Skip to main content
SpringerLink
Log in

Relationship between the Ni hyperaccumulator Alyssum murale and the parasitic plant Orobanche nowackiana from serpentines in Albania

  • Special Feature
  • Ultramafic Ecosystems: Proceedings of the 9th International Conference on Serpentine Ecology
  • Published:
Ecological Research

Abstract

Orobanche nowackiana Markgr. is the only parasitic flowering plant in Europe which is an obligate serpentinophyte. This plant parasitizes the Ni hyperaccumulator Alyssum murale Waldst. & Kit. which grows in many areas including serpentine slopes of Mt. Komjan (Albania). The aims of the study were to investigate this host/parasite relationship from a biogeochemical point of view in order to evaluate: (1) the metal accumulation in different parts of the parasite and host plants and (2) the effect of Orobanche infection on host growth. Soil and plant samples of A. murale and O. nowackiana were analyzed for elemental concentrations after acid digestion using inductively coupled plasma atomic emission spectrometry (Ca, Mg, Fe, Ni, Cr, Co, Zn, Cu, Mn, Na, Al), colorimetry (for N and P), and flame photometry (for K). Individuals of A. murale, both infected and healthy, showed slight differences in their composition of essential elements (N, P, K) and of some micronutrients. The parasite had higher P, K, Na, and lower N, Ca, Mg, Ni, Zn, Co, Mn and Al concentrations than the host. Orobanche nowackiana is a Ni accumulator with 299 mg kg−1 in the leaves. Hyperaccumulation of Ni by A. murale did not prevent attack by O. nowackiana. After infection there was a decline in Ni concentration and the dry weight of all organs of the host, thus reducing the biomass yield and consequently Ni phytoextraction yield of A. murale. This infection could be a potential threat to the use of A. murale for Ni agromining.

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

Similar content being viewed by others

References

  • Andreev NI (1930) Orobanche on sunflower in Don and Armavir regions in 1927–28. Caucasus Plant Prot St Bull 6–7:173–184

    Google Scholar 

  • Baker AJM, Reeves RD, Hajar ASM (1994) Heavy metal accumulation and tolerance in British populations of the metallophyte Thlaspi caerulescens J. & C. Presl (Brassicaceae). New Phytol 127:61–68. https://doi.org/10.1111/j.1469-8137.1994.tb04259.x

    Article  CAS  Google Scholar 

  • Bani A (2018) Element case studies: Nickel. In: van der Ent A, Echevarria G, Baker AJM, Morel JL (eds) Agromining: farming for metals, mineral resource reviews. Springer International Publishing, New York. https://doi.org/10.1007/978-3-319-61899-9_12

    Chapter  Google Scholar 

  • Bani A, Echevarria G, Sulce S, Morel JL, Mullaj A (2007) In-situ phytoextraction of Ni by a native population of Alyssum murale on an ultramafic site (Albania). Plant Soil 293:79–89

    Article  CAS  Google Scholar 

  • Bani A, Echevarria G, Mullaj A, Reeves RD, Morel JL, Sulçe S (2009) Ni hyperaccumulation by Brassicaceae in serpentine soils of Albania and NW Greece. Northeast Nat 16:385–404

    Article  Google Scholar 

  • Bani A, Pavlova D, Echevarria G, Mullaj A, Reeves RD, Morel JL, Sulçe S (2010) Nickel hyperaccumulation by species of Alyssum and Thlaspi (Brassicaceae) from the ultramafics of Balkans. Botanica Serbica 34:3–14

    Google Scholar 

  • Bani A, Imeri A, Echevarria G, Pavlova D, Reeves RD, Morel JL, Sulçe S (2013) Nickel hyperaccumulation in the serpentine flora of Albania. Fresenius Environ Bull 22:1792–1801

    CAS  Google Scholar 

  • Bani A, Echevarria G, Montarges-Pelletier E, Gjoka F, Sulce S, Morel JL (2014) Pedogenesis and nickel biogeochemistry in a typical Albanian ultramafic toposequence. Environ Monit Assess 186:4431–4442. https://doi.org/10.1007/s10661-014-3709-6

    Article  PubMed  CAS  Google Scholar 

  • Bani A, Echevarria G, Zhang X, Laubie B, Morel JL, Simonnot MO (2015a) The effect of plant density in nickel phytomining field experiments with Alyssum murale in Albania. Aust J Bot 63:72–77. https://doi.org/10.1071/BT14285

    Article  CAS  Google Scholar 

  • Bani A, Echevarria G, Sulçe S, Morel JL (2015b) Improving the agronomy of Alyssum murale for extensive phytomining: a five-year field study. Int J Phytoremediat 17:117–127. https://doi.org/10.1080/15226514.2013.862204

    Article  CAS  Google Scholar 

  • Barina Z, Pifko D (2008) Additions and amendments to the flora of Albania. Willdenowia 38:455–464. https://doi.org/10.3372/wi.38.38206

    Article  Google Scholar 

  • Barker ER, Press MC, Scholes JD, Quick WP (1996) Interactions between the parasitic angiosperm Orobancheae aegyptiaca and its tomato host: growth and biomass allocation. New Phytol 133:637–642. https://doi.org/10.1111/j.1469-8137.1996.tb01932.x

    Article  Google Scholar 

  • Boyd RS, Martens NS, Davis MA (1999) The nickel hyperaccumulator Streptanthus polygaloides (Brassicaceae) is attacked by the parasitic plant Cuscuta californica (Cuscutaceae). Madrono 46:92–99

    Google Scholar 

  • Brooks RR (1987) Serpentine and its vegetation: a multidisciplinary approach. Dioscorides Press, Portland

    Google Scholar 

  • Coic Y, Lesaint G, Jean MG (1965) Sur la composition minerale des especes et organes vegetaux et leur determinism. Ann Physiol Veg (Paris) 5:293–301 (In French with English summary)

    Google Scholar 

  • Delavault P (2015) Knowing the parasite: biology and genetics of Orobanche. Helia 38:15–29. https://doi.org/10.1515/helia-2014-0030

    Article  Google Scholar 

  • Echevarria G (2018) Chapter 8: genesis and behaviour of ultramafic soils and consequences for nickel biogeochemistry. In: van der Ent A, Echevarria G, Baker AJM, Morel JL (eds). Agromining: farming for metals, mineral resource reviews. Springer International Publishing. Germany, In Press. https://doi.org/10.1007/978-3-319-61899-9_8

  • Echevarria G, Morel JL, Fardeau JC, Leclerc-Cessac E (1998) Assessment of phytoavailability of nickel in soils. J Environ Qual 27:1064–1070. https://doi.org/10.2134/jeq1998.00472425002700050011x

    Article  CAS  Google Scholar 

  • Echevarria G, Massoura ST, Sterckeman T, Becquer T, Schwartz C, Morel JL (2006) Assessment and control of the bioavailability of nickel in soils. Environ Toxicol Chem 25:643–651. https://doi.org/10.1897/05-051R.1

    Article  PubMed  CAS  Google Scholar 

  • Edmondson JR (1992) Review of recent taxonomic work on European serpentinicolous phanerogams. In: Baker AJM, Proctor J, Reeves RD (eds) The vegetation of ultramafic (serpentine) soils. Intercept, Andover, Hampshire, UK

    Google Scholar 

  • Estrade N, Cloquet C, Echevarria G, Sterckeman T, Deng THB, Tang YT, Morel JL (2015) Weathering and vegetation controls on nickel isotope fractionation in surface ultramafic environments (Albania). Earth Planet Sci Lett 423:24–25

    Article  CAS  Google Scholar 

  • Fernández-Aparicio M, Flores F, Rubiales D (2016) The effect of Orobanche crenata infection severity in Faba bean, Field Pea, and Grass Pea productivity. Front Plant Sci 7:1–8. https://doi.org/10.3389/fpls.2016.01409

    Article  Google Scholar 

  • Foley MJY (2000) The taxonomic position of Orobanche rechingeri Gilli (Orobanchaceae) in relation to Orobanche nowackiana Markgr. Candollea 55:269–276

    Google Scholar 

  • Gevezova M, Dekalska T, Stoyanov K, Ts Hristeva, Kostov K, Batchvarova R, Denev I (2012) Recent advances in Broomrapes research. J BioSci Biotech 1:91–105

    Google Scholar 

  • Harrison S, Rajakaruna N (2011) Serpentine: the evolution and ecology of a model system. University of California Press, Berkeley

    Google Scholar 

  • Hartvig P (1991) Orobanche. In: Strid A, Tan K (eds) Mountain Flora of Greece, vol 2. Edinburgh University Press, Edinburgh

    Google Scholar 

  • Hibberd JM, Quick WP, Press MC, Scholes JD, Jeschke WD (1999) Solute fluxes from tobacco to the parasitic angiosperm Orobanche cernua and the influence of infection on host carbon and nitrogen relations. Plant Cell Environ 22:937–947

    Article  CAS  Google Scholar 

  • ISO 11261 (1995/2016) Soil quality-determination of total nitrogen–modified Kjeldahl method, determination of calcium and magnesium in soil extracts by flame atomic absorption spectrophotometry (FAAS)

  • ISO 9964-3 (1993/2014) Water quality-determination of sodium and potassium-flame emission spectrometric method; LNO168/10/1 Fred Kruis Environmental Chemistry-Selected methods for Water Quality Analysis

  • Kabata-Pendias A, Pendias H (1984) Trace elements in soils and plants. CRC Press, Boca Raton

    Google Scholar 

  • Kroschel J (2001) A technical manual of parasitic weed Research and Extension. Kluwer Academic Publishers, Dordrecht

    Book  Google Scholar 

  • Kuijt J (1969) The biology of parasitic flowering plants. University of California Press, Berkeley

    Google Scholar 

  • Labrousse P, Delmail D, Arnaud MC, Thalouarn P (2010) Mineral nutrient concentration influences sunflower infection by broomrape (Orobanche cumana). Botany 88:839–849

    Article  CAS  Google Scholar 

  • Lindsay WL, Norvell WA (1978) Development of DTPA soil test for zinc, iron, manganese, and copper. Soil Sci Soc Am J 42:421–428

    Article  CAS  Google Scholar 

  • Lombini A, Dinelli E, Ferrari C, Simoni A (1998) Plant-soil relationships in the serpentinite screes of Mt Prinzera (Northern Appenines, Italy). J Geochem Explor 64:19–33

    Article  CAS  Google Scholar 

  • Manceau A, Boisset MC, Sarret G, Hazemann JL, Mench M, Cambier P, Prost R (1996) Direct determination of lead speciation in contaminated soils by EXAFS spectroscopy. Environ Sci Technol 30:540–1552

    Article  Google Scholar 

  • Markgraf F (1926) Bemerkenswerte neue Pflanzenarten aus Albanien. Ber Deutsch Bot Ges 44:420–432 (In German)

    Google Scholar 

  • Mauromicale G, Lo Monaco A, Longo AMG (2008) Effect of Branched Broomrape (Orobanche ramosa) infection on the growth and photosynthesis of tomato. Weed Sci 56:574–581

    Article  CAS  Google Scholar 

  • McNear DH, Peltier E, Everhart J, Chaney RL, Sutton S, Newville M, Rivers M, Sparks DL (2005) Application of quantitative fluorescence and absorption-edge computed microtomography to image metal compartmentalizationin Alyssum murale. Environ Sci Technol 39:2210–2218

    Article  PubMed  CAS  Google Scholar 

  • Mullaj A, Shehu J, Tan K, Imeraj A (2010) New records for the Albanian flora. Botanica Serbica 34:163–167

    Google Scholar 

  • Nkrumah PN, Baker AJM, Chaney RL, Erskine PD, Echevarria G, Morel J-L, van der Ent A (2016) Current status and challenges in developing nickel phytomining: an agronomic perspective. Plant Soil 406:55–69. https://doi.org/10.1007/s11104-016-2859-4

    Article  CAS  Google Scholar 

  • O’Dell RE, Claassen VP (2011) Restoration and revegetation of harsh soils. In: Harrison SP, Rajakaruna N (eds) Serpentine: the evolution and ecology of a model system. University of California Press, Berkeley, pp 383–413

    Google Scholar 

  • Pr-EN 14672 (2005) Characterization of sludges-determination of total phosphorus; ISO 6878:2004 Water quality-determination of phosphorus-ammonium molybdate spectrometric method; LNO168/10/1 Fred Kruis environmental chemistry-selected methods for water quality analysis

  • Pr-EN 16169 (2011E) Sludge, treated biowaste and soil-determination of Kjeldahl nitrogen; ISO 7150:1984- Water quality-determination of ammonium-manual spectrometric method; LNO168/10/1 Fred Kruis Environmental chemistry selected methods for water quality analysis

  • Press MC, Graves JD, Stewart GR (1990) Physiology of the interaction of angiosperm parasites and their higher plant hosts. Plant Cell Environ 13:91–104

    Article  Google Scholar 

  • Reeves RD (1992) The hyperaccumulation of nickel by serpentine plants. In: Baker AJM, Proctor J, Reeves RD (eds) The vegetation of ultramafic (Serpentine) Soils. Intercept Ltd., Andover, pp 253–277

    Google Scholar 

  • Reeves RD (2006) Hyperaccumulation of trace elements by plants. In: Morel JL, Echevarria, Goncharova N (ed) Phytoremediation of Metal-Contaminated Soils. NATO Science Series (IV) Earth Environ Sci 68:25–52

  • Reeves RD, Baker AJM, Kelepertsis A (1997) The distribution and biogeochemistry of some serpentine plants of Greece. In: Jaffré T, Reeves RD, Becquer T (eds) Écologie des milieux sur roches ultramafiques et sur sols métallifères, Documents Scientifiques et Techniques, III/2. ORSTOM, Nouméa, New Caledonia, pp 205–207 

    Google Scholar 

  • Shallari S, Echevarria G, Schwartz C, Morel JL (2001) Availability of nickel in soils for the hyperaccumulator Alyssum murale Waldst. & Kit. S Afr J Sci 97:568–570

    CAS  Google Scholar 

  • Singh JH, Rai TB (1971) Studies on the physiology of host-parasite relationship in Orobanche. II. Growth and mineral nutrition of host and parasite. Physiol Plant 25:425–431

    Article  CAS  Google Scholar 

  • Stevanović V, Tan K, Iatrou G (2003) Distribution of the endemic Balkan flora on serpentine I.—obligate serpentine endemics. Plant Syst Evol 242:149–170. https://doi.org/10.1007/s00606-003-0044-8

    Article  Google Scholar 

  • Uhlich H, Pusch J, Barthel K (1995) Die Sommerwurzarten Europas. Westarp Wissenschaften, Magdeburg

    Google Scholar 

  • van der Ent A, Baker AJM, Reeves RD, Chaney RL (2015) Agromining: farming for metals in the future? Environ Sci Technol 49:4773–4780

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We would like to acknowledge the technical team of “Laboratoire Sols et Environnement”, Nancy, France. The authors also wish to thank Prof. Dr. Alfred Mullaj for help with identifying the sampling area of Orobanche nowackiana.

Author information

Authors and Affiliations

  1. Environmental Department, Faculty of Agronomy and Environment, Agricultural University of Tirana, Koder-Kamez, Tirane, Albania

    Aida Bani, Seit Shallari & Liri Miho

  2. Department of Botany, Faculty of Biology, University of Sofia, bulvd. Dragan Tzankov 8, 1164, Sofia, Bulgaria

    Dolja Pavlova

  3. Laboratoire Sols et Environnement, Université de Lorraine-INRA, 2, Avenue de la Foret de Haye BP 20163, 54505, Vandoeuvre-Lès-Nancy Cedex, France

    Emile Benizri & Guillaume Echevarria

  4. Department of Biology, Faculty of Natural Science, University of Tirana, Bulevardi Zogu I, Tirane, Albania

    Marjol Meco

  5. Department of Economy and Agrarian Policy, Faculty of Economy and Agribusiness, Agricultural University of Tirana, Koder-Kamez, Tirane, Albania

    Edmira Shahu

  6. Palmerston North, New Zealand

    Roger Reeves

Authors
  1. Aida Bani
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dolja Pavlova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Emile Benizri
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Seit Shallari
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Liri Miho
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Marjol Meco
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Edmira Shahu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Roger Reeves
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Guillaume Echevarria
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Aida Bani.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bani, A., Pavlova, D., Benizri, E. et al. Relationship between the Ni hyperaccumulator Alyssum murale and the parasitic plant Orobanche nowackiana from serpentines in Albania. Ecol Res 33, 549–559 (2018). https://doi.org/10.1007/s11284-018-1593-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11284-018-1593-1

Keywords

Search

Navigation