biologia plantarum

International journal on Plant Life established by Bohumil Němec in 1959

Biologia plantarum 61:293-304, 2017 | DOI: 10.1007/s10535-016-0697-0

Transcriptome-wide identification and expression analyses of ABC transporters in dwarf polish wheat under metal stresses

X. Wang1, C. Wang1, H. Sheng1, Y. Wang1, J. Zeng2, H. Kang1, X. Fan1, L. Sha1, H. Zhang1, Y. Zhou1,*
1 Triticeae Research Institute, Sichuan Agricultural University, Sichuan, Wenjiang, P.R. China
2 College of Resources, Sichuan Agricultural University, Wenjiang, Sichuan, P.R. China

ABC transporters, which comprise one of the largest protein families, are involved in maintaining osmotic homeostasis, nutrient uptake, pathogen resistance, and metal tolerance. In this study, 30 ABC genes in dwarf polish wheat were characterized and classified into seven subfamilies (ABCA - ABCG). Among them, 24 ABC transporters were newly found in wheat. The expressions of 13 ABC genes in roots and leaves under six metal stresses were also analyzed. All these genes were differentially regulated by Cd (except ABCE2, ABCF4, and ABCF6 in roots), suggesting that these genes participate in Cd transport, sequestration, or uptake. These genes were also differentially regulated by other metals including Cu, Mg, Zn, Fe, and Ni. Results suggest that the expressions of ABC transporters in dwarf polish wheat played important roles in metal transport and detoxification.

Keywords: cadmium; copper; gene expression; iron; magnesium; nickel; zinc
Subjects: transcriptome analysis; ABC transporters; cadmium; copper; iron; magnesium; nickel; zinc; gene expression; dwarf Polish wheat

Received: January 31, 2016; Revised: April 25, 2016; Accepted: May 3, 2016; Published: June 1, 2017  Show citation

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Wang, X., Wang, C., Sheng, H., Wang, Y., Zeng, J., Kang, H., ... Zhou, Y. (2017). Transcriptome-wide identification and expression analyses of ABC transporters in dwarf polish wheat under metal stresses. Biologia plantarum61(2), 293-304. doi: 10.1007/s10535-016-0697-0
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References

  1. Ait, A.N., Bernal, M.P., Ater, M.: Tolerance and bioaccumulation of cadmium by Phragmites australis grown in the presence of elevated concentrations of cadmium, copper, and zinc. - Aquat. Bot. 80: 163-176, 2004. Go to original source...
  2. Ames, G.F., Mimura, C.S, Shyamala, V.: Bacterial periplasmicpermeases belong to a family of transport proteins operating from Escherichia coli to human: traffic ATPases. - FEMS Microbiol. 6: 429-446, 1990. Go to original source...
  3. Bhati, K.K., Sharma, S., Aggarwal, S., Kaur, M., Shukla, V., Kaur, J., Mantri, S., Pandey, A.K.: Genome-wide identification and expression characterization of ABCC-MRP transporters in hexaploid wheat. - Front. Plant Sci. 6: 488-502, 2015. Go to original source...
  4. Blattner, R.F., Plunkett, G., Bloch, C.A., Perna, N.T., Burland, V., Riley, M., Collado-Vides, J., Glasner, J.D., Rode, C.K., Mayhew, G.F., Gregor, J., Davis, N.W., Kirkpatrick, H.A., Goeden, M.A., Rose, D.J., Mau, B., Shao, Y.: The complete genome sequence of Escherichia coli K-12. - Science 277: 1453-1474, 1997. Go to original source...
  5. Bovet, L., Eggmann, T., Meylan-Bettex, M., Polier, J., Kammer, P., Marin, E., Feller, U., Marinoia, E.: Transcript levels of AtMRPs after cadmium treatment: induction of AtMRP3. - Plant Cell Environ. 26: 371-381, 2003. Go to original source...
  6. Bovet, L., Feller, U., Martinoia, E.: Possible involvement of plant ABC transporters in cadmium detoxification: a cDNA submicroarray approach. - Environ Int. 31: 263-267, 2005. Go to original source...
  7. Dean, M., Hamon, Y., Chimini, G.: The human ATP-binding cassette (ABC) transporter superfamily. - J Lipid Res. 42: 1007-1017, 2001. Go to original source...
  8. Duan, J., Xia, C., Zhao, G., Jia, J., Kong, X.: Optimizing de novo common wheat transcriptome assembly using short-read RNA-Seq data. - BMC Genomics 13: 392, 2012. Go to original source...
  9. Edgar, R.C.: MUSCLE: multiple sequence alignment with high accuracy and high throughput. - Nucl. Acids Res. 32: 1792-1797, 2004. Go to original source...
  10. Gaillard, S., Jacquet, H., Vavasseur, A., Nathalie, L., Forestier, C.: AtMRP6/AtABC6, 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, 2008. Go to original source...
  11. Grabherr, M.G., Haas, B.J., Yassour, M., Levin, J.Z., Thompson, I.A., Adiconis, X., Fan, L., Raychowdhury, R., Zeng, Q., Chen, Z., Mauceli, E., Hacohen, N., Gnirke, A., Rhind, N., Palma, F., Birren, B.W., Nusbaum, C., Lindblad-Toh, K., Friedman, N., Regev, A.: Full-length transcriptome assembly from RNA-Seq data without a reference genome. - Natur. Biotechnol. 29: 644-652, 2011. Go to original source...
  12. González-Guerrero, M., Benabdellah, K., Valderas, A., Azcón-Aguilar, C., Ferrol, N.: GintABCs encodes a putative ABC transporter of the MRP subfamily induced by Cu, Cd, and oxidative stress in Glomus intraradices. - Mycorrhiza 20: 137-146, 2010. Go to original source...
  13. Hansch, R., Mendel, R.R.: Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl). - Curr. Opin. Plant Biol. 12: 259-266, 2009. Go to original source...
  14. Henikoff, S., Elizabeth, A.G., Pietrokovski, S., Bork, P., Attwood, T.K., Hood, L.: Genome families: the taxonomy of protein paralogs and chimeras. - Science 278: 609-614, 1997. Go to original source...
  15. Higgins, C.F.: ABC transporters: from microorganisms to man. - Annu. Rev. Cell Biol. 8: 67-113, 1992. Go to original source...
  16. Jarup, L.: Hazards of heavy metal contamination. - Brit. med. Bull. 68: 167-182, 2003. Go to original source...
  17. Kim, D.W., Rakwal, R., Agrawal, G.K., Jung, Y.H., Shibato, J., Jwa, N.S., Iwahashi, Y., Iwahashi, H., Kim, D.H., Shim, I.S., Usui, K.: A hydroponic rice seedling culture model system for investigating proteome of salt stress in rice leaf. - Electrophoresis 26: 4521-4539, 2005. Go to original source...
  18. Kim, D,Y., Bovet, L., Kushnir, S., Noh, E.W., Martinoia, E., Lee, Y.: AtATM3 is involved in heavy metal resistance in Arabidopsis. - Plant Physiol. 140: 922-932, 2006. Go to original source...
  19. Kim, D.Y., Bovet, L., Maeshima, M., Martinoia, E., Lee, Y.: The ABC transporter AtPDR8 is a cadmium extrusion pump conferring heavy metal resistance. - Plant J. 50: 207-212, 2007. Go to original source...
  20. Krattinger, S.G., Lagudah, E.S., Spielmeyer, W., Singh, R.P., Huerta-Espino, J., McFadden, H., Bossolini, E., Selter, L.L., Keller, B.: A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. - Science 323: 1360-1363, 2009. Go to original source...
  21. Krattinger, S.G., Lagudah, E.S., Wicker, T., Risk, J.M., Ashton, A.R., Selter, L.L., Matsumoto, T., Keller, B.: Lr34 multipathogen resistance ABC transporter: molecular analysis of homoeologous and orthologous genes in hexaploid wheat and other grass species. - Plant J. 65: 92-403, 2011. Go to original source...
  22. Kretzschmar, T., Burla, B., Lee, Y., Martinoia, E., Nagy, R. Functions of ABC transporters in plants. - Essays Biochem. 50: 145-160, 2011. Go to original source...
  23. Kuromori, T., Miyaji, T., Yabuuchi, H., Shimizu, H., Sugimoto, E., Kamiya, A., Moriyama, Y., Shinozaki, K.: ABC transporter AtABCG25 is involved in abscisic acid transport and responses. - Proc. nat. Acad. Sci. USA 107: 2361-2366, 2010. Go to original source...
  24. Li, Z.S., Lu, Y.P., Zhen, R.G., Szczypka, M., Thiele, D.J., Rea, P.A.: A new pathway for vacuolar cadmium sequestration in Saccharomyces cerevisiae: YCF1-catalyzed transport of bis (glutathionato) cadmium. - Proc. nat. Acad. Sci. USA 94: 42-47, 1997. Go to original source...
  25. Lin, Y.F., Aarts, G.M.: The molecular mechanism of zinc and cadmium stress response in plants. - Cell Mol Life Sci. 69: 3187-3206, 2012. Go to original source...
  26. Livak, K.J., Schmittgen, T.D.: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. - Methods 25: 402-408, 2001. Go to original source...
  27. Martinoia, E., Klein, M., Geisler, M., Bovet, L., Forestier, C., Kolukisaoglu, U., Muller-Rober, B., Schulz, B.: Multifunctionality of plant ABC transporters more than just detoxifiers. - Planta 214: 345-355, 2002. Go to original source...
  28. Mentewab, A., Matheson, K., Adebiyi, M., Robinson, S., Elston, B.: RNA-seq analysis of the effect of kanamycin and the ABC transporter AtWBC19 on Arabidopsis thaliana seedlings reveals changes in metal content. - Plos ONE 9: e109310, 2014. Go to original source...
  29. Michalcová, V., Duąinský, R., Sabo, M., Beyroutiová, M.A., Hauptvogel, P., Ivaničová, Z., ©vec, M.: Taxonomical classification and origin of Kamut® wheat. - Plant Syst. Evol. 300: 1749-1757, 2014. Go to original source...
  30. Moons, A.: Ospdr9, which encodes a PDR-type ABC transporter, is induced by heavy metals, hypoxic stress and redox perturbations in rice roots. - FEBS Lett. 553: 370-376, 2003. Go to original source...
  31. Muhovski, Y., Jacquemin, J.M., Batoko, H.: Identification and differential induction of ABCG transporter genes in wheat cultivars challenged by a deoxynivalenol-producing Fusarium graminearum strain. - Mol. Biol. Rep. 41: 6181-6194, 2014. Go to original source...
  32. Nguyen, V.N.T., Moon, S., Jung, K.H.: Genome-wide expression analysis of rice ABC transporter family across spatiotemporal samples and in response to abiotic stresses. - J. Plant Physiol. 171: 1276-1288, 2014. Go to original source...
  33. Oritz, D.F., Kreppel, L., Spaser, D.M.: Transport of metal-binding peptides by HMT1, a fission yeast ABC-type vacuolar membrane protein. - J. biol. Chem. 270: 4721-4728, 1995. Go to original source...
  34. Pang, K., Li, Y., Liu, M., Meng, Z., Yu, Y.: Inventory and general analysis of the ATP-binding cassette (ABC) gene superfamily in maize (Zea mays L.). - Gene 526: 411-428, 2013. Go to original source...
  35. Park, J., Song, W.Y., Ko, D., Eom, Y., Hansen, T.H., Schiller, M., Lee, T.G., Martinoia, E., Lee, Y.: The phytochelatin transporters AtABCC1 and AtABCC2 mediate tolerance to cadmium and mercury. - Plant J. 69: 278-288, 2012. Go to original source...
  36. Prévéral S., Gayet, L., Moldes, C., Hoffmann, J., Mounicou, S., Gruet, A., Reynaud, F., Lobinski, R., Verbavatz, J.M., Vavasseur, A., Forestier, C.: A common highly conserved cadmium detoxification mechanism from bacteria to humans. - J. biol. Chem. 284: 4936-4943, 2009. Go to original source...
  37. Rajendra, P., Andre, G.: Yeast ATP-binding cassette transporters conferring multidrug resistance. - Annu. Rev. Microbiol. 66: 39-63, 2012. Go to original source...
  38. Remy, L., Carrière, M., Derré-Bobillot, A., Martini, C., Sanguinetti, M., Borezée-Durant, E.: The Staphylococcus aureus Opp1 ABC transporter imports nickel and cobalt in zinc-depleted conditions and contributes to virulence. - Mol. Microbiol. 87: 730-743, 2013. Go to original source...
  39. Rogers, B., Decottignies, A., Kolaczkowski, M., Carvajal, E., Balzi, E., Goffeau, A.: The pleiotropic drug ABC transporters from Saccharomyces cerecisiae. - J. mol. microbiol. Biotechnol. 3: 207-214, 2001.
  40. Sanchez-Fernandez, R., Davies, E.T.G., Coleman, J.O.D., Rea, P.A.: The Arabidopsis thaliana ABC protein superfamily: a complete inventory. - J. biol. Chem. 276: 30231-30244, 2001. Go to original source...
  41. Schreiber, A.W., Hayden, M.J., Forrest, K.L., Kong, S., Langridge, P., Baumann, U.: Transcriptome-scale homoeolog-specific transcript assemblies of bread wheat. - BMC Genomics 13: 492, 2012. Go to original source...
  42. Shang, Y., Xiao, J., Ma, L., Wang, H., Qi, Z., Chen, P., Liu, D., Wang, X.: Characterization of a PDR type ABC transporter gene from wheat (Triticum aestivum L.). - Chin. sci. Bull. 54: 3249-3257, 2009. Go to original source...
  43. Song, W.Y., Park, J., Mendoza-Cozatl, D.G., Suter-Grotemeyer, M., Shim, D., Hortensteiner, S., Geisler, M., Weder, B., Rea, P.A., Rentsch, D., Schroeder, J.I., Lee, Y., Martinoia, E.: Arsenic tolerance in Arabidopsis is mediated by two ABCCtype phytochelatin transporters. - Proc. nat. Acad. Sci. USA 107: 21187-21192, 2010. Go to original source...
  44. Sooksa-Nguan, T., Yakubov, B., Kozlovskyy, V.I., Barkume, C.M., Howe, K.J., Thannhauser, T.W., Rutzke, M.A., Hart J.J., Kochian, L.V., Rea, P.A., Vatamaniuk, O.K.: Drosophila ABC transporter, DmHMT-1, confers tolerance to cadmium. DmHMT-1 and its yeast homolog, SpHMT-1, are not essential for vacuolar phytochelatin sequestration. - J. biol. Chem. 284: 354-362, 2009. Go to original source...
  45. Takayuki, S., Bunichi, E., Hideaki, M.: A gene encoding multidrug resistance (MDR)-like protein is induced by aluminum and inhibitors of calcium flux in wheat. - Plant Cell Physiol. 43: 177-185, 2002. Go to original source...
  46. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., Kumar, S.: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. - Mol. Biol. Evol. 28: 2731-2739, 2011. Go to original source...
  47. Theodoulou, F.L., Clark, I.M., He, X.L., Pallett, K.E., Cole, D.J., Hallahan, D.L.: Co-induction of glutathione-S-transferases and multidrug resistance associated protein by xenobiotics in wheat. - Pest Manage. Sci. 59: 202-214, 2003. Go to original source...
  48. Vatamaniuk, O.K., Bucher, E.A., Sundaram, M.V., Rea, P.A.: CeHMT-1, a putative phytochelatin transporter, is required for cadmium tolerance in Caenorhabditis elegans. - J. biol. Chem. 280: 23684-23690, 2005. Go to original source...
  49. Verrier, P.J., Bird, D., Burla, B., Dassa, E., Forestier, C., Geisler, M., Klein, M., Kolukisaoglu, Ü., Lee, Y., Martinoia, E.: Plant ABC proteins: a unified nomenclature and updated inventory. - Trends Plant Sci. 13: 151-159, 2008. Go to original source...
  50. Walker, J.E., Saraste, M., Runswick, M.J., Gay, N.J.: Distantly related sequences in the α-and β -subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. - EMBO J. 1: 945-951, 1982. Go to original source...
  51. Walter, S., Kahla, A., Arunachalam, C., Perochon, A., Khan, M.R., Scofield, S.R., Doohan, F.M.: A wheat ABC transporter contributes to both grain formation and mycotoxin tolerance. - J. exp. Bot. 66: 2583-2593, 2015. Go to original source...
  52. Wang, Y., Wang, C., Wang, X., Peng, F., Wang, R., Jiang, Y., Zeng, J., Fan, X., Kang, H., Sha, L., Zhang, H., Xiao, X., Zhou, Y.: De novo sequencing and characterization of the transcriptome of dwarf polish wheat (Triticeae polonicum L.). - Int. J. Genomics 2016: 5781412, 2016. Go to original source...
  53. Wang, Y., Wang, C., Zhang, H., Yue, Z., Liu, X., Ji, W.: Genetic analysis of wheat (Triticum aestivum L.) and related species with SSR markers. - Genet. Resour. Crop Evol. 60: 1105-1117, 2013. Go to original source...
  54. Wang, Y., Wang, X., Gu, M., Kang, H., Zeng, J., Fan, X., Sha, L., Zhang, H., Yu, K., Zhou, Y.: Cloning and characterization of four novel SnRK2 genes from Triticum polonicum. - Biol. Plant. 59: 211-219, 2015. Go to original source...
  55. Wang, Y., Yu, K., Vaino, P., Shi, C., Zhou, Y.: Selection of reference genes for normalization of qRT-PCR analysis of differentially expressed genes in soybean exposed to cadmium. - Mol. Biol. Rep. 39: 1585-1594, 2012. Go to original source...
  56. Waraich, E.A., Ahmad, R., Ashraf, M.Y., Saifullah, Ahmad, M.: Improving agricultural water use efficiency by nutrient management in crop plants. - Acta agr. scand. 61: 291-304, 2011. Go to original source...
  57. Wiwart, M., Suchowilska, E., Kandler, W., Sulyok, M., Groenwald, P., Krska, R.: Can Polish wheat (Triticum polonicum L.) be an interesting gene source for breeding wheat cultivars with increased resistance to Fusarium head blight? - Genet Resour. Crop Evol. 60: 2359-2373, 2013. Go to original source...
  58. Zolman, B.K., Silva, I.D., Bartel, B.: The Arabidopsis pxa1 mutant is defective in an ATP-binding cassette transporter-like protein required for peroxisomal fatty acid β-oxidation. - Plant Physiol. 127: 1266-1278, 2001. Go to original source...