Advertisement

Do arsenate reductase activities and oxalate exudation contribute to variations of arsenic accumulation in populations of Pteris vittata?

  • Fuyong Wu
  • Feifei Xu
  • Xiaona Ma
  • Wanqing Luo
  • Laiqing Lou
  • Ming Hung Wong
Soils, Sec 1 • Soil Organic Matter Dynamics and Nutrient Cycling • Research Article
  • 70 Downloads

Abstract

Purpose

Although arsenic (As) hyperaccumulation is a constitutive property for Pteris vittata, there is intraspecific variation in As accumulation among metallicolous (from As-contaminated soils) and nonmetallicolous populations (from uncontaminated soils) and the related mechanisms is still not clear.

Materials and methods

Pot trials, hydroponic culture, and manual simulation were conducted to investigate the roles of arsenate reductase and root exudates in accumulating As in P. vittata, which were collected from two uncontaminated sites including Sun Yat-sen University campus, Guangdong Province (ZD), and a botanical garden in Guangxi Academy of Forestry Sciences, Nanning City, Guangxi Province (NN), and two As and Pb/Zn mining and/or smelting sites located in Shaoguan of Guangdong Province (SG) and Guiyang of Hunan Province (GY).

Results and discussion

The nonmetallicolous populations (ZD and NN) possessed more efficient uptake of arsenate and arsenite than the metallicolous populations (SG and GY). There were significant (p < 0.05) difference in arsenate reductase activities in roots among the four populations of P. vittata and that the higher arsenate reductase activities were recorded in the nonmetallicolous populations (110 nkat mg−1 protein for ZD, 160 nkat mg−1 protein for NN) compared with the metallicolous populations (62.9 nkat mg−1 protein for SG, 78.1 nkat mg−1 protein for GY). Root exudates from the nonmetallicolous population (NN) and the metallicolous population (GY) of P. vittata contained similar compositions of organic acids including oxalic, malic, and succinic acids, of which oxalate were dominant (> 67%). The NN population exuded 4.23 times more oxalate than the SG population. Root exudates from the NN population mobilized significantly (p < 0.05) more As from As-contaminated soils than those from the SG population, of which oxalate had the most effective in As mobilization.

Conclusions

The present study suggests that higher arsenate reductase activities and oxalate exudation in the nonmetallicolous populations may play an important role in increasing their efficiency in phytoremediation of As-contaminated soils.

Keywords

Arsenate reductase Arsenic species Chinese brake fern Intraspecific variation Oxalate secretion 

Notes

Funding

The present work was supported by Natural Science Basic Research Plan in Shaanxi Province of China (Program No. 2016JM4004) and Chinese Universities Scientific Fund (Program No. 2452015179), and the Scientific Research Foundation for the Introduction of Talent, Northwest A&F University, China (2014), is gratefully acknowledged.

Supplementary material

11368_2018_1987_MOESM1_ESM.docx (19 kb)
ESM 1 (DOCX 19 kb)

References

  1. Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266CrossRefGoogle Scholar
  2. Cesaro P, Cattaneo C, Bona E, Berta G, Cavaletto M (2015) The arsenic hyperaccumulating Pteris vittata expresses two arsenate reductases. Sci Rep 5:14525CrossRefGoogle Scholar
  3. Chen TB, Wei CY, Huang ZC, Huang QF, Lu QG, Fan ZL (2002) Arsenic hyperaccumulator Pteris vittata L. and its arsenic accumulation. Chin Sci Bull 47:902–905CrossRefGoogle Scholar
  4. Das S, Chou ML, Jean JS, Yang HJ, Kim PJ (2017) Arsenic-enrichment enhanced root exudates and altered rhizosphere microbial communities and activities in hyperaccumulator Pteris vittata. J Hazard Mater 325:279–287CrossRefGoogle Scholar
  5. Duan GL, Zhu YG, Tong YP, Cai C, Kneer R (2005) Characterization of arsenate reductase in the extract of roots and fronds of Chinese brake fern, an arsenic hyperaccumulator. Plant Physiol 138:461–469CrossRefGoogle Scholar
  6. Dytrtova JJ, Jakl M, Sestakova I, Zins EL, Schroder D, Navratil T (2011) A new approach to study cadmium complexes with oxalic acid in soil solution. Anal Chim Acta 693:100–105CrossRefGoogle Scholar
  7. Garcia JAL, Barbas C, Probanza A, Barrientos ML, Manero FJG (2001) Low molecular weight organic acids and fatty acids in root exudates of two Lupinus cultivars at flowering and fruiting stages. Phytochem Anal 12:305–311CrossRefGoogle Scholar
  8. Halimaa P, Lin YF, Ahonen VH, Blande D, Clemens S, Gyenesei A, Haikio E, Karenlampi SO, Laiho A, Aarts MGM (2014) Gene expression differences between Noccaea caerulescens ecotypes help to identify candidate genes for metal phytoremediation. Environ Sci Technol 48:3344–3353CrossRefGoogle Scholar
  9. He ZY, Yan HL, Chen YS, Shen HL, Xu WX, Zhang HY, Shi L, Zhu YG, Ma M (2016) An aquaporin PvTIP4;1 from Pteris vittata may mediate arsenite uptake. New Phytol 209:746–761CrossRefGoogle Scholar
  10. Hoagland DR, Arnon DI (1938) The water culture method for growing plants without soil. Circ Calif Agric Exp Sta 347:1–39Google Scholar
  11. Li YH, Huang BX, Shan XQ (2003) Determination of low molecular weight organic acids in soil, plants, and water by capillary zone electrophoresis. Anal Bioanal Chem 375:775–780CrossRefGoogle Scholar
  12. Liu Y, Wang HB, Wong MH, Ye ZH (2009) The role of arsenate reductase and superoxide dismutase in As accumulation in four Pteris species. Environ Int 35:491–495CrossRefGoogle Scholar
  13. Liu X, Fu JW, Guan DX, Cao Y, Luo J, Rathinasabapathi B, Chen Y, Ma LQ (2016) Arsenic induced phytate exudation, and promoted FeAsO4 dissolution and plant growth in as-hyperaccumulator Pteris vittata. Environ Sci Technol 50:9070–9077CrossRefGoogle Scholar
  14. Lombi E, Zhao FJ, Fuhrmann M, Ma LQ, McGrath SP (2002) Arsenic distribution and speciation in the fronds of the hyperaccumulator Pteris vittata. New Phytol 156:195–203CrossRefGoogle Scholar
  15. Lou LQ, Ye ZH, Lin AJ, Wong MH (2010) Interaction of arsenic and phosphate on their uptake and accumulation in Chinese brake fern. Int J Phytoremed 12:487–502CrossRefGoogle Scholar
  16. Ma LQ, Komar KM, Tu C, Zhang W, Cai Y, Kennelly ED (2001) A fern that hyperaccumulates arsenic. Nature 409:579CrossRefGoogle Scholar
  17. Morita A, Yanagisawa O, Maeda S, Takatsu S, Ikka T (2011) Tea plant (Camellia sinensis L.) roots secrete oxalic acid and caffeine into medium containing aluminum. Soil Sci Plant Nutr 57:796–802CrossRefGoogle Scholar
  18. Pickering IJ, Gumaelius L, Harris HH, Prince RC, Hirsch G, Banks JA, Salt DE, George GN (2006) Localizing the biochemical transformations of arsenate in a hyperaccumulating fern. Environ Sci Technol 40:5010–5014CrossRefGoogle Scholar
  19. Poynton CY, Huang JWW, Blaylock MJ, Kochian LV, Elless MP (2004) Mechanisms of arsenic hyperaccumulation in Pteris species: root as influx and translocation. Planta 219:1080–1088CrossRefGoogle Scholar
  20. Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci 180:169–181CrossRefGoogle Scholar
  21. Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Annu Rev Plant Physiol Mol Biol 52:527–560CrossRefGoogle Scholar
  22. Su YH, McGrath SP, Zhu YG, Zhao FJ (2008) Highly efficient xylem transport of arsenite in the arsenic hyperaccumulator Pteris vittata. New Phytol 180:434–441CrossRefGoogle Scholar
  23. Tao Q, Hou DD, Yang XE, Li TQ (2016) Oxalate secretion from the root apex of Sedum alfredii contributes to hyperaccumulation of cd. Plant Soil 398:139–152CrossRefGoogle Scholar
  24. Tu SX, Ma L, Luongo T (2004) Root exudates and arsenic accumulation in arsenic hyperaccumulating Pteris vittata and nonhyperaccumulating Nephrolepis exaltata. Plant Soil 258:9–19CrossRefGoogle Scholar
  25. Valentinuzzi F, Cesco S, Tomasi N, Mimmo T (2015) Influence of different trap solutions on the determination of root exudates in Lupinus albus L. Biol Fertil Soils 51:757–765CrossRefGoogle Scholar
  26. Visoottiviseth P, Francesconi K, Sridokchan W (2002) The potential of Thai indigenous plant species for the phytoremediation of arsenic contaminated land. Environ Pollut 118:453–461CrossRefGoogle Scholar
  27. Wan XM, Lei M, Liu YR, Huang ZC, Chen TB, Gao D (2013) A comparison of arsenic accumulation and tolerance among four populations of Pteris vittata from habitats with a gradient of arsenic concentration. Sci Total Environ 442:143–151CrossRefGoogle Scholar
  28. Wang JR, Zhao FJ, Meharg AA, Raab A, Feldmann J, McGrath SP (2002) Mechanisms of arsenic hyperaccumulation in Pteris vittata. Uptake kinetics, interactions with phosphate, and arsenic speciation. Plant Physiol 130:1552–1561CrossRefGoogle Scholar
  29. Whipps JM (1990) Carbon economy. In: Lynch JM (ed) The rhizosphere. John Wiley & Sons Ltd, Essex, pp 59–97Google Scholar
  30. Wu FY, Ye ZH, Wu SC, Wong MH (2007) Metal accumulation and arbuscular mycorrhizal status in metallicolous and nonmetallicolous populations of Pteris vittata L. and Sedum alfredii Hance. Planta 226:1363–1378CrossRefGoogle Scholar
  31. Wu FY, Ye ZH, Wu SC, Leung HM, Wong MH (2009) Variation in arsenic, lead and zinc tolerance and accumulation in six populations of Pteris vittata L. from China. Environ Pollut 157:2394–2404CrossRefGoogle Scholar
  32. Wu FY, Deng D, Wu SC, Lin XG, Wong MH (2015) Arsenic tolerance, uptake and accumulation between nonmetallicolous and metallicolous populations of Pteris vittata L. Environ Sci Pollut Res 22:8911–8918CrossRefGoogle Scholar
  33. Zhang W, Cai Y, Tu C, Ma LQ (2002) Arsenic speciation and distribution in an arsenic hyperaccumulating plant. Sci Total Environ 300:167–177CrossRefGoogle Scholar
  34. Zhao FJ, Hamon RE, McLaughlin MJ (2001) Root exudates of the hyperaccumulator Thlaspi caerulescens do not enhance metal mobilization. New Phytol 151:613–620CrossRefGoogle Scholar
  35. Zhao FJ, Dunham SJ, McGrath SP (2002) Arsenic hyperaccumulation by different fern species. New Phytol 156:27–31CrossRefGoogle Scholar
  36. Zhao FJ, McGrath SP, Meharg AA (2010) Arsenic as a food chain contaminant: mechanisms of plant uptake and metabolism and mitigation strategies. Annu Rev Plant Biol 61:535–559CrossRefGoogle Scholar
  37. Zhu XF, Zheng C, Hu YT, Jiang T, Liu Y, Dong NY, Yang JL, Zheng SJ (2011) Cadmium-induced oxalate secretion from root apex is associated with cadmium exclusion and resistance in Lycopersicon esulentum. Plant Cell Environ 34:1055–1064CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.College of Natural Resources and EnvironmentNorthwest A&F UniversityYanglingPeople’s Republic of China
  2. 2.Key Laboratory of Plant Nutrition and the Agri-environment in Northwest ChinaMinistry of AgricultureYanglingPeople’s Republic of China
  3. 3.College of Life SciencesNanjing Agricultural UniversityNanjingPeople’s Republic of China
  4. 4.Consortium on Health, Environment, Education and Research (CHEER)Education University of Hong KongHong KongPeople’s Republic of China

Personalised recommendations