Abstract
The effects of soil and water contamination by lead (Pb) and the consequences on plant growth and yield are of great concern worldwide. Limits of the Pb concentration in water have been established by governmental institutions but these differ from each other. In this study, Lactuca sativa (var. Reine de Mai) plants were exposed to low Pb(NO3)2 doses (0.05–20 mg L−1), including the recommended limit values for irrigation water by the Food and Agriculture Organization (FAO). After 28 d of exposure, lettuce plants did not present visible morphological alterations or growth impairment, but CO2 assimilation rate (P N), photochemical quenching, and effective quantum efficiency of PSII were negatively affected, while intercellular CO2 concentration, stomatal conductance, or transpiration rate were not influenced. Our results suggested that limitations on photosynthesis occurred from different reasons than due to the decrease of internal CO2 availability, alterations of photophosphorylation, and/or electron transport rate. Thus, this lettuce cultivar showed photosynthetic susceptibility to low doses of Pb, even at lower concentrations than those maximal allowed for irrigation water by FAO. Furthermore, P N seemed to be the most sensitive biomarker for evaluation of Pb susceptibility.
Similar content being viewed by others
Abbreviations
- Chl:
-
chlorophyll
- C i :
-
intercellular CO2 concentration
- DM:
-
dry mass
- ETR:
-
electron transport rate
- F:
-
steady-state fluorescence
- F0 :
-
minimal fluorescence yield of the dark-adapted state
- FAO:
-
Food and Agriculture Organization
- FM:
-
fresh mass
- Fm :
-
maximal fluorescence yield of the dark-adapted state
- Fm':
-
maximal fluorescence yield of the light-adapted state
- Fv/Fm :
-
maximum photochemical efficiency of PSII
- g s :
-
stomatal conductance
- LS:
-
leaf succulence
- NPQ:
-
nonphotochemical quenching
- P N :
-
net photosynthetic rate
- qP :
-
photochemical quenching coefficient
- TSS:
-
total soluble sugar
- WC:
-
water content
- ФPSII:
-
actual photochemical efficiency of PSII
References
Abadin H., Ashizawa A., Stevens Y-W. et al.: Potential for human exposure. - In: Abadin H., Ashizawa A., Stevens Y-W. et al (ed.): Toxicological Profile for Lead. Pp. 301–380. U.S. Dep. Health Human Serv., Atlanta 2007.
Ahmad M.S., Ashraf M., Tabassam Q. et al.: Lead (Pb)-induced regulation of growth, photosynthesis, and mineral nutrition in maize (Zea mays L.) plants at early growth stages.–Biol. Trace Elem. Res. 144: 1229–1239, 2011.
Ali B., Xu X., Gill R.A. et al.: Promotive role of 5-aminolevulinic acid on mineral nutrients and antioxidative defense system under lead toxicity in Brassica napus. - Ind. Crop Prod. 52: 617–626, 2014.
Alkhatib R., Maruthavanan J., Ghoshroy S. et al.: Physiological and ultrastructural effects of lead on tobacco. - Biol. Plantarum 56: 711–716, 2012.
Bharwana S.A., Ali S., Farooq M.A. et al.: Glycine betaineinduced lead toxicity tolerance related to elevated photosynthesis, antioxidant enzymes suppressed lead uptake and oxidative stress in cotton. - Turk. J. Bot. 38: 281–292, 2014.
Bibi M., Hussain M.: Effect of copper and lead on photosynthesis and plant pigments in black gram [Vigna mungo (L.) Hepper]. - B. Environ. Contam. Tox. 74: 1126–1133, 2005.
Burzyński M., Kłobus G.: Changes of photosynthetic parameters in cucumber leaves under Cu, Cd, and Pb stress. - Photosynthetica 42: 505–510, 2004.
Capelo A., Dos Santos C.A., Loureiro S., Pedrosa M.A.: Phytotoxicity of lead on Lactuca sativa: effects on growth, mineral nutrition, photosynthetic activity and oxidant metabolism. - Fresen. Environ. Bull. 21: 450–459, 2012.
Cenkci S., Ciğerci I.H., Yildiz M. et al.: Lead contamination reduces chlorophyll biosynthesis and genomic template stability in Brassica rapa L. - Environ. Exp. Bot. 67: 467–473, 2010.
Couée I., Sulmon C., Gouesbet G. et al.: Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. - J. Exp. Bot. 57: 449–459, 2006.
Feleafel M.N., Mirdad Z.M.: Hazard and effects of pollution by lead on vegetable crops. - J. Agr. Environ. Ethic. 26: 547–567, 2012.
Grant L., Davis J., Hasselblad V. et al.: Executive summary and conclusions. - In: Environmental Protection Agency: Air Quality Criteria for Lead. Pp. 1–161. U.S. Environ. Protection Agency, Research Triangle Park, Atlanta 1986.
Igwe J.C., Nwokennaya E.C., Abia A.A.: The role of pH in heavy metal detoxification by bio-sorption from aqueous solutions containing chelating agents.–Afr. J.Biotechnol. 4: 1109–1112, 2005.
Irigoyen J.J., Emerich D.W., Sánchez Díaz M.: Water-stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativa) plants. - Physiol. Plantarum 84: 55–60, 1992.
Kaznina N.M., Laidinen G.F., Titov A.F. et al.: Effect of lead on the photosynthetic apparatus of annual grasses. - Biol. Bull. 32: 147–150, 2005.
Kosobrukhov A., Knyazeva I., Mudrik V.: Plantago major plants responses to increase content of lead in soil: Growth and photosynthesis. - Plant Growth Regul. 42: 145–151, 2004.
Kumar A., Prasad M.N., Sytar O.: Lead toxicity, defense strategies and associated indicative biomarkers in Talinum triangulare grown hydroponically. - Chemosphere 89: 1056–1065, 2012.
Lamb D.T., Ming H., Megharaj M. et al.: Relative tolerance of a range of australian native plant species and lettuce to copper, zinc, cadmium, and lead. - Arch. Environ. Con. Tox. 59: 424–432, 2010.
Lamhamdi M., Bakrim A., Aarab A. et al.: Lead phytotoxicity on wheat (Triticum aestivum L.) seed germination and seedlings growth. - CR Biol. 334: 118–126, 2011.
Monteiro M.S., Santos C., Soares A.M., Mann R.M.: Assessment of biomarkers of cadmium stress in lettuce. - Ecotox. Environ. Safe. 72: 811–818, 2009.
Nautiyal N., Sinha P.: Lead induced antioxidant defense system in pigeon pea and its impact on yield and quality of seeds. - Acta Physiol. Plant. 34: 977–983, 2012.
Osaki M., Shinano T., Tadano T.: Redistribution of carbon and nitrogen-compounds from the shoot to the harvesting organs during maturation in field crops. - Soil Sci. Plant Nutr. 37: 117–128, 1991.
Parys E., Romanowska E., Siedlecka M. et al.: The effect of lead on photosynthesis and respiration in detached leaves and in mesophyll protoplasts of Pisum sativum. - Acta Physiol. Plant. 20: 313–322, 1998.
Patra M., Bhowmik N., Bandopadhyay B. et al.: Comparison of mercury, lead and arsenic with respect to genotoxic effects on plant systems and the development of genetic tolerance. - Environ. Exp. Bot. 52: 199–223, 2004.
Pourrut B., Shahid M., Dumat C. et al.: Lead uptake, toxicity, and detoxification in plants. - Rev. Environ. Contam. T. 213: 113–136, 2011.
Rodriguez E., da Conceição Santos M., Azevedo R. et al.: Photosynthesis light-independent reactions are sensitive biomarkers to monitor lead phytotoxicity in a Pb-tolerant Pisum sativum cultivar. - Environ. Sci. Pollut. Res. Int. 22: 574–585, 2015.
Shahid M., Dumat C., Pourrut B. et al.: Influence of EDTA and citric acid on lead-induced oxidative stress to Vicia faba roots. - J. Soil. Sediment. 14: 835–843, 2014.
Shahid M., Pinelli E., Pourrut B. et al.: Lead-induced genotoxicity to Vicia faba L. roots in relation with metal cell uptake and initial speciation. - Ecotox. Environ. Safe. 74: 78–84, 2011.
Silva S., Pinto-Carnide O., Martins-Lopes P. et al.: Differential aluminium changes on nutrient accumulation and root differentiation in an Al sensitive vs. tolerant wheat. - Environ. Exp. Bot. 68: 91–98, 2010.
Sims D.A., Gamon J.A.: Relationships between leaf pigment content and spectral reflectance across a wide range of species, leaf structures and developmental stages. - Remote Sens. Environ. 81: 337–354, 2002.
Tian T., Ali B., Qin Y.B. et al.: Alleviation of lead toxicity by 5- aminolevulinic acid is related to elevated growth, photosynthesis, and suppressed ultrastructural damages in oilseed rape. - BioMed. Res. Int. 2014: 530–642, 2014.
van Kooten O., Snel J.F.: The use of chlorophyll fluorescence nomenclature in plant stress physiology. - Photosynth. Res. 25: 147–150, 1990.
Verma S., Dubey R.S.: Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. - Plant Sci. 164: 645–655, 2003.
Wierzbicka M.: Comparison of lead tolerance in Allium cepa with other plant species. - Environ. Pollut. 104: 41–52, 1999.
Wu X., Liu C., Qu C.X. et al.: Effects of lead on activities of photochemical reaction and key enzymes of carbon assimilation in spinach chloroplast. - Biol. Trace Elem. Res. 126: 269–279, 2008.
Yan Z.Z., Tam N.F.Y.: Differences in lead tolerance between Kandelia obovata and Acanthus ilicifolius seedlings under varying treatment times. - Aquat. Toxicol. 126: 154–162, 2013.
Zeng L.S., Liao M., Chen C.L. et al.: Effects of lead contamination on soil microbial activity and rice physiological indices in soil-Pb-rice (Oryza sativa L.) system. - Chemosphere 65: 567–574, 2006.
Zhao S.P., Ye X.Z., Zheng J.C.: Lead-induced changes in plant morphology, cell ultrastructure, growth and yields of tomato. - Afr. J. Biotechnol. 10: 10116–10124, 2011.
Author information
Authors and Affiliations
Corresponding author
Additional information
Acknowledgements
FCT/MCT supported S. Silva (FCT/BPD/74299/2010) and G. Pinto (SFRH/BPD/101669/2014) grants from the financing program QREN-POPH/FSE — Tipologia 4.1–Formação Avançada. We thank for the financial support to CESAM (UID/AMB/50017), to FCT/MEC through national funds, and the co-funding by the FEDER, within the PT2020 Partnership Agreement and Compete 2020, also this work was funded by FEDER/COMPET/POCI, POCI-01-0145-FEDER-006958 (UID/AGR/04033/2013) and UI QOPNA (Ref. FCT UID/QUI/00062/2013).
Rights and permissions
About this article
Cite this article
Silva, S., Pinto, G. & Santos, C. Low doses of Pb affected Lactuca sativa photosynthetic performance. Photosynthetica 55, 50–57 (2017). https://doi.org/10.1007/s11099-016-0220-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11099-016-0220-z