Skip to main content
SpringerLink
Log in

Possible reasons for tolerance to mercury of Lupinus albus cv. G1 inoculated with Hg-resistant and sensitive Bradyrhizobium canariense strains

  • Published:
Symbiosis Aims and scope Submit manuscript

Abstract

Inoculation with a mercury (Hg)-resistant Bradyrhizobium canariense strain (L7AH) confers on Lupinus albus the ability to grow under high concentrations of Hg and to accumulate this heavy metal. To elucidate the mechanism/s implicated in the acquisition of this tolerance, lupins were inoculated with resistant (L7AH) and sensitive (L3) strains and fed with different Hg solutions (0–200 μM HgCl2). Mercury application resulted in cellular alterations in leaves and nodules, depending on the strain inoculated. Mesophyll cell chloroplasts from L7AH-inoculated plants treated with Hg showed similar structure to those in control plants, while those of L3-inoculated plants treated with Hg showed a large increase in the number and size of starch granules. This resulted in a large increase in chloroplast and cell size which produced altered grana distribution with a totally disorganized thylakoid structure and clear signs of degradation. The preservation of the distribution and morphology of chloroplasts in L7AH-inoculated plants may be a reason why the photosynthetic efficiency remained unchanged even after treatment with 200 μM of Hg. Mercury exposure produced changes in L3-infected nodule ultrastructure, with evident signs of degradation, especially in bacteroids. However, only slight alterations of nodule morphology were noticed in L7AH-infected nodules. X-ray microanalysis showed that, while Hg was present in the nodules formed by L3, in both cortex and infected zone, in those formed by L7AH only low levels of Hg in the outermost layers of the cortex were detected. The exclusion of Hg from the infected zone together with the conservation of the symbiosome structure in nodules from L7AH-inoculated plants may explain the maintenance of nitrogenase activity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Bethlenfalvay GJ, Phillips DA (1978) Interactions between symbiotic nitrogen fixation, combined-N application and photosynthesis in Pisum sativum. Physiol Plant 42:119–123

    Article  CAS  Google Scholar 

  • Cakmak I (2000) Role of zinc in protecting plant cells from reactive oxygen species. New Phytol 146:185–205

    Article  CAS  Google Scholar 

  • Carpena R, Vázquez S, Esteban E, Fernández-Pascual M, de Felipe MR, Zornoza P (2003) Cadmium-stress in white lupin: effects on nodule structure and functioning. Plant Physiol Biochem 41:911–919

    Article  CAS  Google Scholar 

  • Chen J, Yang ZM (2012) Mercury toxicity, molecular response and tolerance in higher plants. Biometals 25:847–857

    Article  CAS  PubMed  Google Scholar 

  • de Felipe MR, Fernández-Pascual M, Pozuelo JM (1987) Effects of the herbicides lindex and simazine on chloroplast and nodule development, nodule activity and grain yield in Lupinus albus L. Plant Soil 101:99–105

    Article  Google Scholar 

  • de Lorenzo C, Fernández-Pascual M, de Felipe MR (1994) Protective enzymes against active oxygen species during nitrate-induced senescence of Lupinus albus nodules. J Plant Physiol 144:633–640

    Article  Google Scholar 

  • de Lorenzo C, Fernández-Pascual M, de Felipe MR (1998) Subcellular localization of glycoprotein epitopes during the development of lupin root nodules. Protoplasma 201:71–84

    Article  Google Scholar 

  • de María N, de Felipe MR, Fernández-Pascual M (2005) Alterations induced by glyphosate on lupin photosynthetic apparatus and nodule ultrastructure and some oxygen diffusion related proteins. Plant Physiol Biochem 43:985–996

    Article  PubMed  Google Scholar 

  • de María N, Guevara A, Serra MT, García-Luque I, González A, de Felipe MR, Fernández-Pascual M (2007) Putative porin of Bradyrhizobium sp. (Lupinus) bacteroids induced by glyphosate. Appl Environ Microbiol 73:5075–5082

    Article  PubMed Central  PubMed  Google Scholar 

  • Esteban E, Moreno E, Peñalosa J, Cabrero José I, Millan R, Zornoza P (2008) Short and long-term uptake of Hg in white lupin plants: kinetics and stress indicators. Environ Exp Bot 62:316–322

    Article  CAS  Google Scholar 

  • Fedorova E, Redondo FJ, Koshiba T, de Felipe MR, Pueyo JJ, Lucas MM (2005) Aldehyde oxidase (AO) in the root nodules of Lupinus albus and Medicago truncatula: identification of AO in meristematic and infection zones. Mol Plant-Microbe Interact 18:405–413

  • Fernández-Pascual M, Serra MT, Pozuelo JM, de Felipe MR (1988) Effects of cianazine and linuron on chloroplast development, nodule activity and protein metabolism in Lupinus albus L. J Plant Physiol 133:288–294

    Article  Google Scholar 

  • Fernández-Pascual M, de Lorenzo C, Pozuelo JM, de Felipe MR (1992) Alterations induced by four herbicides on lupin nodule cortex structure, protein metabolism and some senescence-related enzymes. J Plant Physiol 140:385–390

    Article  Google Scholar 

  • Fernández-Pascual M, de Lorenzo C, de Felipe MR, Rajalakshmi S, Gordon AJ, Thomas BJ, Minchin FR (1996) Possible reasons for relative salt stress tolerance in nodules of white lupin cv. Multolupa. J Exp Bot 47:1709–1716

    Article  Google Scholar 

  • Ge C, Ding Y, Wang Z, Wan D, Wang Y, Shang Q, Luo S (2009) Responses of wheat seedlings to cadmium, mercury and trichlorobenzene stresses. J Environ Sci 21:806–813

    Article  CAS  Google Scholar 

  • Geigenberger P (2011) Regulation of starch biosynthesis in response to a fluctuating environment. Plant Physiol 155:1566–1577

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • González-Sama A, Lucas MM, de Felipe MR, Pueyo JJ (2004) An unusual infection mechanism and nodule morphogenesis in white lupin (Lupinus albus). New Phytol 163:371–338

    Article  Google Scholar 

  • Hernández-Jiménez MJ, Lucas MM, de Felipe MR (2002) Antioxidant defense and damage in senescing lupin nodules. Plant Physiol Biochem 40:645–657

    Article  Google Scholar 

  • Hess FD (1980) Influence of specimen topography on microanalysis. In: Hayat, M.A. (Ed) X-Ray Microanalysis in Biology. Macmillan publishers LTD, London 241–261

  • Humme E, Osterrieder A, Robinson DG, Hawes C (2010) Inhibition of Golgi function causes plastid starch accumulation. J Exp Bot 61:2603–2614

    Article  Google Scholar 

  • Iovdijova A, Bencko V (2010) Potential risk of exposure to selected xenobiotic residues and their fate in the food chain - part I: classification of xenobiotics. Ann Agric Environ Med 17:183–192

    CAS  PubMed  Google Scholar 

  • James EK, Minchin FR, Iannetta PPM, Sprent JI (1997) Temporal relationships between nitrogenase and intercellular glycoprotein in developing white lupin nodules. Ann Bot 79:493–503

    Article  CAS  Google Scholar 

  • Minchin FR, Pate JS (1973) Carbon balance of a legume and functional economy of its root nodules. J Exp Bot 24:259--271

  • Montero-Palomero MB, Martín-Barranco A, Escobar C, Hernández LE (2014) Early transcriptional responses to mercury: a role for ethylene in mercury-induced stress. New Phytol 201:116–130

    Article  Google Scholar 

  • Nair S, Jha PK, Babu CR (1993) Variation in poly-β-hydroxybutyrate synthesis in rhizobia reflects strain differentiation and temperature regulation. J Basic Microbiol 33:35–39

    Article  CAS  Google Scholar 

  • Panou-Filotheou H, Bosabalidis AM, Karataglis S (2001) Effects of Cu toxicity on leaves of oregano (Origanum vulgare subsp. Hirtum). Ann Bot 88:207–214

    Article  CAS  Google Scholar 

  • Pastor J, Hernández AJ, Prieto N, Fernández-Pascual M (2003) Accumulating behaviour of Lupinus albus L. growing in a normal and a decalcified calcic luvisol polluted with Zn. J Plant Physiol 160:1455–1463

    Article  Google Scholar 

  • Quartacci MF, Pinzino C, Sgherri CLM, Dalla VF, Navari-Izzo F (2000) Growth in excess copper induces changes in the lipid composition and fluidity of PSII-enriched membranes in wheat. Physiol Plant 108:87–93

    Article  CAS  Google Scholar 

  • Quiñones MA, Ruiz-Díez B, Fajardo S, López-Berdonces MA, Higueras PL, Fernández-Pascual M (2013) Lupinus albus plants acquire mercury tolerance when inoculated with an Hg-resistant Bradyrhizobium strain. Plant Physiol Biochem 73:168–175

    Article  PubMed  Google Scholar 

  • Rellán-Álvarez R, Ortega-Villasante C, Álvarez-Fernandez A, del Campo FF, Hernández LE (2006) Stress responses of Zea mays to cadmium and mercury. Plant Soil 279:41–50

    Article  Google Scholar 

  • Rodríguez L, Rincón J, Asencio I, Rodríguez-Castellanos L (2007) Capability of selected crop plants for shoot mercury accumulation from polluted soils: phytoremediation perspectives. Int J Phytorem 9:1–13

    Article  Google Scholar 

  • Ruiz-Díez B, Quiñones MA, Fajardo S, López MA, Higueras P, Fernández-Pascual M (2012a) Mercury-resistant rhizobial bacteria isolated from nodules of leguminous plants growing in high Hg-contaminated soils. Appl Microbiol Biotechnol 96:543–554

    Article  PubMed  Google Scholar 

  • Ruiz-Díez B, Fajardo S, de Felipe MR, Fernández-Pascual M (2012b) Characterization of rhizobia from legumes of agronomic interest grown in semi-arid areas of Central Spain relates genetic differences to soil properties. J Basic Microbiol 52:66–78

    Article  PubMed  Google Scholar 

  • Sánchez-Pardo B, Fernández-Pascual M, Zornoza P (2012) Copper microlocalisation, ultrastructural alterations and antioxidant responses in the nodules of white lupin and soybean plants grown under conditions of copper excess. Environ Exp Bot 8:52–60

    Article  Google Scholar 

  • Sánchez-Pardo B, Fernández-Pascual M, Zornoza P (2014) Copper microlocalisation and changes in leaf morphology, chloroplast ultrastructure and antioxidative response in white lupin and soybean grown in copper excess. J Plant Res 127:119–129

    Article  PubMed  Google Scholar 

  • Tang C, Robson AD, Dilworth MJ, Kuo J (1992) Microscopic evidence on how iron deficiency limits nodule initiation in Lupinus angustifolius L. New Phytol 121:457–467

    Article  CAS  Google Scholar 

  • Vázquez S, Fernández-Pascual M, Sánchez-Pardo B, Carpena R, Zornoza P (2007) Subcellular compartmentation study of cadmium in white lupin plants by energy dispersive X-ray microanalysis. J Plant Physiol 167:1235–1239

    Article  Google Scholar 

  • Wierzchos J, Ascaso C (1996) Morphological and chemical features of bioweathered granitic biotite induced by lichen activity. Clays Clay Miner 44:652–657

    Article  CAS  Google Scholar 

  • Zornoza P, Vázquez S, Esteban E, Fernández-Pascual M, Carpena R (2002) Cd-stress in nodulated white lupin: strategies to avoid toxicity. Plant Physiol Biochem 40:1003–1009

    Article  CAS  Google Scholar 

  • Zornoza P, Millán R, Sierra MJ, Seco A, Esteban E (2010) Efficiency of white lupin in the removal of mercury from contaminated soils: soil and hydroponic experiments. J Environ Sci 3:421–427

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by Junta de Comunidades de Castilla La-Mancha (POII10-0211-5015) and Ministerio de Economía y Competitividad (AGL2013-40758-R). BR-D was supported by the JCCL-M. The authors would like to thank Dr. F. Minchin for critical proof-reading of the manuscript. We thank V. Sousa-Egipsy for electron microscopy facilities.

Author information

Authors and Affiliations

  1. Instituto de Ciencias Agrarias, ICA-CSIC, C/ Serrano, 115 dpdo, 28006, Madrid, Spain

    Beatriz Ruiz-Díez, Miguel A. Quiñones, Susana Fajardo, César Morcillo & Mercedes Fernández-Pascual

Authors
  1. Beatriz Ruiz-Díez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Miguel A. Quiñones
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Susana Fajardo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. César Morcillo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mercedes Fernández-Pascual
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mercedes Fernández-Pascual.

Additional information

Highlights

Mercury causes serious damage to the ultrastructure of chloroplasts and symbiosomes of lupin when inoculated with an Hg-sensitive Bradyrhizobium strain.

Mercury causes slight damage to the ultrastructure of chloroplasts and symbiosomes of lupin inoculated with an Hg-resistant Bradyrhizobium strain.

Mercury penetrates into the infected zone of nodules when lupin is inoculated with a sensitive Bradyrhizobium strain.

Mercury remains in the outermost cells of the nodule cortex when lupin is inoculated with a resistant Bradyrhizobium strain.

The Hg-resistant Bradyrhizobium strain protects lupin plants from damage caused by Hg.

Electronic supplementary material

ESM 1

(PPT 5.77 mb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ruiz-Díez, B., Quiñones, M.A., Fajardo, S. et al. Possible reasons for tolerance to mercury of Lupinus albus cv. G1 inoculated with Hg-resistant and sensitive Bradyrhizobium canariense strains. Symbiosis 67, 91–102 (2015). https://doi.org/10.1007/s13199-015-0362-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13199-015-0362-y

Keywords

Search

Navigation