Advertisement

Biologia Plantarum

, Volume 61, Issue 2, pp 293–304 | Cite as

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

  • X. Wang
  • C. Wang
  • H. Sheng
  • Y. Wang
  • J. Zeng
  • H. Kang
  • X. Fan
  • L. Sha
  • H. Zhang
  • Y. ZhouEmail author
Original Paper

Abstract

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.

Additional key words

cadmium copper gene expression iron magnesium nickel zinc 

Abbreviations

ABC

ATP-binding cassette

ACT

actin

DPW

dwarf polish wheat

ORFs

open reading frames

qPCR

quantitative PCR

WC

water content

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Supplementary material

10535_2016_697_MOESM1_ESM.pdf (2.2 mb)
Supplementary material, approximately 2290 KB.

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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefPubMedPubMedCentralGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  7. Dean, M., Hamon, Y., Chimini, G.: The human ATP-binding cassette (ABC) transporter superfamily. — J Lipid Res. 42: 1007–1017, 2001.PubMedGoogle Scholar
  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.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Edgar, R.C.: MUSCLE: multiple sequence alignment with high accuracy and high throughput. — Nucl. Acids Res. 32: 1792–1797, 2004.CrossRefPubMedPubMedCentralGoogle Scholar
  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.CrossRefPubMedPubMedCentralGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  15. Higgins, C.F.: ABC transporters: from microorganisms to man. — Annu. Rev. Cell Biol. 8: 67–113, 1992.CrossRefPubMedGoogle Scholar
  16. Jarup, L.: Hazards of heavy metal contamination. — Brit. med. Bull. 68: 167–182, 2003.CrossRefPubMedGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefPubMedPubMedCentralGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefGoogle Scholar
  22. Kretzschmar, T., Burla, B., Lee, Y., Martinoia, E., Nagy, R. Functions of ABC transporters in plants. - Essays Biochem. 50: 145–160, 2011.CrossRefPubMedGoogle Scholar
  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.CrossRefPubMedPubMedCentralGoogle Scholar
  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.CrossRefPubMedPubMedCentralGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefGoogle Scholar
  29. Michalcová, V., Dušinský, R., Sabo, M., Beyroutiová, M.A., Hauptvogel, P., Ivaničová, Z., Švec, M.: Taxonomical classification and origin of Kamut® wheat. — Plant Syst. Evol. 300: 1749–1757, 2014.CrossRefGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  37. Rajendra, P., Andre, G.: Yeast ATP-binding cassette transporters conferring multidrug resistance. — Annu. Rev. Microbiol. 66: 39–63, 2012.CrossRefGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefPubMedPubMedCentralGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefPubMedPubMedCentralGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefPubMedPubMedCentralGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.PubMedPubMedCentralGoogle Scholar
  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.CrossRefPubMedPubMedCentralGoogle Scholar
  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.PubMedPubMedCentralGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.Google Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© The Institute of Experimental Botany 2017

Authors and Affiliations

  • X. Wang
    • 1
  • C. Wang
    • 1
  • H. Sheng
    • 1
  • Y. Wang
    • 1
  • J. Zeng
    • 2
  • H. Kang
    • 1
  • X. Fan
    • 1
  • L. Sha
    • 1
  • H. Zhang
    • 1
  • Y. Zhou
    • 1
    Email author
  1. 1.Triticeae Research InstituteSichuan Agricultural UniversitySichuan, WenjiangP.R. China
  2. 2.College of ResourcesSichuan Agricultural UniversityWenjiang, SichuanP.R. China

Personalised recommendations