Diversity in Expression Patterns and Functional Properties in the Rice HKT Transporter Family  

Abstract

Plant growth under low K + availability or salt stress requires tight control of K + and Na + uptake, long-distance transport, and accumulation. The family of membrane transporters named HKT (for High-Affinity K + Transporters), permeable either to K + and Na + or to Na + only, is thought to play major roles in these functions. Whereas Arabidopsis (Arabidopsis thaliana) possesses a single HKT transporter, involved in Na + transport in vascular tissues, a larger number of HKT transporters are present in rice (Oryza sativa) as well as in other monocots. Here, we report on the expression patterns and functional properties of three rice HKT transporters, OsHKT1;1, OsHKT1;3, and OsHKT2;1. In situ hybridization experiments revealed overlapping but distinctive and complex expression patterns, wider than expected for such a transporter type, including vascular tissues and root periphery but also new locations, such as osmocontractile leaf bulliform cells (involved in leaf folding). Functional analyses in Xenopus laevis oocytes revealed striking diversity. OsHKT1;1 and OsHKT1;3, shown to be permeable to Na + only, are strongly different in terms of affinity for this cation and direction of transport (inward only or reversible). OsHKT2;1 displays diverse permeation modes, Na + -K + symport, Na + uniport, or inhibited states, depending on external Na + and K + concentrations within the physiological concentration range. The whole set of data indicates that HKT transporters fulfill distinctive roles at the whole plant level in rice, each system playing diverse roles in different cell types. Such a large diversity within the HKT transporter family might be central to the regulation of K + and Na + accumulation in monocots.Although it is not clear what levels of Na + are toxic in the plant cell cytosol and actually unacceptable in vivo, the hypothesis that this cation must be excluded from the cytoplasm is widely accepted. The most abundant inorganic cation in the cytosol is K + , in plant as in animal cells. This cation has probably been selected during evolution because it is less chaotropic than Na + (i.e. more compatible with protein structure even at high concentrations; Clarkson and Hanson, 1980). Its selection might also be due to the fact that in primitive cells, which originated in environmental conditions (seawater) where Na + was more abundant than K + , a straightforward process to energize the cell membrane was to accumulate the less abundant cation and to exclude the most abundant one.In the cell, K + plays a role in basic functions, such as regulation of cell membrane polarization, electrical neutralization of anionic groups, and osmoregulation. Concerning the latter function, K + uptake or release is the usual way through which plant cells control their water potential and turgor. Although toxic at high concentrations, Na + can be used as osmoticum and substituted for K and tissue levels have actually been shown to be essential in plant adaptation to salt stress (Greenway and Munns, 1980;Flowers, 1985;Hasegawa...

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

“…5C). This result, indicating an increased Na + transport activity in OsHKT2;4 in low K + and high Na + conditions, is consistent with what was suggested by the reciprocal experiment described by Figure 4, E and F. It should be noted that HKT2;1-type transporters from different cereals have been proposed to be able to mediate Na + -K + symport when expressed in yeast and/or Xenopus oocytes (Rubio et al, 1995;Haro et al, 2005;Jabnoune et al, 2009;Mian et al, 2011). Within the framework of the hypothesis that OsHKT2;4 could also mediate Na + -K + symport activity with variable stoichiometry, as proposed for HvHKT2;1 transporter when expressed in oocytes (Mian et al, 2011), a shift in reversal potential of currents of 31 mV per 10-fold change in ionic activity is very close to the expected shift in a symport of monovalent cations with a 1:1 stoichiometry (i.e.…”

“…3, B and D). Comparing OsHKT2;4 with other HKT transporters so far characterized and in particular with those described as K + permeable (HKT2;1 from different cereals and OsHKT2;2), it could be noticed that OsHKT2;4 displayed the highest conductance to K + relative to that to Na + : Indeed, the conductance to K + was (slightly) higher than the conductance to Na + in OsHKT2;4 (in bath solutions comprising only K + or Na + as monovalent cation), whereas it was strongly lower (by more than 4 times) than the conductance to Na + in all other HKT transporters (Rubio et al, 1995;Gassmann et al, 1996;Uozumi et al, 2000;Horie et al, 2001;Jabnoune et al, 2009;Mian et al, 2011; Fig. 3D; Supplemental Fig.…”

“…S2). Furthermore, the comparison of the reversal potential of currents in the presence of K + or Na + also suggested a selectivity for K + higher in OsHKT2;4 than in other characterized HKT transporters (Gassmann et al, 1996;Jabnoune et al, 2009;Mian et al, 2011;Supplemental Fig. S2).…”

“…Cereals possess a much larger number of HKT genes, e.g. five to 11 genes in the different wheat genomes (Huang et al, 2008) and nine genes in rice (Oryza sativa; Garciadeblás et al, 2003), leading to functional diversity within this family (Jabnoune et al, 2009;Corratgé-Faillie et al, 2010). Based on functional studies in heterologous systems (Xenopus oocytes or yeast cells) and phylogenetic analyses, higher plant HKT transporters have been sorted out into two subfamilies .…”

Cesium Accumulation in Paddy Field Rice Grown in Fukushima from 2011 to 2013: Cultivars and Fertilization

“…Both K and Cs are alkali metals, and Cs transportation is known to be mediated by several K transporters (Qi et al 2008;Jabnoune et al 2009). Thus, Cs uptake and transportation by K transporters compete with K uptake and transportation in plants.…”