings indicated the existence of K⁺ channel populations with similar unitary conductances, but distinct channel kinetics and regulation. The correlation between these recordings and the whole-cell data indicated that although one type of channel kinetics is preferentially activated in each Thlaspi spp., both species have the capability to switch between either type of current. Ion substitution in whole-cell and single-channel experiments indicated that although the SKOR and RKOR channels mediate a net outward K⁺ current, they can also allow a significant Zn²⁺ permeation (i.e. influx). In addition, single-channel recordings allowed us to identify an infrequent type of plasma membrane divalent cation channel that also can mediate Zn²⁺ influx. We propose that the different K⁺ channel types or channel states may result from and are likely to reflect differences in the cytoplasmic and apoplastic ionic environment in each species. Thus, the ability to interchangeably switch between different channel states allows each species to constantly adjust to changes in their apoplastic ionic environment.