Environmental Science and Pollution Research

, Volume 25, Issue 2, pp 1319–1330 | Cite as

Different mechanisms of the metalliferous Zygophyllum fabago shoots and roots to cope with Pb toxicity

  • Antonio López-OrenesEmail author
  • Maria Celeste Dias
  • María Ángeles Ferrer
  • Antonio Calderón
  • José Moutinho-Pereira
  • Carlos Correia
  • Conceição Santos
Research Article


Lead (Pb) remains classified as a priority pollutant. Zygophyllum fabago is considered an early colonizer of heavy metal-polluted soils under semiarid conditions, but physiological mechanisms underlying this colonizing capacity remain unclear. In order to characterize Z. fabago plants’ performance on Pb-contaminated soils, we evaluated how Pb influenced root and shoot growth, carbon metabolism, and oxidative status. For that, 30-day-old seedlings from one population colonizing a mine tailing (“Mercader”) at Murcia (southeast Spain) were exposed to 500-μM Pb(NO3)2 for 1 week. Results showed that this high dose of Pb induced no plant mortality nor senescence, though promoting plant nanism. Besides the efficiency of roots to accumulate Pb, shoots also demonstrate a high efficiency to translocate and accumulate this metal. Pb exposure decreased Zn uptake to the aerial part and reduced net photosynthetic rate (A), RuBisCO activity, chlorophyll, and soluble sugar contents in shoots. Moreover, in shoots, Pb exposure increased the levels of O2 and decreased antioxidant capacity, culminating with a loss of cell membrane integrity (electrolyte leakage) and increased protein oxidation. Compared to controls, exposed roots had less Mn and Zn levels, and despite the rise in H2O2 levels, they were able to modulate non-protein thiols presenting a robust defense capacity. This capacity may support the roots’ ability to maintain cell membrane integrity (electrolyte leakage) with regard to control. Principal component analysis (PCA) contributed to elucidate how this species adjusts physiological mechanisms to cope with Pb toxicity, showing that roots and shoots evolved different antioxidant defenses, which demonstrates the importance of organ specificity in the response of Z. fabago to heavy metals.


Antioxidant capacity Metal stress Oxidative stress Photosynthesis 



net CO2 assimilation rate








dry weight






ferric reducing antioxidant power


fresh weight


hydroxycinnamic acids




soluble non-protein thiols


photosystem II


reactive oxygen species


superoxide dismutase


total antioxidant activity


total phenol content


Funding information

The authors thank the Spanish Government (projects CGL2006-11569 and CTM2011-23958) and the Fundación Séneca (project FB/23/FS/ 02) for financial support. A.L.-O. holds a grant from the MECD (AP2012-2559 and EST13/00414). Part of this work was carried out at the Instituto de Biotecnología Vegetal, Universidad Politécnica de Cartagena (UPCT). The Portuguese Foundation for Science and Technology (FCT) supported the post-doctoral fellowship of M.C. Dias (SFRH/BPD/100865/2014). This work was also financed by FCT/MEC through national funds and the co-funding by the FEDER, within the PT2020 Partnership Agreement and COMPETE 2020, within the project UID/BIA/04004/2013; FEDER/COMPETE/ POCI-POCI-01-0145-FEDER-006958, FCT project UID/AGR/04033, and UID/QUI/00062/2013, POCI/01/0145/FEDER/007265 and PT2020 UID/QUI/50006/2013.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interests.


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Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Antonio López-Orenes
    • 1
    • 2
    Email author
  • Maria Celeste Dias
    • 2
    • 3
  • María Ángeles Ferrer
    • 1
  • Antonio Calderón
    • 1
  • José Moutinho-Pereira
    • 4
  • Carlos Correia
    • 4
  • Conceição Santos
    • 5
  1. 1.Department of Agricultural Science and TechnologyUniversidad Politécnica de CartagenaCartagenaSpain
  2. 2.Department of Chemistry, QOPNAUniversity of AveiroAveiroPortugal
  3. 3.Centre for Functional Ecology (CEF), Department of Life ScienceUniversity of CoimbraCoimbraPortugal
  4. 4.Department of Biology and Environment, Centre for the Research and Technology of Agro-Environmental and Biological Sciences (CITAB)University of Trás-os-Montes e Alto DouroVila RealPortugal
  5. 5.Department of Biology, Faculty of Sciences, LAQV/REQUIMTEUniversity of PortoPortoPortugal

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