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Comparative understanding of metal hyperaccumulation in plants: a mini-review

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Hyperaccumulator plants are ideal models for investigating the regulatory mechanisms of plant metal homeostasis and environmental adaptation due to their notable traits of metal accumulation and tolerance. These traits may benefit either the biofortification of essential mineral nutrients or the phytoremediation of nonessential toxic metals. A common mechanism by which elevated expression of key genes involved in metal transport or chelation contributes to hyperaccumulation and hypertolerance was proposed mainly from studies examining two Brassicaceae hyperaccumulators, namely Arabidopsis halleri and Noccaea caerulescens (formerly Thlaspi caerulescens). Meanwhile, recent findings regarding systems outside the Brassicaceae hyperaccumulators indicated that functional enhancement of key genes might represent a strategy evolved by hyperaccumulator plants. This review provides a brief outline of metal hyperaccumulation in plants and highlights commonalities and differences among various hyperaccumulators.

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  1. Assunção, A. G. L., da Costa Martins, P., de Folter, S., Voojis, R., Schat, H., & Aarts, M. G. M. (2001). Elevated expression of metal transporter genes in three accessions of the metal hyperaccumulator Thlaspi caerulescens. Plant, Cell and Environment,24(2), 217–226.

  2. Becher, M., Talke, I. N., Krall, L., & Krämer, U. (2004). Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. Plant Journal,37(2), 251–268.

  3. Bernard, C., Roosens, N., Czernic, P., Lebrun, M., & Verbruggen, N. (2004). A novel CPx-ATPase from the cadmium hyperaccumulator Thlaspi caerulescens. FEBS Letters,569(1–3), 140–148.

  4. Chiang, H. C., Lo, J. C., & Yeh, K. C. (2006). Genes associated with heavy metal tolerance and accumulation in Zn/Cd hyperaccumulator Arabidopsis halleri: A genomic survey with cDNA microarray. Environmental Science and Technology,40(21), 6792–6798.

  5. Cornu, J. Y., Deinlein, U., Höreth, S., Braun, M., Schmidt, H., Weber, M., et al. (2015). Contrasting effects of nicotianamine synthase knockdown on zinc and nickel tolerance and accumulation in the zinc/cadmium hyperaccumulator Arabidopsis halleri. New Phytologist,206(2), 738–750.

  6. Cosio, C., DeSantis, L., Frey, B., Diallo, S., & Keller, C. (2005). Distribution of cadmium in leaves of Thlaspi caerulescens. Journal of Experimential Botany,56(412), 765–775.

  7. Courbot, M., Willems, G., Motte, P., Arvidsson, S., Roosens, N., Saumitou-Laprade, P., et al. (2007). A major quantitative trait locus for cadmium tolerance in Arabidopsis halleri colocalizes with HMA4, a gene encoding a heavy metal ATPase. Plant Physiology,144(2), 1052–1065.

  8. Deinlein, U., Weber, M., Schmidt, H., Rensch, S., Trampczynska, A., Hansen, T. H., et al. (2012). Elevated nicotianamine levels in Arabidopsis halleri roots play a key role in zinc hyperaccumulation. Plant Cell,24(2), 708–723.

  9. Desbrosses-Fonrouge, A. G., Voigt, K., Schroder, A., Arrivault, S., Thomine, S., & Krämer, U. (2005). Arabidopsis thaliana MTP1 is a Zn transporter in the vacuolar membrane which mediates Zn detoxification and drives leaf Zn accumulation. FEBS Letters,579(19), 4165–4174.

  10. Dräger, D. B., Desbrosses-Fonrouge, A. G., Krach, C., Chardonnens, A. N., Meyer, R. C., Saumitou-Laprade, P., et al. (2004). Two genes encoding Arabidopsis halleri MTP1 metal transport proteins co-segregate with zinc tolerance and account for high MTP1 transcript levels. Plant Journal,39(3), 425–439.

  11. Ebbs, S. D., Zambrano, M. C., Spiller, S. M., & Newville, M. (2009). Cadmium sorption, influx, and efflux at the mesophyll layer of leaves from ecotypes of the Zn/Cd hyperaccumulator Thlaspi caerulescens. New Phytologist,181(3), 626–636.

  12. Filatov, V., Dowdle, J., Smirnoff, N., Ford-Lloyd, B., Newbury, H. J., & Macnair, M. M. (2006). Comparison of gene expression in segregating families identifies genes and genomic regions involved in a novel adaptation, zinc hyperaccumulation. Molecular Ecology,15(10), 3045–3059.

  13. Gao, J., Sun, L., Yang, X., & Liu, J. X. (2013). Transcriptomic analysis of cadmium Stress response in the heavy metal hyperaccumulator Sedum alfredii hance. PLoS ONE,8(6), e64643.

  14. Gendre, D., Czernic, P., Conéjéro, G., Pianelli, K., Briat, J. F., Lebrun, M., et al. (2007). TcYSL3, a member of the YSL gene family from the hyperaccumulator Thlaspi caerulescens, encodes a nicotianamine-Ni/Fe transporter. Plant Journal,49(1), 1–15.

  15. Gustin, J. L., Loureiro, M. E., Kim, D., Na, G., Tikhonova, M., & Salt, D. E. (2009). MTP1-dependent Zn sequestration into shoot vacuoles suggests dual roles in Zn tolerance and accumulation in Zn-hyperaccumulating plants. Plant Journal.,57(6), 1116–1127.

  16. Hammond, J. P., Bowen, H. C., White, P. J., Mills, V., Pyke, K. A., Baker, A. J., et al. (2006). A comparison of the Thlaspi caerulescens and Thlaspi arvense shoot transcriptomes. New Phytologist,170(2), 239–260.

  17. Hanikenne, M., Talke, I. N., Haydon, M. J., Lanz, C., Nolte, A., Motte, P., et al. (2008). Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature,453(7193), 391–395.

  18. Ingle, R. A., Mugford, S. T., Rees, J. D., Campbell, M. M., & Smith, J. A. C. (2005). Constitutively high expression of the histidine biosynthetic pathway contributes to nickel tolerance in hyperaccumulator plants. The Plant Cell,17(7), 2089–2106.

  19. Isaure, M. P., Huguet, S., Meyer, C. L., Castillo-Michel, H., Testemale, D., Vantelon, D., et al. (2015). Evidence of various mechanisms of Cd sequestration in the hyperaccumulator Arabidopsis halleri, the non-accumulator Arabidopsis lyrata, and their progenies by combined synchrotron-based techniques. Journal of Experimential Botany,66(11), 3201–3214.

  20. Kawachi, M., Kobae, Y., Mimura, T., & Maeshima, M. (2008). Deletion of a histidine-rich loop of AtMTP1, a vacuolar Zn2 +/H + antiporter of Arabidopsis thaliana, stimulates the transport activity. The Journal of biological chemistry,283(13), 8374–8383.

  21. Kerkeb, L., & Krämer, U. (2003). The role of free histidine in xylem loading of nickel in Alyssum lesbiacum and Brassica juncea. Plant Physiology,131(2), 716–724.

  22. Krämer, U. (2010). Metal hyperaccumulation in plants. Annual Review of Plant Biology,61, 517–534.

  23. Krämer, U., Cotter-Howells, J. D., Charnock, J. M., Baker, A. J. M., & Smith, J. A. C. (1996). Free histidine as a metal chelator in plants that accumulate nickel. Nature,379, 635–638.

  24. Kramer, U., Pickering, I. J., Prince, R. C., Raskin, I., & Salt, D. E. (2000). Subcellular localization and speciation of nickel in hyperaccumulator and non-accumulator Thlaspi species. Plant Physiology,122(4), 1343–1353.

  25. Krzeslowska, M. (2011). The cell wall in plant cell response to trace metals: Polysaccharide remodeling and its role in defense strategy. Acta Physiologiae Plantarum,33(1), 35–51.

  26. Kupper, H., Lombi, E., Zhao, F. J., Wieshammer, G., & McGrath, S. P. (2001). Cellular compartmentation of nickel in the hyperaccumulators Alyssum lesbiacum, Alyssum bertolonii and Thlaspi goesingense. Journal of Experimential Botany,52(365), 2291–2300.

  27. Kupper, H., Zhao, F. J., & McGrath, S. P. (1999). Cellular compartmentation of zinc in leaves of the hyperaccumulator Thlaspi caerulescens. Plant Physiology,119(1), 305–311.

  28. Liu, H., Zhao, H., Wu, L., & Xu, W. (2017). A genetic transformation method for cadmium hyperaccumulator Sedum plumbizincicola and non-hyperaccumulating ecotype of Sedum alfredii. Frontiers in Plant Science,8, 1047.

  29. Luo, J., Tao, Q., Jupa, R., Liu, Y., Wu, K., Song, Y., et al. (2019). Role of vertical transmission of shoot endophytes in root-associated microbiome assembly and heavy metal hyperaccumulation in Sedum alfredii. Environmental Science and Technology,53(12), 6954–6963.

  30. Ma, J. F., Ueno, D., Zhao, F. J., & McGrath, S. P. (2005). Subcellular localisation of Cd and Zn in the leaves of a Cd-hyperaccumulating ecotype of Thlaspi caerulescens. Planta,220(5), 731–736.

  31. Meier, S. K., Adams, N., Wolf, M., Balkwill, K., Muasya, A. M., Gehring, C. A., et al. (2018). Comparative RNA-seq analysis of nickel hyperaccumulating and non-accumulating populations of Senecio coronatus (Asteraceae). Plant Journal,95(6), 1023–1038.

  32. Meyer, C. L., Juraniec, M., Huguet, S., Chaves-Rodriguez, E., Salis, P., Isaure, M. P., et al. (2015). Intraspecific variability of cadmium tolerance and accumulation, and cadmium-induced cell wall modifications in the metal hyperaccumulator Arabidopsis halleri. Journal of Experimential Botany,66(11), 3215–3227.

  33. Nouet, C., Charlier, J. B., Carnol, M., Bosman, B., Farnir, F., Motte, P., et al. (2015). Functional analysis of the three HMA4 copies of the metal hyperaccumulator Arabidopsis halleri. Journal of Experimential Botany,66(19), 5783–5795.

  34. Peng, J. S., Ding, G., Meng, S., Yi, H. Y., & Gong, J. M. (2017a). Enhanced metal tolerance correlates with heterotypic variation in SpMTL, a metallothionein-like protein from the hyperaccumulator Sedum plumbizincicola. Plant, Cell and Environment,40(8), 1368–1378.

  35. Peng, J. S., & Gong, J. M. (2014). Vacuolar sequestration capacity and long-distance metal transport in plants. Frontiers in Plant Science,5, 19.

  36. Peng, J. S., Wang, Y. J., Ding, G., Ma, H. L., Zhang, Y. J., & Gong, J. M. (2017b). A pivotal role of cell wall in cadmium accumulation in the Crassulaceae hyperaccumulator Sedum plumbizincicola. Molecular Plant,10(5), 771–774.

  37. Persans, M. W., Yan, X., Patnoe, J. M., Krämer, U., & Salt, D. E. (1999). Molecular dissection of the role of histidine in nickel hyperaccumulation in Thlaspi goesingense (Hálácsy). Plant Physiology,121(4), 1117–1126.

  38. Rascio, N., & Navari-Izzo, F. (2011). Heavy metal hyperaccumulating plants: How and why do they do it? And what makes them so interesting? Plant Science,180(2), 169–181.

  39. Reeves, R. D., Baker, A. J. M., Jaffré, T., Erskine, P. D., Echevarria, G., & van der Ent, A. (2018). A global database for plants that hyperaccumulate metal and metalloid trace elements. New Phytologist,218(2), 407–411.

  40. Roosens, N. H., Leplae, R., Bernard, C., & Verbruggen, N. (2005). Variations in plant metallothioneins: The heavy metal hyperaccumulator Thlaspi caerulescens as a study case. Planta, 222, 716–729.

  41. Shahzad, Z., Gosti, F., Frérot, H., Lacombe, E., Roosens, N., Saumitou-Laprade, P., et al. (2010). The five AhMTP1 zinc transporters undergo different evolutionary fates towards adaptive evolution to zinc tolerance in Arabidopsis halleri. PLoS Genetics,6, e1000911.

  42. Talke, I., Hanikenne, M., & Krämer, U. (2006). Zinc dependent global transcriptional control, transcriptional deregulation and higher gene copy number for genes in metal homeostasis of the hyperaccumulator Arabidopsis halleri. Plant Physiology,142(1), 148–167.

  43. Tsednee, M., Yang, S. C., Lee, D. C., & Yeh, K. C. (2014). Root-secreted nicotianamine from Arabidopsis halleri facilitates zinc hypertolerance by regulating zinc bioavailability. Plant Physiology,166(2), 839–852.

  44. Ueno, D., Milner, M. J., Yamaji, N., Yokosho, K., Koyama, E., Zambrano, M. C., et al. (2011). Elevated expression of TcHMA3 plays a key role in the extreme Cd tolerance in a Cd-hyperaccumulating ecotype of Thlaspi caerulescens. Plant Journal,66(5), 852–862.

  45. Uraguchi, S., Weber, M., & Clemens, S. (2019). Elevated root nicotianamine concentrations are critical for Zn hyperaccumulation across diverse edaphic environments. Plant Cell Environment,42(6), 2003–2014.

  46. van de Mortel, J. E., Almar, J. E., Villanueva, L., Schat, H., Kwekkeboom, J., Coughlan, S., et al. (2006). Large expression differences in genes for iron and zinc homeostasis, stress response, and lignin biosynthesis distinguish roots of Arabidopsis thaliana and the related metal hyperaccumulator Thlaspi caerulescens. Plant Physiology,142(2), 1127–1147.

  47. van Hoof, N. A., Hassinen, V. H., Hakvoort, H. W., Ballintijn, K. F., Schat, H., Verkleij, J. A., et al. (2001). Enhanced copper tolerance in Silene vulgaris (Moench) Garcke populations from copper mines is associated with increased transcript levels of a 2b-type metallothionein gene. Plant Physiology,126(4), 1519–1526.

  48. Verbruggen, N., Hermans, C., & Schat, H. (2009). Molecular mechanisms of metal hyperaccumulation in plants. New Phytologist,181(4), 759–776.

  49. Weber, M., Harada, E., Vess, C., Roepenack-Lahaye, E., & Clemens, S. (2004). Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors. Plant Journal,37(2), 269–281.

  50. Weber, M., Trampczynska, A., & Clemens, S. (2005). Comparative transcriptome analysis of toxic metal responses in Arabidopsis thaliana and the Cd(2 +)-hypertolerant facultative metallophyte Arabidopsis halleri. Plant, Cell and Environment,29(5), 950–963.

  51. Weigel, H. J., & Jager, H. J. (1980). Subcellular-distribution and chemical form of cadmium in bean-plants. Plant Physiology, 65(3), 480–482.

  52. Willems, G., Drager, D. B., Courbot, M., Gode, C., Verbruggen, N., & Saumitou-Laprade, P. (2007). The genetic basis of zinc tolerance in the metallophyte Arabidopsis halleri ssp. halleri (Brassicaceae): An analysis of quantitative trait loci. Genetics, 176(1), 659–674.

  53. Wojcik, M., Vangronsveld, J., D’Haen, J., & Tukiendorf, A. (2005). Cadmium tolerance in Thlaspi caerulescens - II Localization of cadmium in Thlaspi caerulescens. Environmental and Experimental Botany,53(2), 163–171.

  54. Wood, J. L., Tang, C., & Franks, A. E. (2016). Microbial associated plant growth and heavy metal accumulation to improve phytoextraction of contaminated soils. Soil Biology & Biochemistry,103(2016), 131–137.

  55. Yang, Q. Y., Ma, X. X., Luo, S., Gao, J., Yang, X. E., & Feng, Y. (2018). SaZIP4, an uptake transporter of Zn/Cd hyperaccumulator Sedum alfredii Hance. Environmental and Experimental Botany,155(2018), 107–117.

  56. Zhao, H., Wang, L., Zhao, F. J., Wu, L., Liu, A., & Xu, W. (2019). SpHMA1 is a chloroplast cadmium exporter protecting photochemical reactions in the Cd hyperaccumulator Sedum plumbizincicola. Plant, Cell and Environment,42(4), 1112–1124.

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This study was financially supported by the National Natural Science Foundation of China (Grants 31700212) and Doctoral Scientific Research Start-up Funding of Hunan University of Science and Technology.

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Correspondence to Jia-Shi Peng or Shuan Meng.

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Peng, J., Guan, Y., Lin, X. et al. Comparative understanding of metal hyperaccumulation in plants: a mini-review. Environ Geochem Health (2020). https://doi.org/10.1007/s10653-020-00533-2

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  • Hyperaccumulator
  • Heavy metal
  • Elevated expression
  • Functional enhancement
  • Cell wall