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Wheat TaVIT2D restores phenotype and mediates iron homeostasis during growth of Arabidopsis thaliana in iron-deficient conditions

  • Raja Jeet
  • Sudhir P. Singh
  • Siddharth Tiwari
  • Promila Pathak
Original Article
  • 32 Downloads

Abstract

Iron (Fe) uptake is a highly regulated process in plants. In cereals, like wheat and rice, dietary Fe concentration in seeds is very low because it is primarily localized as iron-phytate in vacuoles in aleurone layer. Fe transport into vacuoles and vacuolar sequestration are mediated by Vacuolar Iron Transporter (VIT) genes. In wheat seed, TaVIT2D was expressed at higher level in aleurone (removed as bran during milling) as compared to endosperm (makes dietary flour). The constitutive expression of VIT2D of wheat in the vit1 mutant of Arabidopsis thaliana increased Fe accumulation in the root, leaf, and seed during growth in low Fe medium. Expression of genes related to metal uptake and intercellular transport were induced in the complementation lines. The interaction between the vacuolar Fe sequestration and its long-distance transport may be important to address iron biofortification of cereal grains.

Keywords

Iron transport Metal accumulation Fe-homeostasis TaVIT2D vit1 mutant Wheat 

Notes

Acknowledgements

The authors thank Executive Director, National Agri-Food Biotechnology Institute (Department of Biotechnology) for facilitating the research. Fellowship for RJ was supported by Indian Council of Medical Research (ICMR), India. We acknowledge Sébastien Thomine, CNRS, Institute of Integrative Biology of the Cell, France, for sharing the protocol for chlorophyll estimation.

Author contribution statement

SPS and RJ designed the experiments. RJ performed all the experiments. RJ, PP and SPS analyzed the data and wrote the manuscript. PP and ST facilitated the experiments. All authors have read and approved the manuscript.

Compliance with ethical standards

Conflict of interest

All the authors declare no competing financial interest.

Supplementary material

40502_2018_426_MOESM1_ESM.docx (287 kb)
Supplementary material 1 (DOCX 287 kb)
40502_2018_426_MOESM2_ESM.docx (22 kb)
Supplementary material 2 (DOCX 23 kb)

References

  1. Bode, H. P., Dumschat, M., Garotti, S., & Fuhrmann, G. F. (1995). Iron sequestration by the yeast vacuole. A study with vacuolar mutants of Saccharomyces cerevisiae. European Journal of Biochemistry, 228(2), 337–343.  https://doi.org/10.1111/j.1432-1033.1995.0337n.x.CrossRefGoogle Scholar
  2. Brumbarova, T., Bauer, P., & Ivanov, R. (2015). Molecular mechanisms governing Arabidopsis iron uptake. Trends in Plant Science, 20(2), 124–133.  https://doi.org/10.1016/j.tplants.2014.11.004.CrossRefGoogle Scholar
  3. Clemens, S., Deinlein, U., Ahmadi, H., Höreth, S., & Uraguchi, S. (2013). Nicotianamine is a major player in plant Zn homeostasis. BioMetals, 26(4), 623–632.  https://doi.org/10.1007/s10534-013-9643-1.CrossRefGoogle Scholar
  4. Clough, S. J., & Bent, A. F. (1998). Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal, 16(6), 735–743.  https://doi.org/10.1046/j.1365-313x.1998.00343.x.CrossRefGoogle Scholar
  5. Colangelo, E. P., & Guerinot, M. L. (2004). The essential basic helix-loop-helix protein FIT1 is required for the iron deficiency response. The Plant Cell, 16(12), 3400–3412.  https://doi.org/10.1105/tpc.104.024315.CrossRefPubMedCentralPubMedGoogle Scholar
  6. Cong, L., Wang, C., Chen, L., Liu, H., Yang, G., & He, G. (2009). Expression of Phytoene Synthase1 and Carotene Desaturase CRTI genes result in an increase in the total carotenoids content in transgenic elite wheat (Triticum aestivum L.). Journal of Agricultural and Food Chemistry, 57(18), 8652–8660.  https://doi.org/10.1021/jf9012218.CrossRefGoogle Scholar
  7. Connorton, M. J., Jones, R. E., Rodríguez-Ramiro, I., Fairweather-Tait, S., Uauy, C., & Balk, J. (2017). Wheat vacuolar iron transporter TaVIT2 transports Fe and Mn and is effective for biofortification. Plant Physiology, 174(4), 2434–2444.  https://doi.org/10.1104/pp.17.00672.CrossRefPubMedCentralPubMedGoogle Scholar
  8. Conte, S. S., Chu, H. H., Chan-Rodriguez, D., Punshon, T., Vasques, K. A., Salt, D. E., et al. (2013). Arabidopsis thaliana Yellow Stripe1-Like4 and Yellow Stripe1-Like6 localize to internal membranes and are involved in metal ion homeostasis. Frontiers in Plant Science, 4, 283.  https://doi.org/10.3389/fpls.2013.00283.CrossRefPubMedCentralPubMedGoogle Scholar
  9. Curie, C., Cassin, G., Couch, D., Divol, F., Higuchi, K., Le Jean, M., et al. (2009). Metal movement within the plant: contribution of nicotianamine and Yellow Stripe1-Like transporters. Annals of Botany, 103(1), 1–11.  https://doi.org/10.1093/aob/mcn207.CrossRefGoogle Scholar
  10. Curie, C., Panaviene, Z., Loulergue, C., Dellaporta, S. L., Briat, J. F., & Walker, L. E. (2001). Maize Yellow Stripe1 encodes a membrane protein directly involved in Fe(III) uptake. Nature, 409(6818), 346–349.  https://doi.org/10.1038/35053080.CrossRefGoogle Scholar
  11. Divol, F., Couch, D., Conéjéro, G., Roschzttardtz, H., Mari, S., & Curie, C. (2013). The Arabidopsis Yellow Stripe Like4 and 6 transporters control iron release from the chloroplast. The Plant Cell, 25(3), 1040–1055.  https://doi.org/10.1105/tpc.112.107672.CrossRefPubMedCentralPubMedGoogle Scholar
  12. Evers, T., & Millar, S. (2002). Cereal grain structure and development: some implications for quality. Journal of Cereal Science, 36(3), 261–284.  https://doi.org/10.1006/jcrs.2002.0435.CrossRefGoogle Scholar
  13. Gollhofer, J., Timofeev, R., Lan, P., Schmidt, W., & Buckhout, T. J. (2014). Vacuolar-Iron-Transporter1-Like proteins mediate iron homeostasis in Arabidopsis. PLoSONE, 9(10), e110468.  https://doi.org/10.1371/journal.pone.0110468.CrossRefGoogle Scholar
  14. Haas, D. J., Beard, L. J., Murray-Kolb, E. L., Del Mundo, M. A., Felix, A., & Gregorio, G. B. (2005). Iron-biofortified rice improves the iron stores of nonanemic Filipino women. Journal of Nutrition, 135(12), 2823–2830.  https://doi.org/10.1093/jn/135.12.2823.CrossRefGoogle Scholar
  15. Hefferon, K. L. (2015). Nutritionally enhanced food crops; progress and perspectives. International Journal of Molecular Sciences, 16(2), 3895–3914.  https://doi.org/10.3390/ijms16023895.CrossRefPubMedCentralPubMedGoogle Scholar
  16. Hindt, M. N., & Guerinot, M. L. (2012). Getting a sense for signals: regulation of the plant iron deficiency response. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, 1823(9), 1521–1530.  https://doi.org/10.1016/j.bbamcr.2012.03.010.CrossRefGoogle Scholar
  17. Hu, B., Jin, J., Guo, A. Y., Zhang, H., Luo, J., & Gao, G. (2015). GSDS 2.0: An upgraded gene feature visualization server. Bioinformatics, 31(8), 1296–1297.  https://doi.org/10.1093/bioinformatics/btu817.CrossRefGoogle Scholar
  18. Ivanov, R., Brumbarova, T., & Bauer, P. (2012). Fitting into the harsh reality: regulation of iron-deficiency responses in dicotyledonous plants. Molecular Plant, 5(1), 27–42.  https://doi.org/10.1093/mp/ssr065.CrossRefGoogle Scholar
  19. Jakoby, M., Wang, H. Y., Reidt, W., Weisshaar, B., & Bauer, P. (2004). FRU (BHLH029) is required for induction of iron mobilization genes in Arabidopsis thaliana. FEBS Letters, 577(3), 528–534.  https://doi.org/10.1016/j.febslet.2004.10.062.CrossRefGoogle Scholar
  20. Kim, S. A., Punshon, T., Lanzirotti, A., Li, L., Alonso, J. M., Ecker, J. R., et al. (2006). Localization of iron in Arabidopsis seed requires the vacuolar membrane transporter VIT1. Science, 314(5803), 1295–1298.  https://doi.org/10.1126/science.1132563.CrossRefGoogle Scholar
  21. Klatte, M., Schuler, M., Wirtz, M., Fink-Straube, C., Hell, R., & Bauer, P. (2009). The analysis of Arabidopsis nicotianamine synthase mutants reveals functions for nicotianamine in seed iron loading and iron deficiency responses. Plant Physiology, 150(1), 257–271.  https://doi.org/10.1104/pp.109.136374.CrossRefPubMedCentralPubMedGoogle Scholar
  22. Labarbuta, P., Duckett, K., Botting, H. C., Chahrour, O., Malone, J., Dalton, P. J., et al. (2017). Recombinant vacuolar iron transporter family homologue PfVIT from human malaria-causing Plasmodium falciparum is a Fe2+/H+ exchanger. Scientific Reports, 7, 42850.  https://doi.org/10.1038/srep42850.CrossRefPubMedCentralPubMedGoogle Scholar
  23. Lanquar, V., Lelièvre, F., Bolte, S., Hamès, C., Alcon, C., Neumann, D., et al. (2005). Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. The EMBO Journal, 24(23), 4041–4051.  https://doi.org/10.1038/sj.emboj.7600864.CrossRefPubMedCentralPubMedGoogle Scholar
  24. Lanquar, V., Ramos, M. S., Lelièvre, F., Barbier-Brygoo, H., Krieger-Liszkay, A., Krämer, U., et al. (2010). Export of vacuolar manganese by AtNRAMP3 and AtNRAMP4 is required for optimal photosynthesis and growth under manganese deficiency. Plant Physiology, 152(4), 1986–1999.  https://doi.org/10.1104/pp.109.150946.CrossRefPubMedCentralPubMedGoogle Scholar
  25. Legay, S., Guignard, C., Ziebel, J., & Evers, D. (2012). Iron uptake and homeostasis related genes in potato cultivated in vitro under iron deficiency and overload. Plant Physiology and Biochemistry, 60, 180–189.  https://doi.org/10.1016/j.plaphy.2012.08.003.CrossRefGoogle Scholar
  26. Livak, K. J., & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods, 25(4), 402–408.  https://doi.org/10.1006/meth.2001.1262 CrossRefPubMedCentralPubMedGoogle Scholar
  27. Marschner, H. (1995). Mineral nutrition of higher plants (2nd ed.). London: Academic Press.  https://doi.org/10.1016/B978-0-12-473542-2.X5000-7.CrossRefGoogle Scholar
  28. Mary, V., Schnell Ramos, M., Gillet, C., Socha, A. L., Giraudat, J., Agorio, A., et al. (2015). Bypassing iron storage in endodermal vacuoles rescues the iron mobilization defect in the natural resistance associated-macrophage protein3natural resistance associated-macrophage protein4 double mutant. Plant Physiology, 169(1), 748–759.  https://doi.org/10.1104/pp.15.00380.CrossRefPubMedCentralPubMedGoogle Scholar
  29. Momonoi, K., Yoshida, K., Mano, S., Takahashi, H., Nakamori, C., Shoji, K., et al. (2009). A vacuolar iron transporter in tulip, TgVIT1, is responsible for blue coloration in petal cells through iron accumulation. The Plant Journal, 59(3), 437–444.  https://doi.org/10.1111/j.1365-313X.2009.03879.x.CrossRefGoogle Scholar
  30. Morrissey, J., & Guerinot, L. M. (2009). Iron uptake and transport in plants: the good, the bad, and the ionome. Chemical Reviews, 109(10), 4553–4567.  https://doi.org/10.1021/cr900112r.CrossRefPubMedCentralPubMedGoogle Scholar
  31. Murashige, T., & Skoog, F. (1962). A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiologia Plantarum, 15, 473–497.  https://doi.org/10.1111/j.1399-3054.1962.tb08052.x.CrossRefGoogle Scholar
  32. Narayanan, N., Beyene, G., Chauhan, D. R., Gaitán-Solis, E., Grusak, A. M., Taylor, N., et al. (2015). Overexpression of Arabidopsis VIT1 increases accumulation of iron in cassava roots and stems. Plant Science, 240, 170–181.  https://doi.org/10.1016/j.plantsci.2015.09.007.CrossRefGoogle Scholar
  33. Nestel, P., Bouis, H. E., Meenakshi, J. V., & Pfeiffer, W. (2006). Biofortification of staple food crops. Journal of Nutrition, 136(4), 1064–1067.  https://doi.org/10.1093/jn/136.4.1064.CrossRefGoogle Scholar
  34. Nozoye, T., Nagasaka, S., Kobayashi, T., Takahashi, M., Sato, Y., Sato, Y., et al. (2011). Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants. Journal of Biological Chemistry, 286(7), 5446–5454.  https://doi.org/10.1074/jbc.M110.180026.CrossRefGoogle Scholar
  35. Pan, H., Wang, Y., Zha, Q., Yuan, M., Yin, L., Wu, T., et al. (2015). Iron deficiency stress can induce MxNRAMP1 protein endocytosis in M. xiaojinensis. Gene, 567(2), 225–234.  https://doi.org/10.1016/j.gene.2015.05.002.CrossRefGoogle Scholar
  36. Pearce, S., Tabbita, F., Cantu, D., Buffalo, V., Avni, R., Vazquez-Gross, H., et al. (2014). Regulation of Zn and Fe transporters by the GPC1 gene during early wheat monocarpic senescence. BMC Plant Biology, 14, 368.  https://doi.org/10.1186/s12870-014-0368-2.CrossRefPubMedCentralPubMedGoogle Scholar
  37. Peng, S. J., & Gong, M. J. (2014). Vacuolar sequestration capacity and long-distance metal transport in plants. Frontiers in Plant Science, 5, 19.  https://doi.org/10.3389/fpls.2014.00019.CrossRefPubMedCentralPubMedGoogle Scholar
  38. Porra, J. R., Thompson, A. W., & Kriedmann, E. P. (1989). Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 975(1989), 384–394.  https://doi.org/10.1016/S0005-2728(89)80347-0.CrossRefGoogle Scholar
  39. Raguzzi, F., Lesuisse, E., & Crichton, R. R. (1988). Iron storage in Saccharomyces cerevisiae. FEBS Letters, 231(1), 253–258.  https://doi.org/10.1016/0014-5793(88)80742-7.CrossRefGoogle Scholar
  40. Roschzttardtz, H., Conéjéro, G., Curie, C., & Mari, S. (2009). Identification of the endodermal vacuole as the iron storage compartment in the Arabidopsis embryo. Plant Physiology, 151(3), 1329–1338.  https://doi.org/10.1104/pp.109.144444.CrossRefPubMedCentralPubMedGoogle Scholar
  41. Schuler, M., & Bauer, P. (2011). Heavy metals need assistance: the contribution of nicotianamine to metal circulation throughout the plant and the Arabidopsis NAS gene family. Frontiers in Plant Science, 2, 69.  https://doi.org/10.3389/fpls.2011.00069.CrossRefPubMedCentralPubMedGoogle Scholar
  42. Singh, S. P., Jeet, R., Kumar, J., Shukla, V., Srivastava, R., Mantri, S. S., et al. (2014a). Comparative transcriptional profiling of two wheat genotypes, with contrasting levels of minerals in grains, shows expression differences during grain filling. PLoSOne, 9(11), e111718.  https://doi.org/10.1371/journal.pone.0111718.CrossRefGoogle Scholar
  43. Singh, S. P., Vogel-Mikuš, K., Arčon, I., Vavpetič, P., Jeromel, L., Pelicon, P., et al. (2013). Pattern of iron distribution in maternal and filial tissues in wheat grains with contrasting levels of iron. Journal of Experimental Botany, 64(11), 3249–3260.  https://doi.org/10.1093/jxb/ert160.CrossRefPubMedCentralPubMedGoogle Scholar
  44. Singh, S. P., Vogel-Mikuš, K., Vavpetič, P., Jeromel, L., Pelicon, P., Kumar, J., et al. (2014b). Spatial X-ray fluorescence micro-imaging of minerals in grain tissues of wheat and related genotypes. Planta, 240(2), 277–289.  https://doi.org/10.1007/s00425-014-2084-4.CrossRefGoogle Scholar
  45. Slavic, K., Krishna, S., Lahree, A., Bouyer, G., Hanson, K. K., Vera, I., et al. (2016). A vacuolar iron-transporter homologue acts as a detoxifier in Plasmodium. Nature Communications, 7, 10403.  https://doi.org/10.1038/ncomms10403.CrossRefPubMedCentralPubMedGoogle Scholar
  46. Stephan, U. W., & Scholz, G. (1993). Nicotianamine: mediator of transport of iron and heavy metals in the phloem? Physiologia Plantarum, 88(3), 522–529.  https://doi.org/10.1111/j.1399-3054.1993.tb01367.x.CrossRefGoogle Scholar
  47. Vert, A. G., Briat, F. J., & Curie, C. (2003). Dual regulation of the Arabidopsis high-affinity root iron uptake system by local and long-distance signals. Plant Physiology, 132(2), 132796–132804.  https://doi.org/10.1104/pp.102.016089.CrossRefGoogle Scholar
  48. Vert, G., Grotz, N., Dedaldechamp, F., Gaymard, F., Guerinot, M. L., Briat, J. F., et al. (2002). IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. The Plant Cell, 14(6), 1223–1233.  https://doi.org/10.1105/tpc.001388.CrossRefPubMedCentralPubMedGoogle Scholar
  49. von Wirén, N., Klair, S., Bansal, S., Briat, J. F., Khodr, H., Shioiri, T., et al. (1999). Nicotianamine chelates both Fe(III) and Fe(II). Implications for metal transport in plants. Plant Physiology, 119(3), 1107–1114.  https://doi.org/10.1104/pp.119.3.1107.CrossRefGoogle Scholar
  50. Wan, Y., Poole, R. L., Huttly, A. K., Toscano-Underwood, C., Feeney, K., Welham, S., et al. (2008). Transcriptome analysis of grain development in hexaploid wheat. BMC Genomics, 9, 121.  https://doi.org/10.1186/1471-2164-9-121.CrossRefPubMedCentralPubMedGoogle Scholar
  51. Welsch, R., Arango, J., Bar, C., Salazar, B., Al-Babili, S., Beltrán, J., et al. (2010). Provitamin A accumulation in cassava (Manihot esculenta) roots driven by a single nucleotide polymorphism in a Phytoene Synthase gene. The Plant Cell, 22(10), 3348–3356.  https://doi.org/10.1105/tpc.110.077560.CrossRefPubMedCentralPubMedGoogle Scholar
  52. Yoshida, K., & Negishi, T. (2013). The identification of a vacuolar iron transporter involved in the blue coloration of cornflower petals. Phytochemistry, 94, 60–67.  https://doi.org/10.1016/j.phytochem.2013.04.017.CrossRefGoogle Scholar
  53. Yuan, Y., Wu, H., Wang, N., Li, J., Zhao, W., Du, J., et al. (2008). FIT interacts with AtbHLH38 and AtbHLH39 in regulating iron uptake gene expression for iron homeostasis in Arabidopsis. Cell Research, 18(3), 385–397.  https://doi.org/10.1038/cr.2008.26.CrossRefGoogle Scholar
  54. Zhang, Y., Xu, Y. H., Yi, H. Y., & Gong, J. M. (2012). Vacuolar membrane transporters OsVIT1 and OsVIT2 modulate iron translocation between flag leaves and seeds in rice. The Plant Journal, 72, 400–410.  https://doi.org/10.1111/j.1365-313X.2012.05088.x.CrossRefGoogle Scholar

Copyright information

© Indian Society for Plant Physiology 2018

Authors and Affiliations

  • Raja Jeet
    • 1
    • 3
  • Sudhir P. Singh
    • 1
    • 2
  • Siddharth Tiwari
    • 1
  • Promila Pathak
    • 3
  1. 1.National Agri-Food Biotechnology InstituteMohaliIndia
  2. 2.Center of Innovative and Applied BioprocessingMohaliIndia
  3. 3.Department of BotanyPanjab UniversityChandigarhIndia

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