Molecular basis of nitrate uptake by the plant nitrate transporter NRT1.1

Nature

Volumn 507, Issue 7490, 2014, Pages 68-72

  Parker, Joanne L ^a   Newstead, Simon ^a,b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b RUTHERFORD APPLETON LABORATORY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

NITRATE; NITRATE TRANSPORTER; THREONINE;

DATA SET; HERB; HORMONE; LIGAND; MOLECULAR ANALYSIS; NITRATE; NITROGEN; NUTRIENT CYCLING; NUTRIENT UPTAKE; PEPTIDE; PHOSPHORUS; SECONDARY METABOLITE;

ARABIDOPSIS THALIANA; ARTICLE; CRYSTAL STRUCTURE; ENZYME SPECIFICITY; EUKARYOTE; NITRATE UPTAKE; NITROGEN FIXATION; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL;

ARABIDOPSIS THALIANA; EUKARYOTA;

ANION TRANSPORT PROTEINS; ARABIDOPSIS; CRYSTALLOGRAPHY, X-RAY; HISTIDINE; ION TRANSPORT; MODELS, MOLECULAR; NITRATES; PHOSPHORYLATION; PHOSPHOTHREONINE; PLANT PROTEINS; PROTEIN CONFORMATION; PROTONS; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY;

EID: 84895877254     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature13116     Document Type: Article

References (57)

1. Steiner, H.-Y., Naider, F. & Becker, J. M. The PTR family: a new group of peptide transporters. Mol. Microbiol. 16, 825-834 (1995).
2. Daniel, H., Spanier, B., Kottra, G. & Weitz, D. From bacteria to man: archaic protondependent peptide transporters at work. Physiology (Bethesda) 21, 93-102 (2006).
3. Crawford, N. M. Nitrate: nutrient and signal for plant growth. Plant Cell 7, 859-868 (1995).
4. Tsay, Y. F. & Hsu, P. K. The role of plasma membrane nitrogen transporters in nitrogen acquisition and utilization. Plant Cell Monogr. 19, 223-236 (2011).
5. Orsel, M. et al. Characterization of a two-component high-affinity nitrate uptake system in arabidopsis. physiology and protein-protein interaction. Plant Physiol. 142, 1304-1317 (2006).
6. Dechorgnat, J. et al. Fromthe soil to the seeds: the long journey of nitrate in plants. J. Exp. Bot. 62, 1349-1359 (2011).
7. Tsay, Y. F., Schroeder, J. I., Feldmann, K. A. & Crawford, N. M. The herbicide sensitivity gene CHL1 of Arabidopsis encodes a nitrate-inducible nitrate transporter. Cell 72, 705-713 (1993).
8. Léran, S. et al. A unified nomenclature of NITRATE TRANSPORTER 1/PEPTIDE TRANSPORTER family members in plants. Trends Plant Sci. 19, 5-9 (2013).
9. Tsay, Y.-F., Chiu, C.-C., Tsai, C.-B., Ho, C.-H. & Hsu, P.-K. Nitrate transporters and peptide transporters. FEBS Lett. 581, 2290-2300 (2007).
10. Boursiac, Y. et al. ABA transport and transporters. Trends Plant Sci. 18, 325-333 (2013).
11. Nour-Eldin, H. H., Andersen, T. G., Burow, M.&Madsen,S. R.NRT/PTRtransporters are essential for translocation of glucosinolate defence compounds to seeds. Nature 488, 531-534 (2012).
12. Krouk, G. et al. Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Dev. Cell 18, 927-937 (2010).
13. Reddy, V. S., Shlykov, M. A., Castillo, R., Sun, E. I. & Saier, M. H. The major facilitator superfamily (MFS) revisited. FEBS J. 279, 2022-2035 (2012).
14. Newstead, S. et al. Crystal structure of a prokaryotic homologue of themammalian oligopeptide-proton symporters, PepT1and PepT2.EMBOJ.30, 417-426 (2011).
15. Fei, Y. J. et al. Expression cloning of a mammalian proton-coupled oligopeptide transporter. Nature 368, 563-566 (1994).
16. Nakajima, H. et al. Cloning and functional expression in Escherichia coli of the gene encoding the di-and tripeptide transport protein of Lactobacillus helveticus. Appl. Environ. Microbiol. 63, 2213-2217 (1997).
17. Chiang, C.-S., Stacey, G. & Tsay, Y.-F. Mechanisms and functional properties of two peptide transporters, AtPTR2 and fPTR2. J. Biol. Chem. 279, 30150-30157 (2004).
18. Radestock, S. & Forrest, L. R. The alternating-access mechanism of MFS transporters arises from inverted-topology repeats. J. Mol. Biol. 407, 698-715 (2011).
19. Yan, N. Structural advances for the major facilitator superfamily (MFS) transporters. Trends Biochem. Sci. 38, 151-159 (2013).
20. Madej, M. G. & Kaback, H. R. Evolutionary mix-and-match with MFS transporters. Proc. Natl Acad. Sci. USA 110, E4831-E4838 (2013).
21. Solcan, N. et al. Alternating access mechanism in the POT family of oligopeptide transporters. EMBO J. 31, 3411-3421 (2012).
22. Doki, S. et al. Structural basis for dynamic mechanism of proton-coupled symport by the peptide transporter POT. Proc. Natl Acad. Sci. USA 110, 11343-11348 (2013).
23. Liu, K. H., Huang, C. Y. & Tsay, Y. F. CHL1 is a dual-affinity nitrate transporter of Arabidopsis involved in multiple phases of nitrate uptake. Plant Cell 11, 865-874 (1999).
24. Liu, K.-H. & Tsay, Y.-F. Switching between the two action modes of the dual-affinity nitrate transporter CHL1 by phosphorylation. EMBO J. 22, 1005-1013 (2003).
25. Wang, Y.-Y., Hsu, P.-K. & Tsay, Y.-F. Uptake, allocation and signaling of nitrate. Trends Plant Sci. 17, 458-467 (2012).
26. Baaske, P., Wienken, C., Willemsen, M. J. & Braun, D. Protein-binding assays in biological liquids using microscale thermophoresis. J. Biomol. Tech. 22, S55 (2011).
27. Wienken, C. J., Baaske, P., Rothbauer, U. & Braun, D. Protein-binding assays in biological liquids using microscale thermophoresis. Nature Commun. 1, 100 (2010).
28. Sun, L. et al. Crystal structure of a bacterial homologue of glucose transporters GLUT1-4. Nature 490, 361-366 (2012).
29. Dang, S. et al. Structure of a fucose transporter in an outward-open conformation. Nature 467, 734-738 (2010).
30. Guettou, F. et al. Structural insights into substrate recognitionin proton-dependent oligopeptide transporters. EMBO Rep. 14, 804-810 (2013).
31. Yan, H. et al. Structure and mechanism of a nitrate transporter. Cell Rep. 3, 716-723 (2013).
32. Chen, X.-Z., Zhu, T., Smith, D. E. & Hediger, M. A. Stoichiometry and kinetics of the high-affinity H1-coupled peptide transporter PepT2. J. Biol. Chem. 274, 2773-2779 (1999).
33. Chandrasekaran, A., Ojeda, A. M., Kolmakova, N. G.& Parsons, S. M.Mutational and bioinformatics analysis of proline-and glycine-rich motifs in vesicular acetylcholine transporter. J. Neurochem. 98, 1551-1559 (2006).
34. Ugolev, Y., Segal, T., Yaffe, D., Gros, Y. & Schuldiner, S. Identification of conformationally sensitive residues essential for inhibition of vesicular monoamine transport by the noncompetitive inhibitor-tetrabenazine. J. Biol. Chem. 288, 32160-32171 (2013).
35. Newstead, S. et al. High-throughput fluorescent-based optimization of eukaryotic membrane protein overexpression and purification in Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA 104, 13936-13941 (2007).
36. Kazemi Seresht, A., Nørgaard, P., Palmqvist, E. A., Andersen, A. S. & Olsson, L. Modulating heterologous protein production in yeast: the applicability of truncated auxotrophic markers. Appl. Microbiol. Biotechnol. 97, 3939-3948 (2013).
37. Drew, D. et al. GFP-based optimization scheme for the overexpression and purification of eukaryotic membrane proteins in Saccharomyces cerevisiae. Nature Protocols 3, 784-798 (2008).
38. Newstead, S., Ferrandon, S. & Iwata, S. Rationalizing a-helical membrane protein crystallization. Protein Sci. 17, 466-472 (2008).
39. Winter, G., Lobley, C. M. C.&Prince, S. M.Decisionmakingin xia2. Acta Crystallogr.D 69, 1260-1273 (2013).
40. Winter, G. xia2: an expert system for macromolecular crystallography data reduction. J. Appl. Cryst. 43, 186-190 (2009).
41. Kabsch, W. XDS. Acta Crystallogr. D 66, 125-132 (2010).
42. Evans, P. R. An introduction to data reduction: space-group determination, scaling and intensity statistics. Acta Crystallogr. D 67, 282-292 (2011).
43. Sheldrick, G. M. Experimental phasing with SHELXC/D/E: combining chain tracing with density modification. Acta Crystallogr. D 66, 479-485 (2010).
44. Abrahams, J. P. & Leslie, A. G. W. Methods used in the structure determination of bovine mitochondrial F1 ATPase. Acta Crystallogr. D 52, 30-42 (1996).
45. Cowtan, K. DM: an automated procedure for phase improvement by density modification. Joint CCP4 and ESF-EACBM Newsletter on Protein Crystallography 31, 34-38 (1994).
46. Pedersen, B. P., Morth, J. P. & Nissen, P. Structure determination using poorly diffracting membrane-protein crystals: the H1-ATPase and Na1,K1-ATPase case history. Acta Crystallogr. D 66, 309-313 (2010).
47. Jones, T. A., Zou, J. Y., Cowan,S. W.&Kjeldgaard, M.Improved methods for building proteinmodels in electron densitymaps and the location of errors in thesemodels. Acta Crystallogr. A 47, 110-119 (1991).
48. Yang, Z. et al. UCSF Chimera, MODELLER, and IMP: An integrated modeling system. J. Struct. Biol. 179, 269-278 (2012).
49. Blanc, E. et al. Refinement of severely incomplete structures with maximum likelihood in BUSTER-TNT. Acta Crystallogr. D 60, 2210-2221 (2004).
50. Davis, I. W., Murray, L. W., Richardson, J. S. & Richardson, D. C. MOLPROBITY: structure validation and all-atom contact analysis for nucleic acids and their complexes. Nucleic Acids Res. 32, W615-W619 (2004).
51. Schrodinger, LLC. The PyMOL Molecular Graphics System, Version 1.3r1.
52. Foucaud, C. & Poolman, B. Lactose transport system of Streptococcus thermophilus. Functional reconstitution of the protein and characterization of the kinetic mechanism of transport. J. Biol. Chem. 267, 22087-22094 (1992).
53. Knol, J. et al. Unidirectional reconstitutioninto detergent-destabilized liposomes of the purified lactose transport system of Streptococcus thermophilus. J. Biol. Chem. 271, 15358-15366 (1996).
54. Smirnova, I. et al. Sugar binding induces an outward facing conformation of LacY. Proc. Natl Acad. Sci. USA 104, 16504-16509 (2007).
55. Zheng, H., Wisedchaisri, G. & Gonen, T. Crystal structure of a nitrate/nitrite exchanger. Nature 497, 647-651 (2013).
56. Katoh, K. & Toh, H. Recent developments in the MAFFT multiple sequence alignment program. Brief. Bioinform. 9, 286-298 (2008).
57. Clamp, M., Cuff, J., Searle, S. M. & Barton, G. J. The Jalview Java alignment editor. Bioinformatics 20, 426-427 (2004).