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Root foraging and selenium uptake in the Australian hyperaccumulator Neptunia amplexicaulis and non‐accumulator Neptunia gracilis

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Abstract

Background and aims

Neptunia amplexicaulis, endemic to Central Queensland (Australia), is one of the strongest selenium (Se) hyperaccumulators known globally, capable of accumulating up to 13 600 µg Se g− 1 in its leaves. This work aimed to elucidate root foraging in response to Se in N. amplexicaulis applied in two different chemical forms and concentrations compared to the sympatric non-accumulator N. gracilis.

Methods

Neptunia amplexicaulis and N. gracilis seeds were germinated and transplanted into rhizotrons filled with half control and half Se-dosed soils with low (5 µg Se g− 1) or high (30 µg Se g− 1) levels of Se in soluble (Na2SeO4) or insoluble (CaSeO3) form. After 3 weeks, the root density in the two areas of the rhizotrons was measured and plants were removed from the soil to determine biomass and for chemical analysis of Se and other elements.

Results

Major changes were observed in the low Se dosed side in Na2SeO4 form, and in the high Se dosed side in CaSeO3 form in N. amplexicaulis roots: a higher density, Se concentration, Se:S ratio, and a tendency to increase the biomass. In contrast, a reduction in the root density with 30 µg Se g− 1 in respose to the CaSeO3 form was observed in N. gracilis.

Conclusions

Neptunia amplexicaulis preferentially foraged in Se soluble enriched soil, which may be beneficial for the plant given the increase in the root biomass at low Se dosed soil. In contrast, a reduction in the root density in N. gracilis indicated avoidance of soils enriched with high insoluble form of Se.

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References

  • Anderson JW (1993) Selenium interactions in sulfur metabolism. In: Sulfur nutrition and assimilation in higher plants: Regulatory, agricultural and environmental aspects. SPB Academic Publishing, The Hague, pp 49–60

    Google Scholar 

  • Assunção AGL, Bookum WM, Nelissen HJM, Vooijs R, Schat H, Ernst WHO (2003a) Differential metal-specific tolerance and accumulation patterns among Thlaspi caerulescens populations originating from different soil types. New Phytol 159:411–419

    Article  PubMed  Google Scholar 

  • Assunção AGL, Schat H, Aarts MGM (2003b) Thlaspi caerulescens, an attractive model species to study heavy metal hyperaccumulation in plants, vol 159. Blackwell Publishing Ltd., Oxford

  • AVH (2019) The Australasian Virtual Herbarium. Council Heads of Australasian Herbaria. https://avh.chah.org.au/. Accessed 6/09 2019

  • Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyper accumulate metallic elements. Biorecovery 1:81–126

    CAS  Google Scholar 

  • Bell PF, Parker DR, Page AL (1992) Contrasting selenate sulfate interactions in selenium-accumulating and nonaccumulating plant species. Soil Sci Soc Am J 56:1818–1824

    Article  CAS  Google Scholar 

  • Broadley MR, White PJ, Bryson RJ, Meacham MC, Bowen HC, Johnson SE, Hawkesford MJ, McGrath SP, Zhao FJ, Breward N, Harriman M, Tucker M (2006) Biofortification of UK food crops with selenium. Proc Nutr Soc 65:169–181

    Article  CAS  PubMed  Google Scholar 

  • Brown T, Shrift A (1982) Selenium: Toxicity and tolerance in higher plants. Biol Rev Camb Philos Soc 57:59–84

    Article  CAS  Google Scholar 

  • Broyer T, Johnson C, Huston R (1972) Selenium and nutrition of Astragalus. Plant Soil 36:635–649

    Article  CAS  Google Scholar 

  • Cappa J, Pilon-Smits E (2014) Evolutionary aspects of elemental hyperaccumulation. Planta 239:267–275

    Article  CAS  PubMed  Google Scholar 

  • Dechamps C, Noret N, Mozek R, Draye X, Meerts P (2008) Root allocation in metal-rich patch by Thlaspi caerulescens from normal and metalliferous soil—new insights into the rhizobox approach. Plant Soil 310:211–224

    Article  CAS  Google Scholar 

  • El Mehdawi AF, Reynolds RJB, Prins CN, Lindblom SD, Cappa JJ, Fakra SC, Pilon-Smits EAH (2014) Analysis of selenium accumulation, speciation and tolerance of potential selenium hyperaccumulator Symphyotrichum ericoides. Physiol Plant 152:70–83

    Article  PubMed  Google Scholar 

  • Ellis DR, Salt DE (2003) Plants, selenium and human health. Curr Opin Plant Biol 6:273–279

    Article  CAS  PubMed  Google Scholar 

  • Feist LJ, Parker DR (2001) Ecotypic variation in selenium accumulation among populations of Stanleya pinnata. New Phytol 149:61–69

    Article  CAS  PubMed  Google Scholar 

  • Freeman JL, Zhang LH, Marcus MA, Fakra S, McGrath SP, Pilon-Smits EAH (2006) Spatial imaging, speciation, and quantification of selenium in the hyperaccumulator plants Astragalus bisulcatus and Stanleya pinnata. Plant Physiol 142:124–134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galeas ML, Zhang LH, Freeman JL, Wegner M, Pilon-Smits EAH (2007) Seasonal fluctuations of selenium and sulfur accumulation in selenium hyperaccumulators and related nonaccumulators. New Phytol 173:517–525

    Article  CAS  PubMed  Google Scholar 

  • Galeas ML, Klamper EM, Bennett LE, Freeman JL, Kondratieff BC, Quinn CF, Pilon-Smits EAH (2008) Selenium hyperaccumulation reduces plant arthropod loads in the field. New Phytol 177:715–724

    Article  CAS  PubMed  Google Scholar 

  • Gonneau C, Noret N, Godé C, Frérot H, Sirguey C, Sterckeman T, Pauwels M (2017) Demographic history of the trace metal hyperaccumulator Noccaea caerulescens (J. Presl and C. Presl) F. K. Mey. in Western Europe. Mol Ecol 26:904–922

    Article  PubMed  Google Scholar 

  • Goodson CC, Parker DR, Amrhein C, Zhang Y (2003) Soil selenium uptake and root system development in plant taxa differing in Se-accumulating capability. New Phytol 159:391–401

    Article  CAS  PubMed  Google Scholar 

  • Guan P et al (2014) Nitrate foraging by Arabidopsis roots is mediated by the transcription factor TCP20 through the systemic signaling pathway. PNAS 111:15267–15272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haines BJ (2002) Zincophilic root foraging in Thlaspi caerulescens. New Phytol 155:363–372

    Article  CAS  PubMed  Google Scholar 

  • Hartikainen H, Pietola L, Simojoki A (2001) Quantification of fine root responses to selenium toxicity. Agric Food Sci 10:53–58

    Article  CAS  Google Scholar 

  • Harvey M-A et al (2020) Distribution and chemical form of selenium in Neptunia amplexicaulis from Central Queensland, Australia. Metallomics 12:514–527

    Article  CAS  PubMed  Google Scholar 

  • Hopper JL, Parker DR (1999) Plant availability of selenite and selenate as influenced by the competing ions phosphate and sulfate. Plant Soil 210:199–207

    Article  CAS  Google Scholar 

  • Jaffré T, Brooks RR, Lee J, Reeves RD (1976) Sebertia acuminata: A hyperaccumulator of nickel from New Caledonia. Science 193:579–580

    Article  PubMed  Google Scholar 

  • Knott SG, McCray CWR (1959) Two naturally occurring outbreaks of selenosis in Queensland. Aust Vet J 35:332–334

    Article  Google Scholar 

  • Kong L, Wang M, Bi D (2005) Selenium modulates the activities of antioxidant enzymes, osmotic homeostasis and promotes the growth of sorrel seedlings under salt stress. Plant Growth Regul 45:155–163

    Article  CAS  Google Scholar 

  • Kukier U, Chaney RL (2001) Amelioration of nickel phytotoxicity in muck and mineral soils. J Environ Qual 30:1949–1960

    Article  CAS  PubMed  Google Scholar 

  • Li HF, McGrath SP, Zhao FJ (2008) Selenium uptake, translocation and speciation in wheat supplied with selenate or selenite. New Phytol 178:92–102

    Article  CAS  PubMed  Google Scholar 

  • Liu J-Q, Allan DL, Vance CP (2010) Systemic signaling and local sensing of phosphate in common bean: Cross-talk between photosynthate and microrna399. Mol Plant 3:428–437

    Article  CAS  PubMed  Google Scholar 

  • McCray CWR, Hurwood IS (1963) Selenosis in north west Queensland associated with marine cretaceous formation. Qld J Agric Sci 20:475–498

    CAS  Google Scholar 

  • Mehdawi E, Paschke AF, Paschke MW, Pilon-Smits EAH (2015) Symphyotrichum ericoides populations from seleniferous and nonseleniferous soil display striking variation in selenium accumulation. New Phytol 206:231–242

    Article  PubMed  Google Scholar 

  • Neuhierl B, Böck A (1996) On the mechanism of selenium tolerance in selenium-accumulating plants: purification and characterization of a specific selenocysteine methyltransferase from cultured cells of Astragalus bisulcatus.Eur J Biochem 239:235–238

    Article  CAS  PubMed  Google Scholar 

  • Peterson PJ, Butler GW (1967) Significance of selenocystathionine in an Australian selenium-accumulating plant, Neptunia amplexicaulis. Nature 213:599–600

    Article  CAS  Google Scholar 

  • Pilon-Smits EAH et al (1999) Overexpression of ATP sulfurylase in Indian mustard leads to increased selenate uptake, reduction and tolerance. Plant Physiol 119:23–132

    Article  Google Scholar 

  • Pilon-Smits EA, Quinn CF, Tapken W, Malagoli M, Schiavon M (2009) Physiological functions of beneficial elements. Curr Opin Plant Biol 12:267–274

    Article  CAS  PubMed  Google Scholar 

  • Quinn CF, Freeman J, Galeas ML, Klamper EM, Pilon-Smits EAH (2008) The role of selenium in protecting plants against prairie dog herbivory: implications for the evolution of selenium hyperaccumulation. Oecologia 155:267–275

    Article  PubMed  Google Scholar 

  • Quinn CF, Freeman JL, Reynolds RJB, Cappa JJ, Fakra SC, Marcus MA, Lindblom SD, Quinn EK, Bennet LE, Pilot-Smits EAH (2010) Selenium hyperaccumulation offers protection from cell disruptor herbivores. BMC Ecol 10:19

    Article  PubMed  PubMed Central  Google Scholar 

  • Rao S, Yu T, Cong X, Xu F, Lai X, Zhang W, Liao Y, Cheng S (2020) Integration analysis of PacBio SMRT- and Illumina RNA-seq reveals candidate genes and pathway involved in selenium metabolism in hyperaccumulator Cardamine violifolia. BMC Plant Biol 20:492

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosenfeld I, Beath OA (1964) Selenium: Geobotany, biochemistry, toxicity and nutrition. Academic Press, New York

    Google Scholar 

  • Schiavon M, Pilon-Smits EA (2016) The fascinating facets of plant selenium accumulation – biochemistry, physiology, evolution and ecology. New Phytol 213:1582–1596

    Article  PubMed  Google Scholar 

  • Schiavon M, Pilon M, Malagoli M, Pilon-Smits EA (2015) Exploring the importance of sulfate transporters and ATP sulphurylases for selenium hyperaccumulation-a comparison of Stanleya pinnata and Brassica juncea (Brassicaceae). Front Plant Sci 6:2

    Article  PubMed  PubMed Central  Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schwartz C, Morel JL, Saumier S, Whiting SN, Baker AJM (1999) Root development of the Zinc-hyperaccumulator plant Thlaspi caerulescens as affected by metal origin, content and localization in soil. Plant Soil 208:103–115

    Article  CAS  Google Scholar 

  • Shrift A (1969) Aspects of selenium metabolism in higher plants. Annu Rev Plant Physiol 20:475–494

    Article  CAS  Google Scholar 

  • Singh KM, Singh KN, Bhandari KD (1980) Interaction of selenium and sulfur on the growth and chemical composition of Raya. Soil Sci 129:238–244

    Article  CAS  Google Scholar 

  • Sors TG, Ellis DR, Na GN, Lahner B, Lee S, Leustek T, Pickering IJ, Salt DE (2005) Analysis of sulfur and selenium assimilation in Astragalus plants with varying capacities to accumulate selenium. Plant J 42:785–797

    Article  CAS  PubMed  Google Scholar 

  • Sors TG, Martin CP, Salt DE (2009) Characterization of selenocysteine methyltransferases from Astragalus species with contrasting selenium accumulation capacity Plant J 59:110–122

    Article  CAS  PubMed  Google Scholar 

  • Stadtman TC (1990) Selenium biochemistry. Annu Rev Biochem 59:111–127

    Article  CAS  PubMed  Google Scholar 

  • Terry N, Zayed AM, de Souza MP, Tarun AS (2000) Selenium in higher plants. Annu Rev Plant Physiol 51:401–432

    Article  CAS  Google Scholar 

  • Tognacchini A, Salinitro M, Puschenreiter M, van der Ent A (2020) Root foraging and avoidance in hyperaccumulator and excluder plants: a rhizotron experiment. Plant Soil 450:287–302

    Article  CAS  Google Scholar 

  • Trelease SF, Trelease HM (1938) Selenium as a stimulating and possibly essential element for indicator plants. Am J Bot 25:372–380

    Article  CAS  Google Scholar 

  • van der Ent A, Baker A, Reeves RD, Pollard A, Schat H (2013) Hyperaccumulators of metal and metalloid trace elements: Facts and fiction. Plant Soil 362:319–334

    Article  Google Scholar 

  • Van Hoewyk D (2013) A tale of two toxicities: malformed selenoproteins and oxidative stress both contribute to selenium stress in plants. Annals Bot-London 112:965–972

    Article  Google Scholar 

  • Wang Y, Kanipayor R, Brindle ID (2014) Rapid high-performance sample digestion for ICP determination by ColdBlock™ digestion: part 1 environmental samples. J Anal At Spectom 29:162–168

    Article  CAS  Google Scholar 

  • White PJ (2016) Selenium accumulation by plants. Ann Bot 117:217–235

    CAS  PubMed  Google Scholar 

  • White PJ, Bowen HC, Parmaguru P, Fritz M, Spracklen WP, Spiby RE, Meacham MC, Mead A, Harriman M, Trueman LJ, Smith BM, Thomas B, Broadley MR (2004) Interactions between selenium and sulphur nutrition in Arabidopsis thaliana. J Exp Bot 55:1927–1937

    Article  CAS  PubMed  Google Scholar 

  • White PJ, Bowen HC, Marshall B, Broadley MR (2007) Extraordinarily high leaf selenium to sulfur ratios define ‘Se-accumulator’ plants. Ann Bot 100:111–118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whiting SN, Leake JR, McGrath SP, Baker AJM (2000) Positive responses to Zn and Cd by roots of the Zn and Cd hyperaccumulator Thlaspi caerulescens. New Phytol 145:199–210

    Article  CAS  Google Scholar 

  • Xue T, Hartikainen H, Piironen V (2001) Antioxidative and growth-promoting effect of selenium on senescing lettuce. Plant Soil 237:55–61

    Article  CAS  Google Scholar 

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Acknowledgements

K. Pinto Irish and M-A. Harvey are the recipients of Australian Government Research Training Program (RTP) Scholarships at The University of Queensland and their research is supported by this funding.

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Authors and Affiliations

  1. Centre for Mined Land Rehabilitation, Sustainable Minerals Institute, The University of Queensland, Queensland, Australia

    Katherine Pinto Irish, Maggie-Anne Harvey, Peter D. Erskine & Antony van der Ent

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  1. Katherine Pinto Irish
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  2. Maggie-Anne Harvey
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Correspondence to Antony van der Ent.

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Pinto Irish, K., Harvey, MA., Erskine, P.D. et al. Root foraging and selenium uptake in the Australian hyperaccumulator Neptunia amplexicaulis and non‐accumulator Neptunia gracilis. Plant Soil 462, 219–233 (2021). https://doi.org/10.1007/s11104-021-04843-x

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