Planta

, Volume 237, Issue 3, pp 717–729 | Cite as

Inoculation of Astragalusracemosus and Astragalus convallarius with selenium-hyperaccumulator rhizosphere fungi affects growth and selenium accumulation

  • Stormy Dawn Lindblom
  • Sirine C. Fakra
  • Jessica Landon
  • Paige Schulz
  • Benjamin Tracy
  • Elizabeth A. H. Pilon-Smits
Original Article

Abstract

Little is known about how fungi affect plant selenium (Se) accumulation. Here we investigate the effects of two fungi on Se accumulation, translocation, and chemical speciation in the hyperaccumulator Astragalus racemosus and the non-accumulator Astragalus convallarius. The fungi, Alternaria astragali (A3) and Fusarium acuminatum (F30), were previously isolated from Astragalus hyperaccumulator rhizosphere. A3-inoculation enhanced growth of A. racemosus yet inhibited growth of A. convallarius. Selenium treatment negated these effects. F30 reduced shoot-to-root Se translocation in A. racemosus. X-ray microprobe analysis showed no differences in Se speciation between inoculation groups. The Astragalus species differed in Se localization and speciation. A. racemosus root-Se was distributed throughout the taproot and lateral root and was 90 % organic in the lateral root. The related element sulfur (S) was present as a mixture of organic and inorganic forms in the hyperaccumulator. Astragalus convallarius root-Se was concentrated in the extreme periphery of the taproot. In the lateral root, Se was exclusively in the vascular core and was only 49 % organic. These findings indicate differences in Se assimilation between the two species and differences between Se and S speciation in the hyperaccumulator. The finding that fungi can affect translocation may have applications in phytoremediation and biofortification.

Keywords

Plant–microbe interactions Hyperaccumulation Alternaria astragali Fusarium acuminatum μ-X-ray absorption near edge spectroscopy μ-X-ray fluorescence mapping 

Notes

Acknowledgments

We thank Ami Wangeline for providing the two fungal isolates, and Jose Rodolfo Valdez Barillas for helping with fungal cultivation and preparation. Funding for these studies was provided by National Science Foundation grant # IOS-0817748 to Elizabeth A. H. Pilon-Smits. The Advanced Light Source is supported by the Office of Science, Basic Energy Sciences, and Division of Materials Science of the U.S. Department of Energy (DE-AC02-05CH11231).

References

  1. Beath OA (1982) The story of selenium in Wyoming. Univ Wyo Agric Exp Stat Bull 774Google Scholar
  2. Beath OA, Gilbert CS, Eppson HF (1939) The use of indicator plants in locating seleniferous soils in the Western United States. I General Am J Bot 26:257–269CrossRefGoogle Scholar
  3. Boyd RS (2010) Heavy metal pollutants and chemical ecology: exploring new frontiers. J Chem Ecol 36:46–58PubMedCrossRefGoogle Scholar
  4. Boyd RS, Martens SN (1992) The raison d’être for metal for metal hyperaccumulation by plants. In: Baker AJM, Proctor J, Reeves RD (eds) The vegetation of ultramafic (Serpentine) soils. Intercept, Andover, pp 279–289Google Scholar
  5. de Souza MP, Chu D, Zhao M, Zayed AM, Ruzin SE, Schichnes D, Terry N (1998a) Rhizosphere bacteria enhance selenium accumulation and volatilization by Indian mustard. Plant Physiol 119:565–574CrossRefGoogle Scholar
  6. de Souza MP, Pilon-Smits EAH, Lytle CM, Hwang S, Tai J, Honma TSU, Yeh L, Terry N (1998b) Rate-limiting steps in selenium assimilation and volatilization by Indian mustard. Plant Physiol 117:1487–1494PubMedCrossRefGoogle Scholar
  7. Djanaguiraman M, Devi DD, Shanker AK, Sheeba JA and Bangarusamy U (2005) Selenium—an antioxidative protectant in soybean during senescence. Plant Soil 272:77–86Google Scholar
  8. El Mehdawi AF, Quinn CF, El-Mehdawi AF, Quinn CF, Pilon-Smits EAH (2011) Effects of selenium hyperaccumulation on plant–plant interactions: evidence for elemental allelopathy. New Phytol 191:120–131PubMedCrossRefGoogle Scholar
  9. El Mehdawi AF, Cappa JJ, Fakra SC, Self J, Pilon-Smits EAH (2012) Interactions of selenium hyperaccumulators and nonaccumulators during cocultivation on seleniferous or noseleniferous soil—the importance of having good neighbors. New Phytol 194:264–277PubMedCrossRefGoogle Scholar
  10. El-Mehdawi AF, Pilon-Smits EAH (2012) Ecological aspects of plant selenium hyperaccumulation. Plant Biol (in press). doi:10.1111/j.1438-8677.2011.00535.x
  11. Fassel VA (1978) Quantitative elemental analysis by plasma emission spectroscopy. Science 202:183–191PubMedCrossRefGoogle Scholar
  12. Freeman JL, Zhang LH, Marcus MA, Fakra S, Pilon-Smits EAH (2006) Spatial imaging, speciation and quantification of selenium in the hyperaccumulator plants Astragalus bisulcatus and Stanleya pinnata. Plant Physiol 142:124–134PubMedCrossRefGoogle Scholar
  13. Galeas ML, Zhang LH, Freeman JL, Wegner M, Pilon-Smits EAH (2007) Seasonal fluctuations of selenium and sulfur accumulation in selenium hyperaccumulators and related non-accumulators. New Phytol 173:517–525PubMedCrossRefGoogle Scholar
  14. Grant K, Carey NM, Mendoza M, Schulze M, Pilon M, Pilon-Smits EAH, Van Hoewyk D (2011) Adenosine 5-phosphosulfate reductase (APR2) mutation in Arabidopsis implicates glutathione deficiency in selenate toxicity. Biochem J 438:325–335PubMedCrossRefGoogle Scholar
  15. Hanson B, Garifullina GF, Lindblom SD, Wangeline A, Ackley A, Kramer K, Norton AP, Lawrence CB, Pilon Smits EAH (2003) Selenium accumulation protects Brassica juncea from invertebrate herbivory and fungal infection. New Phytol 159:461–469CrossRefGoogle Scholar
  16. Hartikainen H (2005) Biogeochemistry of selenium and its impact on food chain quality and human health. J Trace Elem Med Biol 18:309–318PubMedCrossRefGoogle Scholar
  17. Hartikainen H, Xue T, Piironen V (2000) Selenium as an anti-oxidant and pro-oxidant in ryegrass. Plant Soil 225:193–200CrossRefGoogle Scholar
  18. Hoagland D, Arnon DI (1938) The water culture method for growing plants without soil. Bull Calif Agric Exp Stat, Circ 347Google Scholar
  19. Ip C, Thompson HJ, Zhu Z, Ganther HE (2000) In vivo studies of methylseleninic acid: evidence that a monomethylated selenium metabolite is critical for cancer chemoprevention. Cancer Res 60:2882–2886PubMedGoogle Scholar
  20. Jalilehvand F (2006) Sulfur: not a “silent” element any more. Chem Soc Rev 35:1256–1268PubMedCrossRefGoogle Scholar
  21. Lindblom SD, Valdez-Barillas JR, Fakra S, Marcus MA, Wangeline AL, Pilon-Smits EAH (2012) Influence of microbial associations on selenium localization and speciation in roots of Astragalus and Stanleya hyperaccumulators. Environ Exp Bot doi:10.1016/j.envexpbot.2011.12.011 Google Scholar
  22. Lobanov AV, Hatfield DL, Gladyshev VN (2009) Eukaryotic selenoproteins and selenoproteomes. Biochim Biophys Acta 1790:1424–1428PubMedCrossRefGoogle Scholar
  23. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol Plant 15:437–497CrossRefGoogle Scholar
  24. Neuhierl B, Bock 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 239:235–238PubMedCrossRefGoogle Scholar
  25. Pickering IJ, Wright C, Bubner B, Ellis D, Persans MJ, Yu EY, George GN, Prince RC, Salt DE (2003) Chemical form and distribution of selenium and sulfur in the selenium hyperaccumulator Astragalus bisulcatus. Plant Physiol 131:1460–1467PubMedCrossRefGoogle Scholar
  26. Pilon-Smits EAH, Pilon M (2006) Sulfur metabolism in plastids. In: Wise RR, Hoober JK (eds) Advances in photosynthesis and respiration—the structure and function of plastids. Kluwer Academic Publishers, Dordrecht, pp 387–402CrossRefGoogle Scholar
  27. Pilon-Smits EAH, Quinn CF, Tapken W, Malagoli M, Schiavon M (2009) Physiological functions of beneficial elements. Curr Opin Plant Biol 12:267–274PubMedCrossRefGoogle Scholar
  28. Quinn CF, Wyant KA, Wangeline AL, Shulman J, Galeas ML, Valdez JR, Self JR, Paschke MW, Pilon-Smiots EAH (2011) Enhanced decomposition of selenium hyperaccumulator litter in a seleniferous habitat—evidence for specialist decomposers? Plant Soil 341:51–61CrossRefGoogle Scholar
  29. Stadtman TC (1990) Selenium biochemistry. Annu Rev Biochem 59:111–127PubMedCrossRefGoogle Scholar
  30. Stadtman TC (1996) Selenocysteine. Annu Rev Biochem 65:83–100PubMedCrossRefGoogle Scholar
  31. Terry N, Zayed AM, de Souza MP, Tarun AS (2000) Selenium in higher plants. Annu Rev Plant Physiol Plant Mol Biol 51:401–432PubMedCrossRefGoogle Scholar
  32. Vairavamurthy A (1998) Using X-ray absorption to probe sulfur oxidation states in complex molecules. Spectrochim Acta Part A 54:2009–2017CrossRefGoogle Scholar
  33. Van Hoewyk D, Garifullina GF, Ackley AR, Abdel-Ghany SE, Marcus MA, Fakra S, Ishiyama K, Inoue E, Pilon M, Takahashi H, Pilon-Smits EAH (2005) Overexpression of AtCpNifS enhances selenium tolerance and accumulation in Arabidopsis. Plant Physiol 139:1518–1528PubMedCrossRefGoogle Scholar
  34. Van Hoewyk D, Takahashi H, Hess A, Tamaoki M, Pilon-Smits EAH (2008) Transcriptome and biochemical analyses give insights into selenium-stress responses and selenium tolerance mechanisms in Arabidopsis. Physiol Plant 132:236–253PubMedGoogle Scholar
  35. Wangeline AL, Reeves FB (2007) Two new Alternaria species from selenium-rich habitats in the Rocky Mountain Front Range. Mycotaxon 99:83–89Google Scholar
  36. Wangeline AL, Valdez JR, Lindblom SD, Bowling KL, Reeves FB, Pilon-Smits EAH (2011) Selenium tolerance in rhizosphere fungi from Se hyperaccumulator and non-hyperaccumulator plants. Am J Bot 98:1139–1147PubMedCrossRefGoogle Scholar
  37. Xue T, Hartikainen H, Piironen V (2001) Antioxidant and growth-promoting effect of selenium on senescing lettuce. Plant Soil 237:55–61CrossRefGoogle Scholar
  38. Zarcinas BA, Cartwright B, Spouncer LR (1987) Nitric acid digestion and multi element analysis of plant material by inductively coupled plasmaspectrometry. Commun Soil Sci Plan Anal 18:131–146CrossRefGoogle Scholar
  39. Zhang Y, Gladyshev VN (2009) Comparative genomics of trace elements: emerging dynamic view of trace element utilization and function. Chem Rev 109:4828–4861PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Stormy Dawn Lindblom
    • 1
  • Sirine C. Fakra
    • 2
  • Jessica Landon
    • 1
  • Paige Schulz
    • 1
  • Benjamin Tracy
    • 1
  • Elizabeth A. H. Pilon-Smits
    • 1
  1. 1.Biology DepartmentColorado State UniversityFort CollinsUSA
  2. 2.Advanced Light SourceLawrence Berkeley National LaboratoryBerkeleyUSA

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