A rice high-affinity potassium transporter (HKT) conceals a calcium-permeable cation channel

Abstract

Plant high-affinity K + transport (HKT) proteins are so named because of their relation to bacterial and fungal transporters that mediate high-affinity K + uptake. The view that HKT family members are sodium-selective uniporters or sodium-potassium symporters is widely held. We have found that one of the rice HKT proteins also functions as a Ca 2+ -permeable cation channel that conducts current carried by a wide range of monovalent and divalent cations. The HKT rice gene, named OsHKT2;4, is expressed in several cell types, including root hairs and vascular parenchyma cells. The protein is localized to the plasma membrane, thereby providing a mechanism for cation uptake and extrusion. This finding goes against firmly entrenched dogma in showing that HKT proteins can function as both ion carriers and channels. The study further extends the function of HKT proteins to Ca 2+ -linked processes and, in so doing, defines a previously undescribed type of Ca 2+ -permeable cation channels in plants. The work also raises questions about the evolutionary changes in this protein family following the divergence of monocots and dicots.calcium transport | moncot-dicot divergence | nonselective cation channel

The Rice Monovalent Cation Transporter OsHKT2;4: Revisited Ionic Selectivity

“…OsHKT2;4 has been proposed to constitute a Ca 2+ -permeable cation/K + channel or transporter when expressed in Xenopus oocytes (Lan et al, 2010;Horie et al, 2011). Currents attributed to OsHKT2;4 in the report by Lan et al (2010) displayed a large slowly activating inwardly rectifying component and were thus very different from the instantaneously activating ohmic ones obtained in our study (compare with traces above).…”

“…Currents attributed to OsHKT2;4 in the report by Lan et al (2010) displayed a large slowly activating inwardly rectifying component and were thus very different from the instantaneously activating ohmic ones obtained in our study (compare with traces above). We therefore reexamined OsHKT2;4 permeability to Ca 2+ (Fig.…”

“…In each set of solutions, the concentration of the monovalent cations (either K + or Na + or both Na + and K + ) was fixed and that of Ca 2+ was variable (0.3, 1.8, or 10 mM). It should be noted that two sets of solutions, those containing either 1 mM K + or 3 mM Na + , displayed the same (or almost the same) cation composition as sets of solutions used by Lan et al (2010) to address OsHKT2;4 permeability to Ca 2+ . Increasing external Ca 2+ from 0.3 to 10 mM in the presence of 1 mM K + and/or 3 mM Na + was shown to have no significant effect on OsHKT2;4 current amplitude ( .…”

“…Rise to an Instantaneously Activating Non-Voltage-Regulated Conductance OsHKT2;4 expression in Xenopus oocytes being expected not to lead to large exogenous currents (Lan et al, 2010), we paid special attention to the quality of oocytes used. Figure 1A provides examples of currents recorded in a control (water-injected) oocyte from a batch selected for OsHKT2;4 expression.…”

“…Surprisingly, a subfamily 2 rice HKT transporter that remained to be characterized, OsHKT2;4, was recently reported to form a calcium-permeable weakly selective cation channel (Lan et al, 2010) or a Ca 2+ -permeable K + transporter (Horie et al, 2011) when heterologously expressed in Xenopus oocytes. These results were exciting for the plant ion transport community, since in addition to the fact that they raised questions of structural evolution within the HKT family, at least for the former of these studies, they identified OsHKT2;4 as a potential actor of plant cell Ca 2+ signaling, in which very few proteins playing a role as Ca 2+ transporters or channels have been clearly identified at the molecular level so far (White et al, 2002;Ali et al, 2007;Cho et al, 2009;Laohavisit et al, 2010Laohavisit et al, , 2012.…”