The oligopeptide transporters: A small gene family with a diverse group of substrates and functions?

Molecular Plant

Volumn 4, Issue 3, 2011, Pages 407-415

  Lubkowitz, Mark ^a  

^a SAINT MICHAEL'S COLLEGE   (United States)

Author keywords

Molecular transport; nutrient and metal transport; Oligopeptide Transporters; transporters

Indexed keywords

EID: 79957480610     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1093/mp/ssr004     Document Type: Review

References (61)

1. Aouida, M., Khodami-Pour, A., and Ramotar, D. (2009). Novel role for the Saccharomyces cerevisiae oligopeptide transporter Opt2 in drug detoxification. Biochem. Cell Biol. 87, 653-661.
2. Barker, L., Kühn, C., Weise, A., Schulz, A., Gebhardt, C., Hirner, B., Hellmann, H., Schulze,W.,Ward, J.M., and Frommer,W.B. (2000). SUT2, a putative sucrose sensor in sieve elements. Plant Cell. 12, 1153-1164. (Pubitemid 30622719)
3. Bock, K.W., Honys, D., Ward, J.M., Padmanaban, S., Nawrocki, E.P., Hirschi, K.D., Twell, D., and Sze, H. (2006). Integrating membrane transport with male gametophyte development and function through transcriptomics. Plant Physiol. 140, 1151-1168. (Pubitemid 43956204)
4. Bogs, J., Bourbouloux, A., Cagnac, O., Wachter, A., Rausch, T., and Delrot, S. (2003). Functional characterization and expression analysis of a glutathione transporter, BjGT1, from Brassica juncea: evidence for regulation by heavy metal exposure. Plant Cell Environ. 26, 1703-1711. (Pubitemid 37292585)
5. Bourbouloux, A., Shahi, P., Chakladar, A., Delrot, S., and Bachhawat, A.K. (2000). Hgt1p, a high affinity glutathione transporter from the yeast Saccharomyces cerevisiae. J. Biol. Chem. 275, 13259-13265. (Pubitemid 30257381)
6. Buckhout, T.J., Yang, J.W., and Schmidt, W. (2009). Early irondeficiency- induced transcriptional changes in Arabidopsis roots as revealed by microarray analyses. BMC Genom. 10, 147.
7. Cagnac, O., Bourbouloux, A., Chakrabarty, D., Zhang, M.Y., and Delrot, S. (2004). AtOPT6 transports glutathione derivatives and is induced by primisulfuron. Plant Physiol. 135, 1378-1387. (Pubitemid 39009385)
8. Carter, C., Pan, S., Zouhar, J., Avila, E.L., Girke, T., and Raikhel, N.V. (2004). The vegetative vacuole proteome of Arabidopsis thaliana reveals predicted and unexpected proteins. Plant Cell. 16, 3285-3303. (Pubitemid 41096007)
9. Chu, H., Chiecko, J., Punshon, T., Lanzirotti, A., Lahner, B., Salt, D.E., and Walker, E.L. (2010). Successful reproduction requires the function of Arabidopsis YELLOW STRIPE-LIKE1 and YELLOW STRIPE-LIKE3 metal-nicotianamine transporters in both vegetative and reproductive structures. Plant Physiol. 154, 197-210.
10. Cobbett, C., and Goldsbrough, P. (2002). Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu. Rev. Plant Biol. 53, 159-182. (Pubitemid 36257491)
11. Curie, C., Panaviene, Z., Loulergue, C., Dellaporta, S.L., Briat, J.F., and Walker, E.L. (2001). Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake. Nature. 409, 346-349. (Pubitemid 32151239)
12. DiDonato, R.J., Jr, Roberts, L.A., Sanderson, T., Eisley, R.B., and Walker, E.L. (2004). Arabidopsis Yellow Stripe-Like2 (YSL2): a metal-regulated gene encoding a plasma membrane transporter of nicotianamine-metal complexes. Plant J. 39, 403-414. (Pubitemid 39040145)
13. Eide, D., Broderius M., Fett J., and Guerinot, M.L. (1996). A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc. Natl Acad. Sci. U S A. 93, 5624-5628. (Pubitemid 26159502)
14. Gendre, D., Czernic, P., Conejero, G., Pianelli, K., Briat, J.F., Lebrun, M., and Mari, S. (2007). TcYSL3, a member of the YSL gene family from the hyper-accumulator Thlaspi caerulescens, encodes a nicotianamine-Ni/Fe transporter. Plant J. 49, 1-15. (Pubitemid 44952693)
15. Gepstein, S., Sabehi, G., Carp, M.J., Hajouj, T., Nesher,MFO, Yariv, I., Dor, C. and Bassani, M. (2003). Large-scale identification of leaf senescence-associated genes. Plant J. 36, 629-642. (Pubitemid 37496491)
16. Grusak, M. (1994). Iron transport to developing ovules of Pisum safivud: seed import characteristics and phloem iron-loading capacity of source regions. Plant Physiol. 104, 649-655.
17. Hauser, M., Donhardt, A.M., Barnes, D., Naider, F., and Becker, J.M. (2000). Enkephalins are transported by a novel eukaryotic peptide uptake system. J. Biol. Chem. 275, 3037-3041. (Pubitemid 30082997)
18. Ho, C.H., Lin, S.H., Hu, H.C., and Tsay, Y.F. (2009). CHL1 functions as a nitrate sensor in plants. Cell. 138, 1184-1194.
19. Hunt, E., Gattolin, S., Newbury, H.J., Bale, J.S., Tseng, H.M., Barrett, D.A., and Pritchard, J. (2010). A mutation in amino acid permease AAP6 reduces the amino acid content of the Arabidopsis sieve elements but leaves aphid herbivores unaffected. J. Exp. Bot. 61, 55-64.
20. Jaquinod, M., Villiers, F., Kieffer-Jaquinod, S., Hugouvieux, V., Bruley, C., Garin, J., and Bourguignon, J. (2007). A proteomics dissection of Arabidopsis thaliana vacuoles isolated from cell culture. Mol. Cellul. Proteom. 6, 394-412. (Pubitemid 46561913)
21. Kim, D.-Y., Bovet, L., Maeshima, M., Martinoia, E., and Youngsook Lee,Y. (2007).TheABCtransporterAtPDR8isacadmiumextrusion pump conferring heavy metal resistance. Plant J. 50, 207-218. (Pubitemid 46624130)
22. Koh, S., Wiles, A.M., Sharp, J.S., Naider, F.R., Becker, J.M., and Stacey, G. (2002). An oligopeptide transporter gene family in Arabidopsis. Plant Physiol. 128, 21-29. (Pubitemid 34119507)
23. Koike, S., Inoue, H., Mizuno, D., Takahashi, M., Nakanishi, H., Mori, S., and Nishizawa, N.K. (2004). OsYSL2 is a rice metal-nicotianamine transporter that is regulated by iron and expressed in the phloem. Plant J. 39, 415-424. (Pubitemid 39040146)
24. Komarova, N.Y., Thor, K., Gubler, A., Meier, S., Dietrich, D., Weichert, A., Grotemeyer, M.S., Tegeder, M., and Rentsch, D. (2008). AtPTR1 and AtPTR5 transport dipeptides in planta. Plant Physiol. 148, 856-869. (Pubitemid 352847544)
25. Kuzuhara, Y., Isobe, A., Awazuhara, M., Fujiwara, T., and Hayashi, H. (2000). Glutathione levels in phloem sap of rice plants under sulfur deficient conditions. Soil Sci. Plant Nutr. 46, 265-270. (Pubitemid 30192251)
26. Long, T.A., Tsukagoshi, H., Busch, W., Lahner, B., Salt, D.E., and Benfey, P.A. (2010). The bHLH transcription factor POPEYE regulates response to iron deficiency in Arabidopsis roots. Plant Cell. 22, 2219-2236.
27. Lubkowitz, M.A., Barnes, D., Breslav, M., Burchfield, A., Naider, F., and Becker, J.M. (1998). Schizosaccharomyces pombe isp4 encodes an oligopeptide transporter and is a member of a novel family of oligopeptide transporters. Mol. Microbiol. 28, 729-741. (Pubitemid 28234383)
28. Lubkowitz, M.A., Hauser, L., Breslav,M., Naider, F., and Becker, J.M. (1997). An oligopeptide transport gene from Candida albicans. Microbiology. 143, 387-396. (Pubitemid 27092174)
29. Mendoza-Cozatl, D.G., Butko, E., Springer, F., Torpey J.W., Komives E.A., Kehr, J., and Schroeder, J.I. (2008). Identification of high levels of phytochelatins, glutathione and cadmium in the phloem sap of Brassica napus: a role for thiol-peptides in the long-distance transport of cadmium and the effect of cadmium on iron translocation. Plant J. 54, 249-259. (Pubitemid 351503116)
30. Murata, Y., Ma, J.F., Yamaji, F., Ueno, D., Nomoto, K., and Iwashita, T. (2006). A specific transporter for iron(III)-phytosiderophore in barley roots. Plant J. 46, 563-572.
31. Ortiz, D.F., Ruscitti, T., McCue, K.F., and Ow, D.W. (1995). Transport of metal-binding peptides by Hmt1, a fission yeast ABC-type vacuolar membrane-protein. J. Biol. Chem. 270, 4721-4728.
32. Osawa, H., Stacey, G., andGassmann,W. (2006). ScOPT1 andAtOPT4 functionas proton-coupledoligopeptide transporters withbroad but distinct substrate specificities. Biochem. J. 393, 267-275. (Pubitemid 43049323)
33. Pich, A., and Scholz, G. (1996). Translocation of copper and other micronutrients in tomato plants (Lycopersicon esculentum Mill.): nicotianamine-stimulated copper transport in the xylem. J. Exp. Bot. 47, 41-47.
34. Pike, S., Patel, A., Stacey, G., and Gassmann,W. (2009). Arabidopsis OPT6 is an oligopeptide transporter with exceptionally broad substrate specificity. Plant Cell Physiol. 50, 1923-1932.
35. Roberts, L.A., Pierson, A.J., Panavise, Z., and Walker, E.L. (2004). Yellow Stripe1 expanded roles for the Maize iron-phytosiderophore transporter. Plant Physiol. 135, 112-120. (Pubitemid 38653658)
36. Robinson, N.J., Procter, C.M., Connolley, E.T., and Guerinot, M.L. (1999). A ferric-chelate reductase for iron uptake from soils. Nature. 397, 694-697.
37. Sanders, A., Collier, R., Trethewy, A., Gould, G., Sieker, R., and Tegeder, M. (2009). AAP1 regulates import of amino acids into developing Arabidopsis embryos. Plant J. 59, 540-552.
38. Schaaf, G., Ludewig, U., Erenoglu, B.E., Mori, S., Kitahara, T., and von Wiren, N. (2004). ZmYS1 functions as a proton-coupled symporter for phytosiderophore- and nicotianamine-chelated metals. J. Biol. Chem. 279, 9091-9096. (Pubitemid 38295973)
39. Schmidke, I., and Stephan, U.W. (1995). Transport of metal micronutrients in the phloem of castor bean (Ricinus communis) seedlings. Physiol. Plant. 95, 147-153.
40. Schmidt, R., Stransky, H., and Koch, W. (2007). The amino acid permease AAP8 is important for early seed development in Arabidopsis thaliana. Planta. 226, 805-813. (Pubitemid 47283072)
41. Shimaoka, T., Ohnishi, M., Sazuka, T., Mitsuhashi, N., Hara Nishimura, I., Shimazaki, K.I., Maeshima, M., Yokota, A., Tomizawa, K.I., and Mimura, T. (2004). Isolation of intact vacuoles and proteomic analysis of tonoplast from suspension-cultured cells of Arabidopsis thaliana. Plant Cell Physiol. 45, 672-683. (Pubitemid 38893491)
42. Srivastava, A.K., Ramaswamy, N.K., Suprasanna, P., and D'Souza, S.F. (2010). Genome-wide analysis of thioureamodulated salinity stress-responsive transcripts in seeds of Brassica juncea: identification of signaling and effector components of stress tolerance. Ann. Bot. 106, 663-674.
43. Stacey, M.G., Koh, S., Becker, J., and Stacey,G. (2002). AtOPT3, amember of the oligopeptide transporter family, is essential for embryo development in Arabidopsis. Plant Cell. 14, 2799-2811. (Pubitemid 35326305)
44. Stacey, M.G., Osawa, H., Patel, A., Gassmann, W., and Stacey, G. (2006). Expression analyses of Arabidopsis oligopeptide transporters during seed germination, vegetative growth and reproduction. Planta. 223, 291-305. (Pubitemid 43011732)
45. Stacey, M.G., Patel, A., McClain, W.E., Mathieu, M., Remley, M., Rogers, E.E., Gassmann, W., Blevins, D.G., and Stacey, G. (2008). The Arabidopsis AtOPT3 protein functions in metal homeostasis and movement of iron to developing seeds. Plant Physiol. 146, 589-601. (Pubitemid 351230787)
46. Steiner, H.Y., Song, W., Zhang, L., Naider, F., Becker, J.M., and Stacey, G. (1994). An Arabidopsis peptide transporter is a member of a new class of membrane transport proteins. Plant Cell. 6, 1289-1299.
47. Szponarski, W., Sommerer, N., Boyer, J.C., Rossignol, M., and Gibrat, R. (2004). Large-scale characterization of integral proteins from Arabidopsis vacuolar membrane by twodimensional liquid chromatography. Proteomics. 4, 397-406. (Pubitemid 38235256)
48. Tegeder, M., and Rentsch, D. (2010). Uptake and partitioning of amino acids and peptides. Mol. Plant. 3, 997-1011.
49. Thakur, A., Kaur, J., and Anand, K. (2008). Bachhawat Pgt1, a glutathione transporter from the fission yeast Schizosaccharomyces pombe. FEMS Yeast Res. 8, 916-929.
50. Thomine, S., LeLievre, F., Debarbieux, E., Schroeder, J.I., and Barbier- Brygoo, H. (2003). AtNRAMP3, a multispecific vacuolar metal transporter involved in plant responses to iron deficiency. Plant J. 34, 685-695. (Pubitemid 36720202)
51. Truernit, E., Stadler, R., Baier, K., and Sauer, N. (1999). A male gametophyte- specific monosaccharide transporter in Arabidopsis. Plant J. 17, 191-201.
52. Vasconcelos, M.W., Li, G.W., Lubkowitz, M.A., and Grusak, M.A. (2008). Characterization of the PT clade of oligopeptide transporters in rice. Plant Genome. 1, 77-88.
53. Vert, G.A., Briat, J.F., and Curie, C. (2002). Dual regulation of the Arabidopsis high-affinity root iron uptake system by local and long-distance signals. Plant Physiol. 132, 796-804. (Pubitemid 36715078)
54. von Wiren, N., Klair, S., Bansal, S., Briat, J.F., Khodr, H., Shioiri, T., Leigh, R.A., and Hider, R.C. (1999). Nicotianamine chelates both Fe(III) and Fe(II): implication for metal transport in plants. Plant Physiol. 119, 1107-1114. (Pubitemid 29388283)
55. Wang, Y.Q., Zhu, S.Y.,Wang, Y., and Zhang, M.Y. (2007). Tissue and inducible expression of a rice glutathione transporter gene promoter in transgenic Arabidopsis. Botan. Stud. 48, 35-41. (Pubitemid 46293914)
56. Wiles, A.M., Naider, F., and Becker, J.M. (2006). Transmembrane domain prediction and consensus sequence identification of the oligopeptide transport family. Res. Microbiol. 4, 395-406.
57. Wintz, H., Fox, T., Wu, Y.Y., Feng, V., Chen, W.Q., Chang, H.S., Zhu, T., and Vulpe, C. (2003). Expression profiles of Arabidopsis thaliana in mineral deficiencies reveal novel transporters involved in metal homeostasis. J. Biol. Chem. 278, 47644-47653. (Pubitemid 37523209)
58. Yen, M.R., Tseng, Y.H., and Saier, M.H., Jr (2001). Maize Yellow Stripe1, an iron-phytosiderophore uptake transporter, is a member of the oligopeptide transporter (OPT) family. Microbiology. 147, 2881-2883.
59. Zhang, M.Y., Bourbouloux, A., Cagnac, O., Srikanth, C.V., Rentsch, D., Bachhawat, A.K., and Delrot, S. (2004). A novel family of transporters mediating the transport of glutathione derivatives in plants. Plant Physiol. 134, 482-491. (Pubitemid 38178719)
60. Zheng, L., et al. (2009). Physiological and transcriptome analysis of iron and phosphorus interaction in rice seedlings. Plant Physiol. 151, 262-274.
61. Zhu, Y.L., Pilon-Smits, E.A.H., Tarun, A.S., Weber, S.U., Jouanin, L., and Terry, N. (1999). Cadmium tolerance and accumulation in Indian mustard is enhanced by over expressing gammaglutamylcysteine synthetase. Plant Physiol. 121, 1169-1177. (Pubitemid 30018503)