OsHKT2;2/1-mediated Na+ influx over K+ uptake in roots potentially increases toxic Na+ accumulation in a salt-tolerant landrace of rice Nona Bokra upon salinity stress
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HKT transporters are Na+-permeable membrane proteins, which mediate Na+ and K+ homeostasis in K+-depleted and saline environments in plants. Class II HKT transporters, a distinct subgroup found predominantly in monocots, are known to mediate Na+-K+ co-transport in principle. Here we report features of ion transport functions of No-OsHKT2;2/1, a class II transporter identified in a salt tolerant landrace of indica rice, Nona Bokra. We profiled No-OsHKT2;2/1 expression in organs of Nona Bokra plants with or without salinity stress. Dominant accumulation of the No-OsHKT2;2/1 transcript in K+-starved roots of Nona Bokra plants largely disappeared in response to 50 mM NaCl. We found that No-OsHKT2;2/1 expressed in the high-affinity K+ uptake deficient mutant of Saccharomyces cerevisiae and Xenopus laevis oocytes shows robust K+ selectivity even in the presence of a large amount of NaCl as reported previously. However, No-OsHKT2;2/1-expressing yeast cells exhibited Na+ hypersensitive growth under various concentrations of K+ and Na+ as the cells expressing Po-OsHKT2;2, a similar class II transporter from another salt tolerant indica rice Pokkali, when compared with the growth of cells harboring empty vector or cells expressing OsHKT2;4. The OsHKT2;4 protein expressed in Xenopus oocytes showed strong K+ selectivity in the presence of 50 mM NaCl in comparison with No-OsHKT2;2/1 and Po-OsHKT2;2. Together with apparent plasma membrane-localization of No-OsHKT2;2/1, these results point to possibilities that No-OsHKT2;2/1 could mediate destructive Na+ influx over K+ uptake in Nona Bokra plants upon salinity stress, and that a predominant physiological function of No-OsHKT2;2/1 might be the acquisition of Na+ and K+ in K+-limited environments.
KeywordsHKT K+ uptake Na+ transport Rice Salt stress
We would like to express our gratitude to Dr. Kazuya Yoshida and Prof. Yoshiyuki Murata (Okayama Univ.) for helpful discussions. We also would like to thank Prof. Jian Feng Ma (Okayama Univ.), Dr. Pulla Kaothien-Nakayama and Ms. Saori Okamura for the support of TEVC experiments, the comments on the manuscript and the assistance for this study, respectively. This work was supported by the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan 25119709 and the MEXT as part of Joint Research Program implemented at the Institute of Plant Science and Resources, Okayama University in Japan 2520, 2622, 2716 (to T.H.). The research in A.C. lab is supported by a grant from the Ministero dell’Istruzione, dell’Università e della Ricerca Fondo per gli Investimenti della Ricerca di Base (FIRB) 2010 RBFR10S1LJ_001.
- Flowers TJ, Läuchli A (1983) Sodium versus potassium: Substitution and compartmentation. Inorganic Plant Nutrition 15:651–681Google Scholar
- Hamamoto S, Horie T, Hauser F, Deinlein U, Schroeder JI, Uozumi N (2014) HKT transporters mediate salt stress resistance in plants: from structure and function to the field. Curr Opin Biotech. 32C:113–120Google Scholar
- Horie T, Brodsky DE, Costa A, Kaneko T, Lo Schiavo F, Katsuhara M, Schroeder JI (2011) K+ transport by the OsHKT2;4 transporter from rice with atypical Na+ transport properties and competition in permeation of K+ over Mg2+ and Ca2+ ions. Plant Physiol 156:1493–1507PubMedPubMedCentralCrossRefGoogle Scholar
- Jabnoune M, Espeout S, Mieulet D, Fizames C, Verdeil JL, Conejero G, Rodriguez-Navarro A, Sentenac H, Guiderdoni E, Abdelly C, Very AA (2009) Diversity in expression patterns and functional properties in the rice HKT transporter family. Plant Physiol 150:1955–1971PubMedPubMedCentralCrossRefGoogle Scholar
- Kato Y, Sakaguchi M, Mori Y, Saito K, Nakamura T, Bakker EP, Sato Y, Goshima S, Uozumi N (2001) Evidence in support of a four transmembrane-pore-transmembrane topology model for the Arabidopsis thaliana Na+/K+ translocating AtHKT1 protein, a member of the superfamily of K+ transporters. Proc Natl Acad Sci USA 98:6488–6493PubMedPubMedCentralCrossRefGoogle Scholar
- Mäser P, Eckelman B, Vaidyanathan R, Horie T, Fairbairn DJ, Kubo M, Yamagami K, Yamaguchi K, Nishimura M, Uozumi N, Robertson W, Sussman MR, Schroeder JI (2002a) Altered shoot/root Na+ distribution and bifurcating salt sensitivity in Arabidopsis by genetic disruption of the Na+ transporter AtHKT1. FEBS Lett 531:157–161PubMedCrossRefGoogle Scholar
- Mäser P, Hosoo Y, Goshima S, Horie T, Eckelman B, Yamada K, Yoshida K, Bakker EP, Shinmyo A, Oiki S, Schroeder JI, Uozumi N (2002b) Glycine residues in potassium channel-like selectivity filters determine potassium selectivity in four-loop-per-subunit HKT transporters from plants. Proc Natl Acad Sci USA 99:6428–6433PubMedPubMedCentralCrossRefGoogle Scholar
- Sunarpi Horie T, Motoda J, Kubo M, Yang H, Yoda K, Horie R, Chan WY, Leung HY, Hattori K, Konomi M, Osumi M, Yamagami M, Schroeder JI, Uozumi N (2005) Enhanced salt tolerance mediated by AtHKT1 transporter-induced Na+ unloading from xylem vessels to xylem parenchyma cells. Plant J. 44:928–938PubMedCrossRefGoogle Scholar
- Takai T, Nonoue Y, Yamamoto S, Yamanouchi U, Matsubara K, Liang ZW, Lin HX, Ono N, Uga Y, Yano M (2007) Development of chromosome segment substitution lines derived from backcross between indica donor rice cultivar ‘Nona Bokra’ and Japonica recipient cultivar ‘Koshihikari’. Breed Sci. 57:257–261CrossRefGoogle Scholar
- Tholema N, Vor der Bruggen M, Maser P, Nakamura T, Schroeder JI, Kobayashi H, Uozumi N, Bakker EP (2005) All four putative selectivity filter glycine residues in KtrB are essential for high affinity and selective K+ uptake by the KtrAB system from Vibrio alginolyticus. J Biol Chem 280:41146–41154PubMedCrossRefGoogle Scholar