ISSN 1021-4437, Russian Journal of Plant Physiology, 2013, Vol. 60, No. 5, pp. 623–632. © Pleiades Publishing, Ltd., 2013.
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INTRODUCTION
Tribulus terrestris L. is a flowering plant of the fam-
ily Zygophyllaceae, native to warm temperate and
tropical regions of the Old World in southern Europe,
southern Asia, throughout Africa, and Australia.
T. terrestris plant extracts contain saponins, fla-
vonoids, amides, and alkaloids [1]. The biologically
active furostanol saponin fraction of this plant finds
application in the contemporary medicine as a com-
1
This text was submitted by the authors in English.
ponent of drugs effective in treatment impotence and
other sexual disorders [2].
T. terrestris grown on industrially polluted soil
showed good ability for Cd, Pb, and Zn accumulation
and could be used for phytoremediation of polluted
soils [3]. The plant biomass production and the heavy
metal (HM) concentration in the harvestable biomass
are important factors for the practical efficiency of
phytoextraction [4]. One strategy to achieve the higher
HM removal efficiency is to enhance the concentra-
tions of soluble HMs in the soil with the application of
complexing agents [5]. EDTA is widely investigated
due to its high complexing capability towards Pb, Cu,
Cd, and Zn. That leads to an increase in the metal
uptake by plants like Brassica juncea, Helianthus
annuus, and Zea mays [6]. The medicinal plants could
be grown as alternatives to edible crops in HM-pol-
luted agricultural soils, because possess a significant
EDTA Reduces Heavy Metal Impacts on Tribulus terrestris
Photosynthesis and Antioxidants
1
Y. Markovska
a
, M. Geneva
b
, P. Petrov
b
, M. Boychinova
b
, I. Lazarova
c
, I. Todorov
b
, and I. Stancheva
b
a
Faculty of Biology, Sofia University “St. Kliment Ohridski”, 8 D. Tzankov Blvd., 1164 Sofia, Bulgaria
b
Department of Plant Mineral Nutrition and Water Relation, Institute of Plant Physiology and Genetics,
Bulgarian Academy of Sciences, Acad. G. Bonchev str., Bl. 21, 1113 Sofia, Bulgaria;
fax- +359-2-873-9952, e-mail: ira_stancheva@abv.bg
c
Faculty of Pharmacy, Department of Chemistry, Medical University of Sofia, Bulgaria
Received August 21, 2012
Abstract—The effects of EDTA application to heavy metal-polluted soil on phytoextraction of heavy metals,
leaf anatomy, gas exchange parameters, enzyme activities of C4 carbon cycle, antioxidant defense, and active
compounds of Tribulus terrestris L. were evaluated. The addition of EDTA to the soil polluted with Cd and
Pb markedly increased dry weight and Pb, Zn, and Cd contents in shoots. Plants responded to the action of
EDTA by an increased stomatal conductance, photosynthetic and transpiration rates, water use efficiency,
chlorophyll and carotenoid contents. The activities of C4 carbon cycle enzymes simultaneously increased,
thus concentrating CO
2
for enhanced CO
2
assimilation and providing NADPH for the antioxidant system.
Antioxidants, such as ascorbate, reduced glutathione, and flavonoids, increased more in the shoots of T. ter-
restris after the addition of EDTA. The activities of guaiacol peroxidase, catalase, and the enzymes of the
ascorbate–glutathione cycle enhanced significantly in the presence of EDTA. Increased activities of antiox-
idant enzymes suggest that they have some additive functions in the mechanism of metal tolerance. EDTA
application lowered the activity of phenylalanine ammonia-lyase and the content of total phenols, MDA,
hydrogen peroxide, dehydroascorbate, and lipid-soluble antioxidant capacity expressed as α-tocopherol.
Increased levels of total radical-scavenging activity are in correspondence with the activity of water-soluble
antioxidant compounds in T. terrestris tissues. The content of furostanol saponins protodioscin, protot-
ribestin, and rutin increased as a result of EDTA addition. The results obtained allowed us to assume that
applied EDTA reduced a negative heavy metal impact on puncture vine photosynthesis and antioxidant
potential.
Keywords: Tribulus terrestris, C4 carbon cycle enzymes, EDTA, heavy metals, leaf anatomy, antioxidant
capacity, furostanol saponins
DOI: 10.1134/S1021443713050117
Abbreviations: AGC—ascorbate–glutathione cycle; ASC—
ascorbic acid; CAT—catalase; DHASC—dehydroascorbic acid;
GPX—glutathione peroxidase; GR—glutathione reductase;
GSH—reduced; GSSG—oxidized glutathione, GST—glu-
tathione S-transferase; HM—heavy metal; NADP-ME—
NADP-malic enzyme; PAL—phenylalanine ammonia-lyase;
PEPC—phosphoenolpyruvate carboxylase; PPDK—pyruvate
orthophosphate dikinase; SOD—superoxide dismutase.
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