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Identification of Arabidopsis thaliana NRT1/PTR FAMILY (NPF) proteins capable of transporting plant hormones

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Abstract

NRT1/PTR FAMILY (NPF) proteins were originally identified as nitrate or di/tri-peptide transporters. Recent studies revealed that this transporter family also transports the plant hormones auxin (indole-3-acetic acid), abscisic acid (ABA), and gibberellin (GA), as well as secondary metabolites (glucosinolates). We developed modified yeast two-hybrid systems with receptor complexes for GA and jasmonoyl-isoleucine (JA-Ile), to detect GA and JA-Ile transport activities of proteins expressed in the yeast cells. Using these GA and JA-Ile systems as well as the ABA system that we had introduced previously, we determined the capacities of Arabidopsis NPFs to transport these hormones. Several NPFs induced the formation of receptor complexes under relatively low hormone concentrations. Hormone transport activities were confirmed for some NPFs by direct analysis of hormone uptake of yeast cells by liquid chromatography–tandem mass spectrometry. Our results suggest that at least some NPFs could function as hormone transporters.

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References

  • Almagro A, Lin SH, Tsay YF (2008) Characterization of the Arabidopsis nitrate transporter NRT1.6 reveals a role of nitrate in early embryo development. Plant Cell 20:3289–3299

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Blakeslee JJ, Peer WA, Murphy AS (2005) Auxin transport. Curr Opin Plant Biol 8:494–500

    Article  CAS  PubMed  Google Scholar 

  • Boursiac Y, Leran S, Corratge-Faillie C, Gojon A, Krouk G, Lacombe B (2013) ABA transport and transporters. Trends Plant Sci 18:325–333

    Article  CAS  PubMed  Google Scholar 

  • Endo A, Sawada Y, Takahashi H, Okamoto M, Ikegami K, Koiwai H, Seo M, Toyomasu T, Mitsuhashi W, Shinozaki K, Nakazono M, Kamiya Y, Koshiba T, Nambara E (2008) Drought induction of Arabidopsis 9-cis-epoxycarotenoid dioxygenase occurs in vascular parenchyma cells. Plant Physiol 147:1984–1993

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fan SC, Lin CS, Hsu PK, Lin SH, Tsay YF (2009) The Arabidopsis nitrate transporter NRT1.7, expressed in phloem, is responsible for source-to-sink remobilization of nitrate. Plant Cell 21:2750–2761

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Guo FQ, Young J, Crawford NM (2003) The nitrate transporter AtNRT1.1 (CHL1) functions in stomatal opening and contributes to drought susceptibility in Arabidopsis. Plant Cell 15:107–117

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Habets ME, Offringa R (2014) PIN-driven polar auxin transport in plant developmental plasticity: a key target for environmental and endogenous signals. New Phytol 203:362–377

    Article  CAS  PubMed  Google Scholar 

  • Hsu PK, Tsay YF (2013) Two phloem nitrate transporters, NRT1.11 and NRT1.12, are important for redistributing xylem-borne nitrate to enhance plant growth. Plant Physiol 163:844–856

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Huang NC, Liu KH, Lo HJ, Tsay YF (1999) Cloning and functional characterization of an Arabidopsis nitrate transporter gene that encodes a constitutive component of low-affinity uptake. Plant Cell 11:1381–1392

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jiang F, Hartung W (2008) Long-distance signalling of abscisic acid (ABA): the factors regulating the intensity of the ABA signal. J Exp Bot 59:37–43

    Article  CAS  PubMed  Google Scholar 

  • Jikumaru Y, Asami T, Seto H, Yoshida S, Yokoyama T, Obara N, Hasegawa M, Kodama O, Nishiyama M, Okada K, Nojiri H, Yamane H (2004) Preparation and biological activity of molecular probes to identify and analyze jasmonic acid-binding proteins. Biosci Biotechnol Biochem 68:1461–1466

    Article  CAS  PubMed  Google Scholar 

  • Kang J, Hwang JU, Lee M, Kim YY, Assmann SM, Martinoia E, Lee Y (2010) PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid. Proc Natl Acad Sci USA 107:2355–2360

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kanno Y, Hanada A, Chiba Y, Ichikawa T, Nakazawa M, Matsui M, Koshiba T, Kamiya Y, Seo M (2012) Identification of an abscisic acid transporter by functional screening using the receptor complex as a sensor. Proc Natl Acad Sci USA 109:9653–9658

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Karim S, Holmstrom KO, Mandal A, Dahl P, Hohmann S, Brader G, Palva ET, Pirhonen M (2007) AtPTR3, a wound-induced peptide transporter needed for defence against virulent bacterial pathogens in Arabidopsis. Planta 225:1431–1445

    Article  CAS  PubMed  Google Scholar 

  • Kende H, Zeevaart J (1997) The five “classical” plant hormones. Plant Cell 9:1197–1210

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ko D, Kang J, Kiba T, Park J, Kojima M, Do J, Kim KY, Kwon M, Endler A, Song WY, Martinoia E, Sakakibara H, Lee Y (2014) Arabidopsis ABCG14 is essential for the root-to-shoot translocation of cytokinin. Proc Natl Acad Sci USA 111:7150–7155

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Koiwai H, Nakaminami K, Seo M, Mitsuhashi W, Toyomasu T, Koshiba T (2004) Tissue-specific localization of an abscisic acid biosynthetic enzyme, AAO3, in Arabidopsis. Plant Physiol 134:1697–1707

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Komarova NY, Thor K, Gubler A, Meier S, Dietrich D, Weichert A, Suter Grotemeyer M, Tegeder M, Rentsch D (2008) AtPTR1 and AtPTR5 transport dipeptides in planta. Plant Physiol 148:856–869

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kretzschmar T, Kohlen W, Sasse J, Borghi L, Schlegel M, Bachelier JB, Reinhardt D, Bours R, Bouwmeester HJ, Martinoia E (2012) A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching. Nature 483:341–344

    Article  CAS  PubMed  Google Scholar 

  • Krouk G, Lacombe B, Bielach A, Perrine-Walker F, Malinska K, Mounier E, Hoyerova K, Tillard P, Leon S, Ljung K, Zazimalova E, Benkova E, Nacry P, Gojon A (2010) Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Dev Cell 18:927–937

    Article  CAS  PubMed  Google Scholar 

  • Kuromori T, Miyaji T, Yabuuchi H, Shimizu H, Sugimoto E, Kamiya A, Moriyama Y, Shinozaki K (2010) ABC transporter AtABCG25 is involved in abscisic acid transport and responses. Proc Natl Acad Sci USA 107:2361–2366

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Leran S, Varala K, Boyer JC, Chiurazzi M, Crawford N, Daniel-Vedele F, David L, Dickstein R, Fernandez E, Forde B, Gassmann W, Geiger D, Gojon A, Gong JM, Halkier BA, Harris JM, Hedrich R, Limami AM, Rentsch D, Seo M, Tsay YF, Zhang M, Coruzzi G, Lacombe B (2014) A unified nomenclature of NITRATE TRANSPORTER 1/PEPTIDE TRANSPORTER family members in plants. Trends Plant Sci 19:5–9

    Article  CAS  PubMed  Google Scholar 

  • Li JY, Fu YL, Pike SM, Bao J, Tian W, Zhang Y, Chen CZ, Li HM, Huang J, Li LG, Schroeder JI, Gassmann W, Gong JM (2010) The Arabidopsis nitrate transporter NRT1.8 functions in nitrate removal from the xylem sap and mediates cadmium tolerance. Plant Cell 22:1633–1646

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lin SH, Kuo HF, Canivenc G, Lin CS, Lepetit M, Hsu PK, Tillard P, Lin HL, Wang YY, Tsai CB, Gojon A, Tsay YF (2008) Mutation of the Arabidopsis NRT1.5 nitrate transporter causes defective root-to-shoot nitrate transport. Plant Cell 20:2514–2528

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lumba S, Cutler S, McCourt P (2010) Plant nuclear hormone receptors: a role for small molecules in protein–protein interactions. Annu Rev Cell Dev Biol 26:445–469

    Article  CAS  PubMed  Google Scholar 

  • Matsuura H, Takeishi S, Kiatoka N, Sato C, Sueda K, Masuta C, Nabeta K (2012) Transportation of de novo synthesized jasmonoyl isoleucine in tomato. Phytochemistry 83:25–33

    Article  CAS  PubMed  Google Scholar 

  • Nakajima M, Shimada A, Takashi Y, Kim YC, Park SH, Ueguchi-Tanaka M, Suzuki H, Katoh E, Iuchi S, Kobayashi M, Maeda T, Matsuoka M, Yamaguchi I (2006) Identification and characterization of Arabidopsis gibberellin receptors. Plant J 46:880–889

    Article  CAS  PubMed  Google Scholar 

  • Nour-Eldin HH, Andersen TG, Burow M, Madsen SR, Jorgensen ME, Olsen CE, Dreyer I, Hedrich R, Geiger D, Halkier BA (2012) NRT/PTR transporters are essential for translocation of glucosinolate defence compounds to seeds. Nature 488:531–534

    Article  CAS  PubMed  Google Scholar 

  • Parker JL, Newstead S (2014) Molecular basis of nitrate uptake by the plant nitrate transporter NRT1.1. Nature 507:68–72

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Petrasek J, Friml J (2009) Auxin transport routes in plant development. Development 136:2675–2688

    Article  CAS  PubMed  Google Scholar 

  • Pimenta Lange MJ, Knop N, Lange T (2012) Stamen-derived bioactive gibberellin is essential for male flower development of Cucurbita maxima L. J Exp Bot 63:2681–2691

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Santner A, Estelle M (2009) Recent advances and emerging trends in plant hormone signalling. Nature 459:1071–1078

    Article  CAS  PubMed  Google Scholar 

  • Santner A, Calderon-Villalobos LI, Estelle M (2009) Plant hormones are versatile chemical regulators of plant growth. Nat Chem Biol 5:301–307

    Article  CAS  PubMed  Google Scholar 

  • Seo M, Koshiba T (2011) Transport of ABA from the site of biosynthesis to the site of action. J Plant Res 124:501–507

    Article  CAS  PubMed  Google Scholar 

  • Sun J, Bankston JR, Payandeh J, Hinds TR, Zagotta WN, Zheng N (2014) Crystal structure of the plant dual-affinity nitrate transporter NRT1.1. Nature 507:73–77

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Swarup R, Peret B (2012) AUX/LAX family of auxin influx carriers—an overview. Front Plant Sci 3:225

    Article  PubMed Central  PubMed  Google Scholar 

  • Takeuchi J, Okamoto M, Akiyama T, Muto T, Yajima S, Sue M, Seo M, Kanno Y, Kamo T, Endo A, Nambara E, Hirai N, Ohnishi T, Cutler SR, Todoroki Y (2014) Designed abscisic acid analogs as antagonists of PYL–PP2C receptor interactions. Nat Chem Biol 10:477–482

    Article  CAS  PubMed  Google Scholar 

  • Tsay YF, Chiu CC, Tsai CB, Ho CH, Hsu PK (2007) Nitrate transporters and peptide transporters. FEBS Lett 581:2290–2300

    Article  CAS  PubMed  Google Scholar 

  • Wang YY, Tsay YF (2011) Arabidopsis nitrate transporter NRT1.9 is important in phloem nitrate transport. Plant Cell 23:1945–1957

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yang H, Murphy AS (2009) Functional expression and characterization of Arabidopsis ABCB, AUX 1 and PIN auxin transporters in Schizosaccharomyces pombe. Plant J 59:179–191

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Zhu H, Pan Y, Yu Y, Luan S, Li L (2014a) A DTX/MATE-type transporter facilitates abscisic acid efflux and modulates ABA sensitivity and drought tolerance in Arabidopsis. Mol Plant 7:1522–1532

    Article  CAS  PubMed  Google Scholar 

  • Zhang K, Novak O, Wei Z, Gou M, Zhang X, Yu Y, Yang H, Cai Y, Strnad M, Liu CJ (2014b) Arabidopsis ABCG14 protein controls the acropetal translocation of root-synthesized cytokinins. Nat Commun 5:3274

    PubMed  Google Scholar 

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Acknowledgments

This work was supported in part by the Japan Society of Promotion of Science (JSPS) KAKENHI [Challenging Exploratory Research (24657040) to M.S.].

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Authors and Affiliations

  1. Department of Biological Sciences, Tokyo Metropolitan University, Hachioji-shi, Tokyo, 192-0387, Japan

    Yasutaka Chiba, Shinya Miyakawa, Tomokazu Koshiba & Mitsunori Seo

  2. RIKEN Center for Sustainable Resource Science, Yokohama, Kanagawa, 230-0045, Japan

    Yasutaka Chiba, Takafumi Shimizu, Yuri Kanno, Yuji Kamiya & Mitsunori Seo

Authors
  1. Yasutaka Chiba
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  2. Takafumi Shimizu
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  3. Shinya Miyakawa
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  4. Yuri Kanno
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  5. Tomokazu Koshiba
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  6. Yuji Kamiya
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  7. Mitsunori Seo
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Correspondence to Mitsunori Seo.

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Chiba, Y., Shimizu, T., Miyakawa, S. et al. Identification of Arabidopsis thaliana NRT1/PTR FAMILY (NPF) proteins capable of transporting plant hormones. J Plant Res 128, 679–686 (2015). https://doi.org/10.1007/s10265-015-0710-2

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  • DOI: https://doi.org/10.1007/s10265-015-0710-2

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