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

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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.