The solute specificity profiles of nucleobase cation symporter 1 (NCS1) from Zea mays and Setaria viridis illustrate functional flexibility

详细信息    查看全文

• 作者：Micah Rapp ; Jessica Schein ; Kevin A. Hunt ; Vamsi Nalam ; George S. Mourad…
• 关键词：Setaria viridis ; Zea mays ; Purine ; Pyrimidine ; Nucleobase cation symporter 1
• 刊名：Protoplasma
• 出版年：2016
• 出版时间：March 2016
• 年：2016
• 卷：253
• 期：2
• 页码：611-623
• 全文大小：3,353 KB
• 参考文献：Argyrou E, Sophianopoulou V, Schultes N, Diallinas G (2001) Functional characterization of a maize purine transporter by expression in Aspergillus nidulans. Plant Cell 13:953–964CrossRef PubMed PubMedCentral
  Ashihara H, Sano H, Crozier A (2008) Caffeine and related purine alkaloids: biosynthesis, catabolism, function and genetic engineering. Phytochemistry 69:841–856CrossRef PubMed
  Bennetzen JL, Schmutz J, Wang H, Percifield R, Hawkins J, Pontaroli AC, Estep M, Feng L, Vaughn JN, Grimwood J, Jenkins J, Barry K, Lindquist E, Hellsten U, Deshpande S, Wang X, Wu X, Mitros T, Triplett J, Yang X, Ye C-Y, Mauro-Herrera M, Wang L, Li P, Manoj Sharma M, Sharma R, Ronald PC, Panaud O, Kellogg EA, Brutnell TP, Doust AN, Tuskan GA, Rokhsar D, Devos KM (2012) Reference genome sequence of the model plant Setaria. Nat Biotechnol 30:555–561CrossRef PubMed
  Bréthes D, Chirio MC, Napias C, Chevallier MR, Lavie JL, Chevallier J (1992) In vivo and in vitro studies of the purine cytosine permease of Saccharomyces cerevisiae: functional analysis of a mutant with an altered apparent transport constant of uptake. Eur J Biochem 204:699–704CrossRef PubMed
  Bürkle L, Cedzich A, Dopke C, Stransky H, Okumoto S, Gillissen B, Kuhn C, Frommer WB (2003) Transport of cytokinins mediated by purine transporters of the PUP family expressed in phloem, hydathodes, and pollen of Arabidopsis. Plant J 34:13–26CrossRef PubMed
  Cedzich A, Stransky H, Schulz B, Frommer WB (2008) Characterization of cytokinin and adenine transport in Arabidopsis cell cultures. Plant Physiol 148:1857–1867CrossRef PubMed PubMedCentral
  Christianson TW, Sikorsk RS, Dant M, Shero JH, Hieter P (1992) Multifunctional yeast high copy-number shuttle vectors. Gene 110:119–122CrossRef PubMed
  Collier R, Tegeder M (2012) Soybean ureide transporters play a critical role in nodule development, function and nitrogen export. Plant J 72:355–367CrossRef PubMed
  De Koning H, Diallinas G (2000) Nucleobase transporters. Mol Membr Biol 17:75–94CrossRef PubMed
  Desimone M, Catoni E, Ludewig U, Hilpert M, Schneider A, Kunze R, Tegeder M, Frommer WB, Schumacher K (2002) A novel superfamily of transporters for allantoin and other oxo-derivatives of nitrogen heterocyclic compounds in Arabidopsis. Plant Cell 14:847–856CrossRef PubMed PubMedCentral
  Emanuelsson O, Nielsen H, von Heijne G (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci 8:978–984CrossRef PubMed PubMedCentral
  Ferreira T, Bréthes D, Pinson B, Napias C, Chevallier J (1997) Functional analysis of mutated purine-cytosine permease from Saccharomyces cerevisiae. J Biol Chem 272:9697–9702CrossRef PubMed
  Ferreira T, Napias C, Chevallier J, Bréthes D (1999a) Evidence for a dynamic role for proline376 in the purine-cytosine permease of Saccharomyces cerevisiae. Eur J Biochem 263:57–64CrossRef PubMed
  Ferreira T, Chevallier J, Paumard P, Napias C, Bréthes D (1999b) Screening of an intragenic second-site suppressor of purine-cytosine permease from Saccharomyces cerevisiae. Eur J Biochem 260:22–30CrossRef PubMed
  Frébort I, Kowalska M, Hluska T, Frébortova J, Galuszka P (2011) Evolution of cytokinin biosynthesis and degradation. J Exp Bot 62:2431–2452CrossRef PubMed
  Friso G, Majeran W, Huang M, Sun Q, van Wijk KJ (2010) Reconstruction of metabolic pathways, protein expression, and homeostasis machineries across maize bundle sheath and mesophyll chloroplasts: large-scale quantitative proteomics using the first maize genome assembly1. Plant Physiol 152:1219–1250CrossRef PubMed PubMedCentral
  Gietz DR, Woods RA (2002) Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol 350:87–96CrossRef PubMed
  Gillissen B, Bürkle L, André B, Kühn C, Rentsch K, Brandl B, Frommer WB (2000) A new family of high-affinity transporters for adenine, cytosine, and purine derivatives in Arabidopsis. Plant Cell 12:291–300CrossRef PubMed PubMedCentral
  Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Daniel S, Rokhsar DS (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40(D1):D1178–D1186CrossRef PubMed PubMedCentral
  Gournas C, Papageorgiou I, Diallinas G (2008) The nucleobase-ascorbate transporter (NAT) family: genomics, evolution, structure-function relationships and physiological role. Mol Biosyst 4:404–414CrossRef PubMed
  Hamari Z, Amillis S, Drevet C, Apostolaki A, Vágvölgyi C, Diallinas G, Scazzocchio C (2009) Convergent evolution and orphan genes in the Fur4p-like family and characterization of a general nucleoside transporter in Aspergillus nidulans. Mol Microbiol 73:43–57CrossRef PubMed
  Jelesko JG (2012) An expanding role for purine uptake permease-like transporters in plant secondary metabolism. Front Plant Sci 3:1–5CrossRef
  Jeschke G (2013) A comparative study of structures and structural transitions of secondary transporters with the LeuT fold. Eur Biophys J 42:181–197CrossRef PubMed PubMedCentral
  Jund R, Chevallier MR, Lacroute F (1988) Primary structure of the uracil transport protein of Saccharomyces cerevisiae. Eur J Biochem 171:417–424CrossRef PubMed
  Kafer C, Zhou L, Santoso D, Guirgis A, Weers B, Park S, Thornburg R (2004) Regulation of pyrimidine metabolism in plants. Front Biosci 9:1611–1625CrossRef PubMed
  Kombrick E, Beevers H (1983) Transport of purine and pyrimidine bases and nucleosides from endosperm to cotyledons in germinating castor bean seedlings. Plant Physiol 73:370–376CrossRef
  Krogh A, Larsson B, von Heijne G, Sonnhammer ELL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580CrossRef PubMed
  Krypotou E, Kosti V, Amillis S, Myrianthopoulos V, Mikros E, Diallinas G (2012) Modeling, substrate docking and mutational analysis identify residues essential for the function and specificity of a eukaryotic purine-cytosine NCS1 transporter. J Biol Chem 287:36792–36803CrossRef PubMed PubMedCentral
  Ma P, Baldwin JM, Baldwin SA, Henderson PJF (2013) Membrane transport proteins: the nucleobase cation symporter 1 family. In: Roberts GCK (ed) Encyclopedia of biophysics. Springer, European Biophysical Societies’ Association, pp 1485–1489CrossRef
  Mansfield TA, Schultes NP, Mourad GS (2009) AtAzg1 and AtAzg2 comprise a novel family of purine transporters in Arabidopsis. Fed Euro Biochem Soc Lett 583:481–486CrossRef
  Maurino VG, Grube E, Zielinski J, Schild A, Fischer K, Flügge U-I (2006) Identification and expression analysis of twelve members of the nucleobase–ascorbate transporter (NAT) gene family in Arabidopsis thaliana. Plant Cell Physiol 47:1381–1393CrossRef PubMed
  Moffatt BA, Ashihara H (2002) Purine and pyrimidine nucleotide synthesis and metabolism In: Somerville CR, Meyerowitz EM (eds) The Arabidopsis book. American Society of Plant Biologists, pp 1-20. doi/10.​1199/​tab.​0018
  Mourad GS, Tippmann-Crosby J, Hunt KA, Gicheru Y, Bade K, Mansfield TA, Schultes NP (2012) Genetic and molecular characterization reveals a unique nucleobase cation symporter 1 in Arabidopsis. Fed Euro Biochem Soc Lett 586:1370–1378CrossRef
  Nelson BK, Cai X, Nebenführ A (2007) A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J 51:1126–1136CrossRef PubMed
  Niopek-Witz S, Deppe J, Lemieux MJ, Möhlmann T (2014) Biochemical characterization and structure-function relationship of two plant NCS2 proteins, the nucleobase transporters NAT3 and NAT12 from Arabidopsis thaliana. Biochim Biophys Acta 12:3025–3035CrossRef
  Pantazopoulou A, Diallinas G (2007) Fungal nucleobase transporters. FESM Microbiol Rev 31:657–675CrossRef
  Ross CW (1991) Biosynthesis of nucleotides, In: Stumpf PK, Conn EE (eds) The biochemistry of plants. Academic Press, pp 169–205.
  Schein J, Hunt KA, Minton J, Schultes NP, Mourad GS (2013) The nucleobase cation symporter 1 from Chlamydomonas reinhardtii and the evolutionary distant Arabidopsis thaliana share function and establish a plant-specific solute transport profile. Plant Physiol Biochem 70:52–60CrossRef PubMed
  Schmidt A, Su Y_H, Kunze R, Warner S, Hewitt M, Slocum RD, Ludewig U, Frommer WB, Desimone M (2004) UPS1 and UPS2 from Arabidopsis mediate high affinity transport of uracil and 5-fluorouracil. J Biol Chem 279:44817–44824CrossRef PubMed
  Schmidt A, Baumann N, Schwarzkopf A, Frommer WB, Desimone M (2006) Comparative studies on ureide permeases in Arabidopsis thaliana and analysis of two alternative splice variants of AtUPS5. Planta 224:1329–1340CrossRef PubMed
  Schultes NP, Brutnell TP, Allen A, Dellaporta SL, Nelson T, Chen J (1996) Leaf permease1 gene of maize is required for chloroplast development. Plant Cell 8:463–475CrossRef PubMed PubMedCentral
  Serrano R, Villalba J-M (1995) Expression and localization of plant membrane proteins in Saccharomyces. Methods Cell Biol 50:481–496CrossRef PubMed
  Shi Y (2013) Common folds and transport mechanisms of secondary active transporters. Annu Rev Biophys 42:51–72CrossRef PubMed
  Shimamura T, Weyand S, Beckstein O, Rutherford NG, Hadden JM, Sharples D, Sansom MSP, Iwata S, Henderson PJF, Cameron AD (2010) Molecular basis of alternating access membrane transport by the sodium-hydantoin transporter Mhp1. Science 328:470–473CrossRef PubMed PubMedCentral
  Soderlund C, Descour A, Kudrna D, Bomhoff M, Boyd L, Currie J, Angelova A, Collura K, Wissotski M, Ashley E, Morrow D, Fernandes J, Walbot V, Yu Y (2009) Sequencing, mapping, and analysis of 27,455 maize full-length cDNAs. PLoS Genet 5:e1000740CrossRef PubMed PubMedCentral
  Stasolla C, Katahira R, Thorpe TA, Ashihara H (2003) Purine and pyrimidine nucleotide metabolism in higher plants. J Plant Physiol 160:1271–1295CrossRef PubMed
  Stolz J, Vielreicher M (2003) Tpn1p, the plasma membrane vitamin B6 transporter of Saccharomyces cerevisiae. J Biol Chem 278:18990–18996CrossRef PubMed
  Szydlowski N, Bürkle L, Pourcel L, Moulin M, Stolz J, Fitzpatrick TB (2013) Recycling of pyridoxine (vitamin B6) by PUP1 in Arabidopsis. Plant J 75:40–52CrossRef PubMed
  Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680CrossRef PubMed PubMedCentral
  Wagner R, de Montigny J, de Wergifosse P, Souciet JL, Potier S (1998) The ORF YBL042 of Saccharomyces cerevisiae encodes a uridine permease. FESM Microbiol Lett 159:69–75CrossRef
  Werner AK, Witte C-P (2011) The biochemistry of nitrogen mobilization: purine ring catabolism. Trends Plant Sci 16:381–387CrossRef PubMed
  Weyand S, Shimamura T, Yajima S, Suzuki S, Mirza O, Krusong K, Carpenter EP, Rutherford NG, Hadden JM, O’Reilly J, Ma P, Saidijam M, Patching SG, Hope RJ, Norbertczak HT, Roach PCJ, Iwata S, Henderson PJF, Cameron AD (2008) Structure and molecular mechanism of a nucleobase–cation–symport-1 family transporter. Science 322:709–713CrossRef PubMed PubMedCentral
  Weyand S, Shimamura T, Beckstein O, Sansom MSP, Iwata S, Henderson PJF, Cameron AD (2011) The alternating access mechanism of transport as observed in the sodium-hydantoin transporter Mhp1. J Synchrotron Radiat 18:20–23CrossRef PubMed PubMedCentral
  Winzeler EA, Shoemaker DD, Astromoff A, Liang H, Anderson K, Andre B, Bangham R, Benito R, Boeke JD, Bussey H, Chu AM, Connelly C, Davis K, Dietrich F, Dow SW, Bakkoury ME, Foury F, Friend SH, Gentalen E, Giaever G, Hegemann JH, Jones T, Laub M, Liao H, Davis RW (1999) Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285:901–906CrossRef PubMed
  Witz S, Jung B, Fürst S, Möhlmann T (2012) De novo pyrimidine nucleotide synthesis mainly occurs outside of plastids, but a previously undiscovered nucleobase importer provides substrates for the essential salvage pathway in Arabidopsis. Plant Cell 24:1549–1559CrossRef PubMed PubMedCentral
  Witz S, Panwar P, Schober M, Deppe J, Pasha FA, Lemieux MJ, Möhlmann T (2014) Structure-function relationship of a plant NCS1 member—homology modeling and mutagenesis identified residues critical for substrate specificity of PLUTO, a nucleobase transporter from Arabidopsis. PLoS 9(3):e91343CrossRef
  Yan N (2013) Structural investigations of the proton-coupled secondary transporters. Curr Opin Struct Biol 23:483–491CrossRef PubMed
  Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2:1565–1572CrossRef PubMed
  Zrenner R, Stitt M, Sonnewald U, Boldt R (2006) Pyrimidine and purine biosynthesis and degradation in plants. Annu Rev Plant Biol 57:805CrossRef PubMed
  Zrenner R, Riegler H, Marquard CR, Lange PR, Geserick C, Bartosz CE, Chen CT, Solcum RD (2009) A functional analysis of the pyrimidine catabolic pathway in Arabidopsis. New Phytol 183:117–132CrossRef PubMed PubMedCentral
  
• 作者单位：Micah Rapp (1)
  Jessica Schein (1)
  Kevin A. Hunt (1)
  Vamsi Nalam (1)
  George S. Mourad (1)
  Neil P. Schultes (2)
  
  1. Department of Biology, Indiana University-Purdue University Fort Wayne, 2101 East Coliseum Blvd., Fort Wayne, IN, 46805, USA
  2. Department of Plant Pathology and Ecology, The Connecticut Agricultural Experiment Station, 123 Huntington St, New Haven, CT, 06511, USA
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Life Sciences
  Cell Biology
  Plant Sciences
  Zoology
  
• 出版者：Springer Wien
• ISSN：1615-6102

文摘

The solute specificity profiles (transport and binding) for the nucleobase cation symporter 1 (NCS1) proteins, from the closely related C4 grasses Zea mays and Setaria viridis, differ from that of Arabidopsis thaliana and Chlamydomonas reinhardtii NCS1. Solute specificity profiles for NCS1 from Z. mays (ZmNCS1) and S. viridis (SvNCS1) were determined through heterologous complementation studies in NCS1-deficient Saccharomyces cerevisiae strains. The four Viridiplantae NCS1 proteins transport the purines adenine and guanine, but unlike the dicot and algal NCS1, grass NCS1 proteins fail to transport the pyrimidine uracil. Despite the high level of amino acid sequence similarity, ZmNCS1 and SvNCS1 display distinct solute transport and recognition profiles. SvNCS1 transports adenine, guanine, hypoxanthine, cytosine, and allantoin and competitively binds xanthine and uric acid. ZmNCS1 transports adenine, guanine, and cytosine and competitively binds, 5-fluorocytosine, hypoxanthine, xanthine, and uric acid. The differences in grass NCS1 profiles are due to a limited number of amino acid alterations. These amino acid residues do not correspond to amino acids essential for overall solute and cation binding or solute transport, as previously identified in bacterial and fungal NCS1, but rather may represent residues involved in subtle solute discrimination. The data presented here reveal that within Viridiplantae, NCS1 proteins transport a broad range of nucleobase compounds and that the solute specificity profile varies with species.