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Plant and Soil

, Volume 430, Issue 1–2, pp 205–217 | Cite as

Trapping of lead (Pb) by corn and pea root border cells

  • David A. Huskey
  • Gilberto Curlango-Rivera
  • Robert A. Root
  • Fushi Wen
  • Mary Kay Amistadi
  • Jon Chorover
  • Martha C. Hawes
Regular Article
  • 174 Downloads

Abstract

Aims

Most plants produce a root tip extracellular matrix that includes viable border cell populations programmed to disperse into soil. Like neutrophils, border cells export structures that trap pathogens and prevent root tip infection. Border cells also trap metals. The goal of this study was to determine if border cells trap Pb.

Methods

Border cell responses to Pb were observed microscopically. Border cell impact on Pb-induced injury to roots was assessed using root growth assays. Pb removal from solution was measured using inductively coupled plasma mass spectrometry (ICP-MS). Speciation of Pb associated with border cells was evaluated by synchrotron X-ray absorption spectroscopy (XAS).

Results

Increased border cell trap size and number occurred within minutes in response to Pb but not silicon (Si). Transient immersion of root tips into Pb after border cells were removed resulted in growth inhibition. Immersion of root tips and border cells into Pb solution resulted in significant removal of Pb. Si levels in the presence of root tips remained unchanged. The Pb speciation, measured with Pb LIII XAS, altered when reacted with border cells, indicating that direct binding by extracellular traps occurred.

Conclusions

Border cells can trap Pb and prevent damage to the root tip.

Keywords

Border cells Extracellular DNA traps Rhizosphere Root cap Rhizofiltration 

Abbreviations

exDNA

Extracellular DNA

ANOVA

Analysis of variance

DI

Deionized

Pb

Lead

ICP-MS

Inductively coupled plasma-mass spectrometry

Si

Silicon

Notes

Acknowledgements

Portions of this research were carried out at the Stanford Synchrotron Radiation Lightsource, a national user facility operated by Stanford University on behalf of the U.S. Department of Energy, Office of Basic Energy Sciences. The authors thank the reviewers of the manuscript for helpful suggestions to improve the presentation. The authors thank the College of Agriculture and Life Sciences and the Department of Soil, Water and Environmental Sciences at the University of Arizona, and the National Science Foundation (1032339) for their support of the research.

References

  1. Ashraf U, Kanu AS, Mo Z, Hussain S, Anjum SA, Khan I, Abbas RN, Tang X (2015) Lead toxicity in rice: effects, mechanisms, and mitigation strategies-a mini review. Environ Science and Pollution Res 22:18318–18332CrossRefGoogle Scholar
  2. Baetz U, Martinoia E (2014) Root exudates: the hidden part of plant defense. Trends Plant Sci 19:90–98CrossRefPubMedGoogle Scholar
  3. Barrow NJ (2017) The effects of pH on phosphate uptake from the soil. Plant Soil 410:401–410CrossRefGoogle Scholar
  4. Brigham LA, Woo HH, Wen F, Hawes MC (1998) Meristem-specific suppression of mitosis and a global switch in gene expression in the root cap of pea by endogenous signals. Plant Physiol 118:1223–1231CrossRefPubMedPubMedCentralGoogle Scholar
  5. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrach Y, Zychlinsky A (2004) Neutrophil extracellular traps kill bacteria. Science 303:1532–1535CrossRefPubMedGoogle Scholar
  6. Cai M, Zhang S, Xing C, Wang F, Wang N, Zhu I (2008) Developmental characteristics and aluminum resistance of root border cells in rice seedlings. Plant Sci 180:702–708CrossRefGoogle Scholar
  7. Curlango-Rivera G, Duclos DV, Ebolo JJ, Hawes MC (2010) Transient exposure of root tips to primary and secondary metabolites: impact on root growth and production of border cells. Plant Soil 332:267–275CrossRefGoogle Scholar
  8. Curlango-Rivera G, Huskey DA, Mostafa A, Kessler JO, Xiong Z, Hawes MC (2013) Intraspecies variation in cotton border cell production: rhizosphere microbiome implications. American J Botany 100:9–15CrossRefGoogle Scholar
  9. Fahr M, Laplaze L, Bendaou N, Hocher V, Mzibri ME, Bogusz D, Mouni A (2013) Effect of lead on root growth. Frontiers in Plant Sci 4:175–182CrossRefGoogle Scholar
  10. Gao X, Root RA, Farrell J, Ela W, Chorover J (2013) Effect of silicic acid on arsenate and arsenite retention mechanisms on 6-L ferrihydrite: a spectroscopic and batch adsorption approach. Appl Geochem 38:110–120CrossRefPubMedPubMedCentralGoogle Scholar
  11. Gramss G, Voigt K (2016) Gradual accumulation of heavy metals in an industrial wheat crop from uranium mine soil and the potential use of the herbage. Agriculture-Basel 6:51CrossRefGoogle Scholar
  12. Greaves MP, Darbyshire JF (1972) The ultrastructure of the mucilaginous layer on plant roots. Soil Biol Biochem 4:443–446CrossRefGoogle Scholar
  13. Griffin GJ, Hale MG, Shay FJ (1976) Nature and quantity of sloughed organic matter produced by roots of axenic peanut plants. Soil Biol Biochem 8:29–32CrossRefGoogle Scholar
  14. Gunawardena U, Rodriguez M, Straney D, Romeo JT, VanEtten HD, Hawes MC (2005) Tissue- specific localization of pea root infection by Nectria haematococca. Mechanisms and consequences. Plant Physiol 137:1363–1374CrossRefPubMedPubMedCentralGoogle Scholar
  15. Hamamoto L, Hawes MC, Rost TL (2006) The production and release of root cap border cells is a function of root apical meristem type in dicotyledonous angiosperm plants. Annals Bot 97:917–923CrossRefGoogle Scholar
  16. Hanc Y, Malecka A, Kutrowska A et al (2016) Direct analysis of elemental biodistribution in pea seedlings by LA-ICP-MS, EDX and confocal microscopy: imaging and quantification. Microchem J 128:305–311CrossRefGoogle Scholar
  17. Hashimito Y, Takaoka M, Shiota K (2011) Enhanced transformation of lead speciation in rhizosphere soils using phosphorus amendments and phytostabilization: an X-ray absorption fine structure spectroscopy investigation. J Environ Qual 40:696–703CrossRefGoogle Scholar
  18. Hawes MC, Pueppke S (1986) Sloughed peripheral root cap cells: and callus formation from single cells. American J Botany 73:1466–1473CrossRefGoogle Scholar
  19. Hawes MC, Brigham LA, Wen F, Woo HH, Zhu Y (1998) Function of root border cells in plant health: pioneers in the rhizosphere. Annu Rev Phytopathol 36:311–327CrossRefPubMedGoogle Scholar
  20. Hawes MC, Curlango-Rivera G, Wen F, White GJ, VanEtten HD, Xiong Z (2011) Extracellular DNA: the tip of root defenses? Plant Sci 180:141–145CrossRefGoogle Scholar
  21. Hawes MC, Curlango-Rivera G, Xiong Z, Kessler JO (2012) Roles of root border cells in plant defense and regulation of rhizosphere microbial populations by extracellular DNA ‘trapping. Plant Soil 355:1–16CrossRefGoogle Scholar
  22. Hawes MC, Wen F, Elquza E (2015) Extracellular DNA: a bridge to cancer. Cancer Res 75:1–5CrossRefGoogle Scholar
  23. Hawes MC, Allen C, Turgeon BG, Curlango-Rivera G, Tran MT, Huskey DA, Xiong Z (2016a) Root border cells and their role in plant defense. Annu Rev Phytopathol 54:1–19CrossRefGoogle Scholar
  24. Hawes MC, McLain J, Ramirez-Andreotta M, Curlango-Rivera G, Flores-Lara Y, Brigham LA (2016b) Extracellular trapping of soil contaminants by root border cells: new insights into plant defense. Agronomy 6:1–9CrossRefGoogle Scholar
  25. Hayes SM, Webb SM, Bargar JR, O'Day PA, Maier RM, Chorover J (2012) Geochemical weathering increases lead bioaccessibility in semi-arid mine tailings. Environ Science & Technology 6:5834–5841CrossRefGoogle Scholar
  26. Honeker LK, Root RA, Chorover J, Maier RM (2016) Resolving colocalization of bacteria and metal(loid)s on plant root surfaces by combining fluorescence in situ hybridization (FISH) with multiple-energy micro-focused X-ray fluorescence. J Microbiological Methods 131:23–33CrossRefGoogle Scholar
  27. Huang JW, Chen J, Cunningham SD (1997) Phytoextraction of lead from contaminated soils. Phytoremediation of Soil and Water Contaminants 664:283–298CrossRefGoogle Scholar
  28. Huang B, Zhu L, Liu XY, Zhang Y, Zhao N (2009) Individual and joint effects of lead and mercury on the viability of root border cells in mung bean (Vigna radiata). Progress in Environmental Science Technol II:254–258Google Scholar
  29. Huskey DA, Curlango-Rivera G, Root RA, Chorover J, Hawes MC (2017) Extracellular trapping of metals by plant root border cells. Keele Meeting Proceedings 12:25Google Scholar
  30. Iqbal M, Ahmad A, Ansari MKA, Qureshi MI, Aref IM, Khan PR, Hegazy SS, el-Atta H, Husen A, Hakeem KR (2015) Improving the phytoextraction capacity of plants to scavenge metal(loid)-contaminated sites. Environ Reviews 23:44–65CrossRefGoogle Scholar
  31. Jones DL, Nguyen C, Finlay RD (2009) Carbon flow in the rhizosphere: carbon trading at the soil- root interface. Plant Soil 321:5–33CrossRefGoogle Scholar
  32. Knox OGG, Gupta VSR, Nehl DB, Stiller WN (2007) Constitutive expression of cry proteins in roots and border cells of transgenic cotton. Euphytica 154:83–90CrossRefGoogle Scholar
  33. Knudson L (1919) Viability of detached root cap cells. American J Botany 6:309–310CrossRefGoogle Scholar
  34. Kreuzeder A, Santner J, Scharsching V, Oburger E, Hoefer C, Hann S, Wenzel WW (2018) In situ observation of localized, sub-mm scale changes of phosphorus biogeochemistry in the rhizosphere. Plant Soil 424:573–589.  https://doi.org/10.1007/s11104-017-3542-0 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Krzeslowska M (2011) The cell wall in plant cell response to trace metals: polysaccharide remodeling and its role in defense strategy. Acta Physiol Plant 33:35–51CrossRefGoogle Scholar
  36. Li X, Liu JY, Fang J et al (2017) Boron supply enhances aluminum tolerance in root border cells of pea (Pisum sativum) by interacting with cell wall pectins. Frontiers Plant Sci 8:2–9Google Scholar
  37. Lynch JM, Whipps JM (1990) Substrate flow in the rhizosphere. Plant Soil 129:1–10CrossRefGoogle Scholar
  38. Ma JF, Miyake Y, Takahashi E (2001) Silicon as a beneficial element for crop plants. Studies in Plant Science 8:17–39CrossRefGoogle Scholar
  39. Miyasaka S, Hawes MC (2001) Possible role of root border cells in detection and avoidance of aluminum toxicity. Plant Physiol 125:1978–1987CrossRefPubMedPubMedCentralGoogle Scholar
  40. Nguyen XV, Tran MH, Papenbrock J (2017) Different organs of Enhalus acoroides (Hydrocharitaceae) can serve as specific bioindicators for sediment contaminated with different heavy metals. South African J Botany 113:389–395CrossRefGoogle Scholar
  41. Odell RE, Dumlao MR, Samar D, Silk WK (2008) Stage-dependent border cell and carbon flow from roots to rhizosphere. American J Botany 95:441–446CrossRefGoogle Scholar
  42. Papayannopoulos V (2017) Neutrophil extracellular traps in immunity and disease. Nat Rev Immunol 18:134–147.  https://doi.org/10.1038/nri.2017.105 CrossRefPubMedGoogle Scholar
  43. Patra M, Bhowmik N, Bandopadhyay B, Sharma A (2004) Comparison of mercury, lead and arsenic with respect to genotoxic effects on plant systems and the development of genetic tolerance. Environ Exp Bot 52:199–223CrossRefGoogle Scholar
  44. Paull RE, Jones RL (1975) Studies on the secretion of root cap slime. Plant Physiol 56:307–312CrossRefPubMedPubMedCentralGoogle Scholar
  45. Peng C, Wang Y, Sun L, Xu C, Zhang L, Shi J (2016) Distribution and speciation of cu in the root border cells of rice by STXM combined with NEXAFS. Bull Environmental Contamination and Toxicology 96:408–414CrossRefGoogle Scholar
  46. Radmer L, Tesfaye M, Somers DA, Temple SJ, Vance CP, Samac DA (2012) Aluminum resistance mechanisms in oat (Avena sativa L.). Plant Soil 351:121–134CrossRefGoogle Scholar
  47. Ravel B, Newville M (2005) ATHENA, ARTEMIS, HEPHAESTUS: data analysis for X-ray absorption spectroscopy using IFEFFIT. J Synchrotron Radiation 12:537–541CrossRefGoogle Scholar
  48. Read DB, Gregory PJ (1997) Surface tension and viscosity of axenic maize and lupin root mucilages. New Phytol 37:623–628CrossRefGoogle Scholar
  49. Rehr JJ, Kas JJ, Prange MP, Sorini AP, Takimoto Y, Vila FD (2009) Ab initio theory and calculations of X-ray spectra. Comptes Rendus Physique 10:548–559CrossRefGoogle Scholar
  50. Rogers HT (1942) The source and phosphatase activity of exoenzyme systems of corn and tomato roots. Soil Sci 54:353–366CrossRefGoogle Scholar
  51. Ruangdech T, Wongphatcharachai M, Staley C, Sadowsky MJ, Sajjaphanc K (2017) Influence of heavy metals on rhizosphere microbial communities of Siam weed (Chromolaena odorata (L.) using a 16S rRNA gene amplicon sequencing approach. Agriculture and Natural Resources 51:137e141Google Scholar
  52. Saifullah ME, Qadir M et al (2009) EDTA-assisted Pb phytoextraction. Chemosphere 74:1279–1291CrossRefPubMedGoogle Scholar
  53. Samardakiewicz S, Krzesłowska M, Bilski H. Bartosiewicz R, Woźny A (2012) Is callose a barrier for lead ions entering Lemna minor L. root cells? Protoplasma 249:347–351Google Scholar
  54. Sobotik M, Ivanov VB, Obroucheva NV, Seregin IV, Ml M, Antipova OV, Bergmann H (1998) Barrier role of root system in lead-exposed plants. Journal Applied Botany 72:144–148Google Scholar
  55. Solis-Dominguez FA, White SA, Hutter TB, Amistadi MK, Root RA, Chorover J, Mayer RM (2012) Response of key soil parameters during compost-assisted phytostabilization in extremely acidic tailings: effect of plant species. Environ Science & Technology 46:1019–1027CrossRefGoogle Scholar
  56. Srimake M, Miyasaka SC (2015) Evaluation of aluminum sensitivity in barrel medic germplasm. J Am Society for Hort Sci 141:249–255Google Scholar
  57. Stephen J, Scales HE, Benson RA, Erben D, Garside P (2017) Brewer JM (2017) neutrophil swarming and extracellular trap formation play a significant role in alum adjuvant activity. Nature Partner Journals Vaccines 2:1PubMedGoogle Scholar
  58. Sun L et al (2015) Mechanistic study of programmed cell death of root border cells of cucumber (Cucumber sativus L.) induced by copper. Plant Physiol Biochem 96:412–419CrossRefGoogle Scholar
  59. Tollefson SJ, Curlango-Rivera G, Huskey DA, Pew T, Giacomelli G, Hawes MC (2015) Altered carbon delivery from roots: rapid, sustained inhibition of border cell dispersal in response to compost water extracts. Plant Soil 389:145–156CrossRefGoogle Scholar
  60. Tran TM, MacIntyre A, Hawes M, Allen C (2016) Escaping underground nets: extracellular DNases degrade plant extracellular traps and contribute to virulence of the plant pathogenic bacterium Ralstonia solanacearum. PLoS Pathog 12(6):e1005686CrossRefPubMedPubMedCentralGoogle Scholar
  61. Trebolazabala J, Maguregui M, Morillas H, García-Fernandez Z, de Diego A, Madariaga JM (2017) Uptake of metals by tomato plants (Solanum lycopersicum) and distribution inside the plant: field experiments in Biscay (Basque Country). J Food Composition and Analysis 59:161–169CrossRefGoogle Scholar
  62. Van Egeraat AWSM (1975) Exudation of ninhydrin-positive compounds by pea seedling roots: a study of the sites of exudation and of the composition of the exudate. Plant Soil 42:37–47Google Scholar
  63. Watson BS, Bedair MF, Urbanczyk-Wochniak E, Huhman DV, Yang DS, Allen SN, Li W, Tang Y, Sumner LW (2015) Integrated metabolomics and transcriptomics reveal enhanced specialized metabolism in Medicago truncatula root border cells. Plant Physiol 167:1699–1716CrossRefPubMedPubMedCentralGoogle Scholar
  64. Webb SM (2005) SIXpack: a graphical user interface for XAS analysis using IFEFFIT. Phys Scripta T115:1011–1014CrossRefGoogle Scholar
  65. Wen F, VanEtten HD, Tsaprailis G, Hawes MC (2007) Extracellular proteins in pea root tip and border cell exudates. Plant Physiol 43:773–783Google Scholar
  66. Wen F, White GA, Xiong Z, VanEtten HD, Hawes MC (2009) Extracellular DNA is required for root tip resistance to fungal infection. Plant Physiol 151:820–829CrossRefPubMedPubMedCentralGoogle Scholar
  67. Wen F, Curlango-Rivera G, Huskey DA, Xiong X (2017) Visualization of extracellular DNA released during border cell separation from the root cap. American J Botany 104:1–9CrossRefGoogle Scholar
  68. Yang J, Qu M, Fang J, Shen RF, Feng YM, Liu JY, Bian JF, Wu LS, He YM, Yu M (2016) Alkali-soluble pectin is the primary target of aluminum immobilization in root border cells of pea (Pisum sativum). Frontiers in Plant Science 7:1–7Google Scholar
  69. Zhao X, Misaghi IJ, Hawes MC (2000) Stimulation of border cell production in response to increased carbon dioxide levels. Plant Physiol 122:181–188CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • David A. Huskey
    • 1
  • Gilberto Curlango-Rivera
    • 1
  • Robert A. Root
    • 1
  • Fushi Wen
    • 1
  • Mary Kay Amistadi
    • 1
    • 2
  • Jon Chorover
    • 1
    • 2
  • Martha C. Hawes
    • 1
  1. 1.Department of Soil, Water and Environmental ScienceUniversity of ArizonaTucsonUSA
  2. 2.Arizona Laboratory for Emerging ContaminantsUniversity of ArizonaTucsonUSA

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