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J. Biol. Chem., Vol. 277, Issue 21, 18373-18382, May 24, 2002

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Functional Characterization of Betaine/Proline Transporters in Betaine-accumulating Mangrove^*

Rungaroon Waditee^§, Takashi Hibino^¶, Yoshito Tanaka^¶, Tatsunosuke Nakamura, Aran Incharoensakdi^§, Shinsuke Hayakawa^**, Shigetoshi Suzuki^**, Yuzo Futsuhara^**, Yoshinobu Kawamitsu, Tetsuko Takabe^§§, and Teruhiro Takabe^¶¶

From the  Research Institute, ^¶ Faculty of Science and Technology, and ^** School of Agriculture, Meijo University, Nagoya 468-8502, Japan, ^§ Department of Biochemistry, Faculty of Science, Chulalongkorn University, Bangkok 10330, Thailand,  Faculty of Pharmaceutical Science, Chiba University, Chiba 263-8522, Japan,  Faculty of Agriculture, University of the Ryukyus, Okinawa 903-0213, Japan, and ^§§ Graduate School of Agricultural Science, Nagoya University, Chikusa-ku, Nagoya, Aichi 464-8601 Japan

Betaine is an important osmoprotectant in many plants, but its transport activity has only been demonstrated using a proline transporter from tomato, a betaine-nonaccumulating plant. In this study, two full-length and one partial transporter genes were isolated from betaine-accumulating mangrove Avicennia marina. Their homologies to betaine transporters from bacteria and betaine/4-aminobutyrate transporters from mammalian cells were low but were high to proline transporters from Arabidopsis and tomato. Two full-length transporters could complement the Na⁺-sensitive phenotype of the Escherichia coli mutant deficient in betT, putPA, proP, and proU. Both transporters could efficiently take up betaine and proline with similar affinities (K_m, 0.32-0.43 mM) and maximum velocities (1.9-3.6 nmol/min/mg of protein). The uptakes of betaine and proline were significantly inhibited by mono- and dimethylglycine but only partially inhibited by betaine aldehyde, choline, and 4-aminobutyrate. Sodium and potassium chloride markedly enhanced betaine uptake rates with optimum concentrations at 0.5 M, whereas sucrose showed only modest activation. The change of amino acids Thr²⁹⁰-Thr-Ser²⁹² in a putative periplasmic loop to Arg²⁹⁰-Gly-Arg²⁹² yielded the active transporter independent of salts, suggesting the positive charge induced a conformational change to the active form. These data clearly indicate that the betaine-accumulating mangrove contains betaine/proline transporters whose properties are distinct from betaine transporters of bacteria and mammalian cells.

The nucleotide sequence(s) reported in this paper has been submitted to the DDBJ/GenBank^TM/EBI Data Bank with accession number(s) AB075902, AB075903, and AB075904.

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