Evolution, and functional analysis of Natural Resistance-Associated Macrophage proteins (NRAMPs) from Theobroma cacao and their role in cadmium accumulation

Downloads

1. Bozzi, A. T. et al. Conserved methionine dictates substrate preference in Nramp-family divalent metal transporters. Proc Natl Acad Sci 113, 10310–10315 (2016). 2. Bozzi, A. T. et al. Crystal structure and conformational change mechanism of a bacterial Nramp-family divalent metal transporter. Structure 24, 2102–2114 (2016). 3. Chavez, E. et al. Evaluation of soil amendments as a remediation alternative for cadmium-contaminated soils under cacao plantations. Environ Sci Pollut Res 23, 17571–17580 (2016). 4. Yang, Y. et al. Can liming reduce cadmium (Cd) accumulation in rice (Oryza sativa) in slightly acidic soils? A contradictory dynamic equilibrium between Cd uptake capacity of roots and Cd immobilisation in soils. Chemosphere 193, 547–556 (2018). 5. Tang, L. et al. Knockout of OsNramp5 using the CRISPR/Cas9 system produces low Cd-accumulating indica rice without compromising yield. Sci Rep 7, 1–12 (2017). 6. Dix, D. R., Bridgham, J. T., Broderius, M. a., Byersdorfer, C. a. & Eide, D. J. The FET4 gene encodes the low affinity Fe(II) transport protein of Saccharomyces cerevisiae. J Biol Chem 269, 26092–99 (1994). 7. Zhao, H. & Eide, D. The ZRT2 gene encodes the low affinity zinc transporter in Saccharomyces cerevisiae. J Biol Chem 271, 23203–23210 (1996). 8. Thomine, S., Wang, R., Ward, J. M., Crawford, N. M. & Schroeder, J. I. Cadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genes. Proc Natl Acad Sci 97, 4991–4996 (2000). 9. Yang, M. et al. OsNRAMP5 contributes to manganese translocation and distribution in rice shoots. J Exp Bot 65, 4849–4861 (2014). 10. Takahashi, R. et al. The OsNRAMP1 iron transporter is involved in Cd accumulation in rice. J Exp Bot 62, 4843–4850 (2011). 11. Cailliatte, R., Lapeyre, B., Briat, J. F., Mari, S. & Curie, C. The NRAMP6 metal transporter contributes to cadmium toxicity. Biochem J 422, 217–228 (2009). 12. Qin, L. et al. Genome-wide identification and expression analysis of NRAMP family genes in soybean (Glycine Max L.). Front Plant Sci 8, 1–19 (2017). 13. Cannon, S. B., Mitra, A., Baumgarten, A., Young, N. D. & May, G. The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 21, 1–21 (2004). 14. Soltis, D. E., Visger, C. J. & Soltis, P. S. The polyploidy revolution then...and now: Stebbins revisited. Am J Bot 101, 1057–1078 (2014). 15. Bowers, J. L., Chapman, B. A., Rong, J. & Paterson, A. H. Unraveling angiosperms genome evolution by phylogenetic analysis of chromosomal duplications events. Nature 422, 433–438 (2003). 16. Argout, X. et al. The genome of Theobroma cacao. Nat Genet 43, 101–108 (2011). 17. Maser, P. Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol 126, 1646–1667 (2001). 18. Force, A. et al. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151, 1531–1545 (1999). 19. Curie, C., Alonso, J. M., Le Jean, M., Ecker, J. R. & Briat, J. F. Involvement of NRAMP1 from Arabidopsis thaliana in iron transport. Biochem J 347, 749 (2000). 20. Cailliatte, R., Schikora, A., Briat, J. F., Mari, S. & Curie, C. High-affinity manganese uptake by the metal transporter NRAMP1 is essential for Arabidopsis growth in low manganese conditions. Plant Cell 22, 904–917 (2010). 21. Sasaki, A., Yamaji, N., Yokosho, K. & Ma, J. F. Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell 24, 2155–2167 (2012). 22. Gao, H. et al. NRAMP2, a trans-Golgi network-localized manganese transporter, is required for Arabidopsis root growth under manganese deficiency. New Phytol 217, 179–193 (2018). 23. Fujimaki, S. et al. Tracing cadmium from culture to spikelet: Noninvasive imaging and quantitative characterization of absorption, transport, and accumulation of cadmium in an intact rice plant. Plant Physiol 152, 1796–1806 (2010). 24. Boyd, RS. Plant defense using toxic inorganic ions: conceptual models of the defensive enhancement and joint effects hypotheses. Plant Sci 195, 88-95 (2012). 25. Hörger, A.C., Fones, H. N. & Preston, G. M. The current status of the elemental defense hypothesis in relation to pathogens. Front Plant Sci 16, 395 (2013). 26. Poschenrieder, C., Cabot, C., Martos, S., Gallego, B. & Barceló, J. Do toxic ions induce hormesis in plants? Plant Sci 212, 15-25 (2013). 27. Chouhan, S. Verma, S. C. & Thakur, M. Effect of cadmium on biology of tobacco caterpillar Spodoptera litura fabricius (lepidoptera: Noctuidae). Nat Environ Pollut Technol 16, 883-888 (2017). 28. Kazemi-Dinan, A., Thomaschky, S., Stein, R.J., Krämer, U. & Müller, C. Zinc and cadmium hyperaccumulation act as deterrents towards specialist herbivores and impede the performance of a generalist herbivore. New Phytol 202, 628-639 (2014). 29. Li, K. et al. Effects of Cd accumulation on cutworm Spodoptera litura larvae via Cd treated Chinese flowering cabbage Brassica campestris and artificial diets. Chemosphere 200, 151-163 (2018). 30. Plaza, S. et al. Wounding of Arabidopsis halleri leaves enhances cadmium accumulation that acts as a defense against herbivory. Biometals 28, 521-528 (2015). 31. Vlahović, M. et al. Influence of dietary cadmium exposure on fitness traits and its accumulation (with an overview on trace elements) in Lymantria dispar larvae. Comp Biochem Physiol C Toxicol Pharmacol 200, 27-33 (2017). 32. Zhan, H. et al. Effects of Cd2+ exposure on key life history traits and activities of four metabolic enzymes in Helicoverpa armigera (Lepidopteran: Noctuidae). Chem Ecol 33, 325-338 (2018), 33. Oomen, R. J. F. J. et al. Functional characterization of NRAMP3 and NRAMP4 from the metal hyperaccumulator Thlaspi caerulescens. New Phytol 181, 637–650 (2009). 34. Peng, F. et al. Expression of TpNRAMP5, a metal transporter from Polish wheat (Triticum polonicum L.), enhances the accumulation of Cd, Co and Mn in transgenic Arabidopsis plants. Planta 1–12 (2018). 35. Tang, Z. et al. Allelic variation of NtNramp5 associated with cultivar variation in cadmium accumulation in tobacco. Plant Cell Physiol 58, 1583–1593 (2017). 36. Wu, D. et al. The HvNramp5 transporter mediates uptake of cadmium and manganese, but not iron. Plant Physiol 172, 1899–1910 (2016). 37. Ehrnstorfer, I. A., Geertsma, E. R., Pardon, E., Steyaert, J. & Dutzler, R. Crystal structure of a SLC11 (NRAMP) transporter reveals the basis for transition-metal ion transport. Nat Struct Mol Biol 21, 990–996 (2014). 38. Pottier, M. et al. Identification of mutations allowing Natural Resistance Associated Macrophage Proteins (NRAMP) to discriminate against cadmium. Plant J 83, 625–637 (2015). 39. Xia, J., Yamaji, N., Kasai, T. & Ma, J. F. Plasma membrane-localized transporter for aluminum in rice. Proc Natl Acad Sci 107, 18381–18385 (2010). 40. Ishikawa, S. et al. Ion-beam irradiation, gene identification, and marker-assisted breeding in the development of low-cadmium rice. Proc Natl Acad Sci 109, 19166–19171 (2012). 41. Mason, A. B., Allen, K. E. & Slayman, C. W. Effects of C-terminal truncations on trafficking of the yeast plasma membrane H+-ATPase. J Biol Chem 281, 23887–23898 (2006). 42. Edgar, R. C. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004). 43. Kumar, S., Stecher, G. & Tamura, K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol 33, 1870–1874 (2016). 44. Letunic, I. & Bork, P. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 44, W242–W245 (2016). 45 Eide, D. & Guarente, L. Increased dosage of a transcriptional activator gene enhances iron-limited growth of Saccharomyces cerevisiae. J Gen Microbiol 138, 347-354 (1992).