Genome-wide identification and expression characterization of ABCC-MRP transporters in hexaploid wheat

Frontiers in Plant Science

Volumn 6, Issue JULY, 2015, Pages 1-15

  Bhati, Kaushal K ^a   Sharma, Shivani ^a   Aggarwal, Sipla ^a   Kaur, Mandeep ^a   Shukla, Vishnu ^a   Kaur, Jagdeep ^b   Mantri, Shrikant ^a   Pandey, Ajay K ^a  

^a NATIONAL AGRI FOOD BIOTECHNOLOGY INSTITUTE   (India)

^b PANJAB UNIVERSITY   (India)

Author keywords

ABCC MRP proteins; Cadmium stress; Detoxification; Seed development; Triticum aestivum; Yeast complementation

Indexed keywords

ARABIDOPSIS; TRITICUM AESTIVUM; ZEA MAYS;

EID: 84936950971     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00488     Document Type: Article

References (67)

1. Ali, M. A., Hussain, M., Khan, M. I., Ali, Z., Zulkiffal, M., Anwar, J., et al. (2010). Source-sink relationship between photosynthetic organs and grain yield attributes during grain filling stage in spring wheat (Triticum aestivum). Int. J. Agric. Biol. 12, 509-515.
2. Astolfi, S., Ortolani, M. R., Catarcione, G., Paolacci, A. R., Cesco, S., Pinton, R., et al. (2014). Cadmium exposure affects iron acquisition in barley (Hordeum vulgare) seedlings. Physiol. Plant. 152, 646-659. doi: 10. 1111/ppl. 12207.
3. Augustine, L. M., Markelewicz, R. Jr. Boekelheide, K., and Cherrington, N. J. (2005). Xenobiotic and endobiotic transporter mRNA expression in the blood-testis barrier. Drug Metab. Dispos. 33, 182-189. doi: 10. 1124/dmd. 104. 001024.
4. Bakos, E., Evers, R., Sinko, E., Varadi, A., Borst, P., and Sarkadi, B. (2000). Interactions of the human multidrug resistance proteins MRP1 and MRP2 with organic anions. Mol. Pharmacol. 57, 760-768. doi: 10. 1124/mol. 57. 4. 760.
5. Bhati, K. K., Aggarwal, S., Sharma, S., Mantri, S., Singh, S. P., Bhalla, S., et al. (2014). Differential expression of structural genes for the late phase of phytic acid biosynthesis in developing seeds of wheat (Triticum aestivum L.). Plant Sci. 224, 74-85. doi: 10. 1016/j. plantsci. 2014. 04. 009.
6. Bovet, L., Eggmann, T., Meylan-Bettex, M., Polier, J., Kammer, P., Marin, E., et al. (2003). Transcript levels of AtMRPs after cadmium treatment: induction of AtMRP3. Plant Cell Environ. 26, 371-381. doi: 10. 1046/j. 1365-3040. 2003. 00968. x.
7. Brunetti, P., Zanella, L., De Paolis, A., Di Litta, D., Cecchetti, V., Falasca, G., et al. (2015). Cadmium-inducible expression of the ABC-type transporter AtABCC3 increases phytochelatin-mediated cadmium tolerance in Arabidopsis. J. Exp. Bot. 66, 3815-3829. doi: 10. 1093/jxb/erv185.
8. Cakier, B., and Kilickaya, O. (2013). Whole-genome survey of the putative ATP-binding cassette transporter family genes in Vitis vinifera. PLoS ONE 8: e78860. doi: 10. 1371/journal. pone. 0078860.
9. Chaudhuri, B., Ingavale, S., and Bachhawat, A. K. (1997). apd1±, a gene required for red pigment formation in the ade6 mutants of Schizosaccharomyces pombe encodes an enzyme required for glutathione biosynthesis: a role for glutathione and a glutathione-conjugate pump. Genetics 145, 75-83.
10. Cho, U., and Seo, N. (2005). Oxidative stress in A. thaliana exposed to cadmium is due to hydrogen peroxide accumulation. Plant Sci. 168, 113-120. doi: 10. 1016/j. plantsci. 2004. 07. 021.
11. Clemens, S. (2001). Molecular mechanism of plant metal tolerance and homeostasis. Planta 212, 475-486. doi: 10. 1007/s004250000458.
12. Cuypers, A., Smeets, K., Ruytinx, J., Opdenakker, K., Keunen, E., Remans, T., et al. (2011). The cellular redox state as a modulator in cadmium and copper responses in Arabidopsis thalianaseedlings. J. Plant Physiol. 168, 309-316. doi: 10. 1016/j. jplph. 2010. 07. 010.
13. Eastmond, P. J., and Jones, R. L. (2005). Hormonal regulation of gluconeogenesis in cereal aleurone is strongly cultivar-dependent and gibberellin action involves SLENDER1 but not GAMYB. Plant J. 44, 483-493. doi: 10. 1111/j. 1365-313X. 2005. 02544. x.
14. Francisco, R. M., Regalado, A., Ageorges, A., Burla, B. J., Bassin, B., Eisenach, C., et al. (2013). ABCC1, an ATP binding cassette protein from grape berry, transports anthocyanidin 3-O-glucosides. Plant Cell 25, 1840-1854. doi: 10. 1105/tpc. 112. 102152.
15. Frelet-Barrand, A., Kolukisaoglu, H. U., Plaza, S., Ruffer, M., Azevedo, L., Hortensteiner, S., et al. (2008). Comparative mutant analysis of Arabidopsis ABCC-type ABC transporters: AtMRP2 contributes to detoxification, vacuolar organic anion transport and chlorophyll degradation. Plant Cell Physiol. 49, 557-569. doi: 10. 1093/pcp/pcn034.
16. Gaedeke, N., Klein, M., Kolukisaoglu, U., Forestier, C., Müller, A., Ansorge, M., et al. (2001). TheArabidopsis thaliana ABC transporter AtMRP5 controls root development and stomata movement. EMBO J. 20, 1875-1887. doi: 10. 1093/emboj/20. 8. 1875.
17. Gaillard, S., Jacquet, H., Vavasseur, A., Leonhardt, N., and Forestier, C. (2008). AtMRP6/AtABCC6, an ATP-Binding Cassette transporter gene expressed during early steps of seedling development and up-regulated by cadmium in Arabidopsis thaliana. BMC Plant Biol. 8: 22. doi: 10. 1186/1471-2229-8-22.
18. Garcia, O., Bouige, P., Forestier, C., and Dassa, E. (2004). Inventory and comparative analysis of rice and Arabidopsis ATP-binding cassette (ABC) systems. J. Mol. Biol. 343, 249-265. doi: 10. 1016/j. jmb. 2004. 07. 093.
19. Guizani, T. E., Blanc, N., Triki, S., St-Pierre, B., and Ducos, E. (2014). Expression pattern of AtABCC13/MRP11 reveals developmental, hormonal, and nutritional regulations. Biol. Plant. 58, 231-240. doi: 10. 1007/s10535-013-0387-0.
20. Henikoff, S., Greene, E. A., Pietrokovski, S., Bork, P., Attwood, T. K., and Hood, L. (1997). Gene families: the taxonomy of protein paralogs and chimeras. Science 278, 609-614. doi: 10. 1126/science. 278. 5338. 609.
21. Hwang, Y. S., Bethke, P. C., Gubler, F., and Jones, R. L. (2003). cPrG-HCl a potential H+/Cl-symporter prevents acidification of storage vacuoles in aleurone cells and inhibits GA-dependent hydrolysis of storage protein and phytate. Plant J. 35, 154-163. doi: 10. 1046/j. 1365-313X. 2003. 01789. x.
22. Ishikawa, T., Li, Z. S., Lu, Y. P., and Rea, P. A. (1997). The GS-X pump in plant, yeast, and animal cells: structure, function, and gene expression. Biosci. Rep. 17, 189-207. doi: 10. 1023/A: 1027385513483.
23. Jasinski, M., Ducos, E., Martinoia, E., and Boutry, M. (2003). The ATP-binding cassette transporters: structure, function, and gene family comparison between rice and Arabidopsis. Plant Physiol. 131, 1169-1177. doi: 10. 1104/pp. 102. 014720.
24. Jasiñski, M., Stukkens, Y., Degand, H., Purnelle, B., Marchand-Brynaert, J., and Boutry, M. (2001). A plant plasma membrane ATP binding cassette-type transporter is involved in antifungal terpenoid secretion. Plant Cell 13, 1095-1107. doi: 10. 1105/tpc. 13. 5. 1095.
25. Ji, H., Peng, Y., Meckes, N., Allen, S., Stewart, N., and Traw, M. B. (2014). ABC transporter AtABCG16 increases plant tolerance to abscisic acid and assists in basal resistance againstPseudomonas syringae DC3000. Plant Physiol. 166, 879-888. doi: 10. 1104/pp. 114. 248153.
26. Kang, J., Hwang, J. U., Lee, M., Kim, Y. Y., Assmann, S. M., Martinoia, E., et al. (2010). PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid. Proc. Natl. Acad. Sci. U. S. A. 107, 2355-2360. doi: 10. 1073/pnas. 0909222107.
27. Klaassen, C. D., and Aleksunes, L. M. (2010). Xenobiotic, bile acid, and cholesterol transporters: function and regulation. Pharmacol. Rev. 62, 1-96. doi: 10. 1124/pr. 109. 002014.
28. Klein, M., Burla, B., and Martinoia, E. (2006). The multidrug resistance-associated protein (MRP/ABCC) subfamily of ATP-binding cassette transporters in plants. FEBS Lett. 580, 1112-1122. doi: 10. 1016/j. febslet. 2005. 11. 056.
29. Klein, M., Martinoia, E., Hoffmann-Thoma, G., and Weissenbock, G. (2000). A membrane-potential dependent ABC-like transporter mediates the vacoular uptake of rye flavones glucuronidase: regulation of glucuronide uptake by glutathione and its conjugates. Plant J. 21, 289-304. doi: 10. 1046/j. 1365-313x. 2000. 00684. x.
30. Ko, D., Kang, J., Kiba, T., Park, J., Kojima, M., Do, J., et al. (2014). Arabidopsis ABCG14 is essential for the root-to-shoot translocation of cytokinin. Proc. Natl. Acad. Sci. U. S. A. 19, 7150-7155. doi: 10. 1073/pnas. 1321519111.
31. Kolukisaoglu, H. U., Bovet, L., Klein, M., Eggmann, T., Geisler, M., Wanke, D., et al. (2002). Family business: the multidrug-resistance related protein (MRP) ABC transporter genes inArabidopsis thaliana. Planta 216, 107-119. doi: 10. 1007/s00425-002-0890-6.
32. Li, Z. S., Szczypka, M., Lu, Y. P., Thiele, D. J., and Rea, P. A. (1996). The yeast cadmium factor protein (YCF1) is a vacuolar glutathione S-conjugate pump. J. Biol. Chem. 271, 6509-6517.
33. Liu, G., Sanchez-Fernandez, R., Li, Z. S., and Rea, P. A. (2001). Enhanced multi specificity ofArabidopsis vacuolar multidrug resistance-associated protein-type ATP-binding cassette transporter, AtMRP2. J. Biol. Chem. 276, 8648-8656. doi: 10. 1074/jbc. M009690200.
34. Ljung, K., Hull, A. K., Celenza, J., Yamada, M., Estelle, M., Normanly, J., et al. (2005). Sites and regulation of auxin biosynthesis in Arabidopsis roots. Plant Cell 17, 1090-1104. doi: 10. 1105/tpc. 104. 029272.
35. Lu, Y. P., Li, Z. S., Drozdowicz, Y. M., Hortensteiner, S., Martinoia, E., and Rea, P. A. (1998). AtMRP2, an Arabidopsis ATP binding cassette transporter able to transport glutathione S-conjugates and chlorophyll catabolites: functional comparisons with AtMRP1. Plant Cell 10, 267-282.
36. Marchler-Bauer, A., Lu, S., Anderson, J. B., Chitsaz, F., Derbyshire, M. K., DeWeese-Scott, C., et al. (2011). CDD: a conserved domain database for the functional annotation of proteins. Nucleic Acids Res. 39, 225-229. doi: 10. 1093/nar/gkq1189.
37. Martinoia, E., Grill, E., Tommasini, R., Kreuz, K., and Amrhein, N. (1993). An ATP-dependent glutathione-S-conjugate 'export' pump in the vacuolar membrane of plants. Nature 364, 247-249. doi: 10. 1038/364247a0.
38. Mayer, K. F., Rogers, K. F., Doležel, J., Pozniak, C., Eversole, K., Feuillet, C., et al. (2014). A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. International Wheat Genome Sequencing Consortium (IWGSC). Science 345: 1251788. doi: 10. 1126/science. 1251788.
39. Meda, A. R., Scheuermann, E. B., Prechsl, U. E., Erenoglu, B., Schaaf, G., Hayen, H., et al. (2007). Iron acquisition by phytosiderophores contributes to cadmium tolerance. Plant Physiol. 143, 1761-1773. doi: 10. 1104/pp. 106. 094474.
40. Nagy, R., Grob, H., Weder, B., Green, P., Klein, M., Frelet-Barrand, A., et al. (2009). TheArabidopsis ATP-binding cassette protein AtMRP5/AtABCC5 Is a high affinity inositol hexakisphosphate transporter involved in guard cell signaling and phytate storage. J. Biol. Chem. 284, 33614-33622. doi: 10. 1074/jbc. M109. 030247.
41. Pang, K., Li, Y., Liu, M., Meng, Z., and Yu, Y. (2013). Inventory and general analysis of the ATP-binding cassette (ABC) gene superfamily in maize (Zea mays L.). Gene 526, 411-428. doi: 10. 1016/j. gene. 2013. 05. 051.
42. Panzeri, D., Cassani, E., Doria, E., Tagliabue, G., Forti, L., Campion, B., et al. (2011). A defective ABC transporter of the MRP family, responsible for the bean lpa1 mutation, affects the regulation of the phytic acid pathway, reduces seed myo-inositol and alters ABA sensitivity. New Phytol. 191, 70-83. doi: 10. 1111/j. 1469-8137. 2011. 03666. x.
43. Park, J., Song, W., Ko, D., Eom, Y., Hansen, T. H., Schiller, M., et al. (2012). The phytochelatin transporters AtABCC1 and AtABCC2 mediate tolerance to cadmium and mercury. Plant J. 69, 278-288. doi: 10. 1111/j. 1365-313X. 2011. 04789. x.
44. Paumi, C. M., Chuk, M., Snider, J., Stagljar, I., and Michaelis, S. (2009). ABC transporters inSaccharomyces cerevisiae and their interactors: new technologies advances the biology of the ABCC (MRP) subfamily. Microbiol. Mol. Biol. Rev. 73, 577-593. doi: 10. 1128/MMBR. 00020-09.
45. Petrovic, S., Pascolo, L., Gallo, R., Cupelli, F., Ostrow, J. D., Goffeau, A., et al. (2000). The products of YCF1 and YLL015w (BPT1) cooperate for the ATP-dependent vacuolar transport of unconjugated bilirubin in Saccharomyces cerevisiae. Yeast 16, 561-571. doi: 10. 1002/(SICI)1097-0061(200004)16: 6&<561:: AID-YEA551&>3. 0. CO; 2-L.
46. Qiu, Z., Li, J., Zhang, M., Bi, Z., and Li, Z. (2013). He-Ne laser pretreatment protects wheat seedlings against cadmium-induced oxidative stress. Ecotoxicol. Environ. Saf. 88, 135-141. doi: 10. 1016/j. ecoenv. 2012. 11. 001.
47. Rea, P. A. (1999). MRP subfamily ABC transporters from plants and yeast. J. Exp. Bot. 50, 895-913. doi: 10. 1093/jxb/50. Special_Issue. 895.
48. Sanchez-Fernandez, R., Davies, T. G. E., Coleman, J., and Rea, P. A. (2001). The Arabidopsis thaliana ABC protein subfamily, a complete inventory. J. Biol. Chem. 276, 30231-30244. doi: 10. 1074/jbc. M103104200.
49. Schmitteng, L. (2001). Analysis of relative gene expression data using a real time quantitative PCRand 2-(Delta Delta C (T)) method. Methods 25, 402-408. doi: 10. 1006/meth. 2001. 1262.
50. Sharma, K. G., Kaur, R., and Bachhawat, A. K. (2003). The glutathione-mediated detoxification pathway in yeast: an analysis using the red pigment that accumulates in certain adenine biosynthetic mutants of yeasts reveals the involvement of novel genes. Arch. Microbiol. 180, 108-117. doi: 10. 1007/s00203-003-0566-z.
51. Sharma, K. G., Mason, D. L., Liu, G., Rea, P. A., Bachhawat, A. K., and Michaelis, S. (2002). Localization, regulation, and substrate transport properties of Bpt1p, a Saccharomyces cerevisiaeMRP-type ABC transporter. Eukaryotic Cell 1, 391-400. doi: 10. 1128/EC. 1. 3. 391-400. 2002.
52. Shi, J., Wang, W., Schellin, K., Li, B., Faller, M., Styoop, J. M., et al. (2007). Embryo-specific silencing of a transporter reduces phytic acid content of maize and soybean seeds. Nat. Biotechnol. 25, 930-937. doi: 10. 1038/nbt1322.
53. Singh, A., Mantri, S., Sharma, M., Chaudhury, A., Tuli, R., and Roy, J. (2014). Genome-wide transcriptome study in wheat identified candidate genes related to processing quality, majority of them showing interaction (quality × development) and having temporal and spatial distributions. BMC Genomics 15: 29. doi: 10. 1186/1471-2164-15-29.
54. Song, W. Y., Yamaki, T., Yamaji, N., Ko, D., Jung, K. H., Fujii-Kashino, M., et al. (2014). A rice ABC transporter, OsABCC1, reduces arsenic accumulation in the grain. Proc. Natl. Acad. Sci. U. S. A. 111, 15699-15704. doi: 10. 1073/pnas. 1414968111.
55. Sreenivasulu, N., Radchuk, V., Strickert, M., Miersch, O., Weschke, W., and Wobus, U. (2006). Gene expression patterns reveal tissue-specific signalling networks controlling programmed cell death and ABA-regulated maturation in developing barley grains. Plant J. 47, 310-327. doi: 10. 1111/j. 1365-313X. 2006. 02789. x.
56. Swarbreck, D., Ripoll, P. J., Brown, D. A., Edwards, K. J., and Theodoulou, F. (2003). Isolation and characterisation of two multidrug resistance associated protein genes from maize. Gene 315, 153-164. doi: 10. 1016/S0378-1119(03)00734-0.
57. Theodoulou, F. L., Clark, I. M., He, X.-L., Pallett, K. E., Cole, D. J., and Hallahan, D. L. (2003). Co-induction of glutathione-S-transferases and multidrug resistance associated protein by xenobiotics in wheat. Pest Manag. Sci. 59, 202-214. doi: 10. 1002/ps. 576.
58. Thiel, J., Weier, D., Sreenivasulu, N., Strickert, M., Weichert, N., Melzer, M., et al. (2008). Different hormonal regulation of cellular differentiation and function in nucellar projection and endosperm transfer cells: a microdissection-based transcriptome study of young barley grains. Plant Physiol. 148, 1436-1452. doi: 10. 1104/pp. 108. 127001.
59. Tommasini, R., Evers, R., Vogt, E., Mornet, C., Zaman, G., Schinkel, A. H., et al. (1996). The human multidrug resistance-associated protein functionally complements the yeast cadmium resistance factor-1. Proc. Natl. Acad. Sci. U. S. A. 93, 6743-6748. doi: 10. 1073/pnas. 93. 13. 6743.
60. Tommasini, R., Vogt, E., Fromenteau, M., Hoertensteiner, S., Matile, P., Amrhein, N., et al. (1998). An ABC-transporter of Arabidopsis thaliana has both glutathione-conjugate and chlorophyll catabolite transport activity. Plant J. 13, 773-780. doi: 10. 1046/j. 1365-313X. 1998. 00076. x.
61. Verrier, P. J., Bird, D., Burla, B., Dassa, E., Forestier, C., Geisler, M., et al. (2008). Plant ABC proteins-a unified nomenclature and updated inventory. Trends Plant Sci. 13, 151-159. doi: 10. 1016/j. tplants. 2008. 02. 001.
62. Walter, S., Brennan, J., Arunachalam, C., Ansari, K., Hu, X., Khan, M. R., et al. (2008). Components of the gene network associated with genotype-dependent response of wheat to theFusarium mycotoxin deoxynivalenol. Funct. Integr. Genomics 8, 421-427. doi: 10. 1007/s10142-008-0089-4.
63. Walter, S., Kahla, A., Arunachalam, C., Perochon, A., Khan, M. R., Scofield, S. R., et al. (2015). A wheat ABC transporter contributes to both grain formation and mycotoxin tolerance. J. Exp. Bot. 66, 2583-2593. doi: 10. 1093/jxb/erv048.
64. Wang, T., and Wu, M. (2006). An ATP-binding cassette transporter related to yeast vacuolar ScYCF1 is important for Cd sequestration in Chlamydomonas reinhardtii. Plant Cell Environ. 10, 1901-1912. doi: 10. 1111/j. 1365-3040. 2006. 01566. x.
65. Wu, L., Guan, Y., Wu, Z., Yang, K., Lv, J., Converse, R., et al. (2014). OsABCG15 encodes a membrane protein that plays an important role in anther cuticle and pollen exine formation in rice. Plant Cell Rep. 11, 1881-1899. doi: 10. 1007/s00299-014-1666-8.
66. Xu, X. H., Zhao, H. J., Liu, Q. L., Frank, T., Engel, K. H., An, G., et al. (2009). Mutations of the multi-drug resistance associated protein ABC transporter gene 5 result in reduction of phytic acid in rice seeds. Theor. Appl. Genet. 119, 75-83. doi: 10. 1007/s00122-009-1018-1.
67. Zhang, R., Zhu, J., Cao, H. Z., An, Y. R., Huang, J. J., Chen, X. H., et al. (2013). Molecular cloning and expression analysis of PDR1-like gene in ginseng subjected to salt and cold stresses or hormonal treatment. Plant Physiol. Biochem. 71, 203-211. doi: 10. 1016/j. plaphy. 2013. 07. 011.