journal article
Open Access
Dec 17, 2015
Metabolomic analysis with GC-MS to reveal potential metabolites and biological pathways involved in Pb & Cd stress response of radish roots
Abstract
AbstractThe radish (Raphanus sativus L.) is an important root vegetable crop. In this study, the metabolite profiling analysis of radish roots exposed to lead (Pb) and cadmium (Cd) stresses has been performed using gas chromatography-mass spectrometry (GC-MS). The score plots of principal component analysis (PCA) and partial least squares-discriminate analysis (PLS-DA) showed clear discrimination between control and Pb- or Cd-treated samples. The metabolic profiling indicated Pb or Cd stress could cause large metabolite alteration mainly on sugars, amino acids and organic acids. Furthermore, an integrated analysis of the effects of Pb or Cd stress was performed on the levels of metabolites and gene transcripts from our previous transcriptome work in radish roots. Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis of integration data demonstrated that exposure of radish to Pb stress resulted in profound biochemical changes including carbohydrate metabolism, energy metabolism and glutathione metabolism, while the treatment of Cd stress caused significant variations in energy production, amino acid metabolism and oxidative phosphorylation-related pathways. These results would facilitate further dissection of the mechanisms of heavy metal (HM) accumulation/tolerance in plants and the effective management of HM contamination in vegetable crops by genetic manipulation.
Topics
No keywords indexed for this article. Browse by subject →
References
60
[1]
Gupta, N., Khan, D. & Santra, S. Heavy metal accumulation in vegetables grown in a long-term wastewater-irrigated agricultural land of tropical India. Environ. Monit. Assess. 184, 6673–6682 (2012).
10.1007/s10661-011-2450-7
[2]
Liu, X. et al. Human health risk assessment of heavy metals in soil-vegetable system: a multi-medium analysis. Sci. Total Environ. 463, 530–540 (2013).
10.1016/j.scitotenv.2013.06.064
[3]
Pourrut, B., Shahid, M., Douay, F., Dumat, C. & Pinelli, E. Molecular mechanisms involved in lead uptake, toxicity and detoxification in higher plants. In Heavy Metal Stress in Plants (eds Dharmendra K. G., Francisco J. C. & José M. P. ) 121–147 (Springer, 2013).
10.1007/978-3-642-38469-1_7
[4]
Seregin, I. & Ivanov, V. Physiological aspects of cadmium and lead toxic effects on higher plants. Russ. J. Plant Physiol. 48, 523–544 (2001).
10.1023/a:1016719901147
[5]
Benavides, M. P., Gallego, S. M. & Tomaro, M. L. Cadmium toxicity in plants. Braz. J. Plant Physiol. 17, 21–34 (2005).
10.1590/s1677-04202005000100003
[6]
Sharma, P. & Dubey, R. S. Lead toxicity in plants. Braz. J. Plant Physiol. 17, 35–52 (2005).
10.1590/s1677-04202005000100004
[7]
DalCorso, G., Farinati, S. & Furini, A. Regulatory networks of cadmium stress in plants. Plant Signal Behav. 5, 663–667 (2010).
10.4161/psb.5.6.11425
[8]
Thapa, G., Sadhukhan, A., Panda, S. K. & Sahoo, L. Molecular mechanistic model of plant heavy metal tolerance. Biometals 25, 489–505 (2012).
10.1007/s10534-012-9541-y
[9]
Gupta, O., Sharma, P., Gupta, R. & Sharma, I. MicroRNA mediated regulation of metal toxicity in plants: present status and future perspectives. Plant Mol. Biol. 84, 1–18 (2014).
10.1007/s11103-013-0120-6
[10]
Fell, D. A. Beyond genomics. Trends Genet. 17, 680–682 (2001).
10.1016/s0168-9525(01)02521-5
[11]
Urano, K., Kurihara, Y., Seki, M. & Shinozaki, K. ‘Omics’ analyses of regulatory networks in plant abiotic stress responses. Curr. Opin. Plant Biol. 13, 132–138 (2010).
10.1016/j.pbi.2009.12.006
[12]
Booth, S. C., Workentine, M. L., Weljie, A. M. & Turner, R. J. Metabolomics and its application to studying metal toxicity. Metallomics 3, 1142–1152 (2011).
10.1039/c1mt00070e
[13]
Patti, G. J., Yanes, O. & Siuzdak, G. Innovation: Metabolomics: the apogee of the omics trilogy. Nat. Rev. Mol. Cell Biol. 13, 263–269 (2012).
10.1038/nrm3314
[14]
Chagoyen, M. & Pazos, F. Tools for the functional interpretation of metabolomic experiments. Brief. Bioinform. 14, 737–744 (2012).
10.1093/bib/bbs055
[15]
Dunn, W. B. & Ellis, D. I. Metabolomics: current analytical platforms and methodologies. TrAC-Trends Analyt. Chem. 24, 285–294 (2005).
10.1016/j.trac.2004.11.021
[16]
Metabolomics for Functional Genomics, Systems Biology, and Biotechnology
Kazuki Saito, Fumio Matsuda
Annual Review of Plant Biology
2010
10.1146/annurev.arplant.043008.092035
[17]
Nikiforova, V. J. et al. Systems rebalancing of metabolism in response to sulfur deprivation, as revealed by metabolome analysis of Arabidopsis plants. Plant Physiol. 138, 304–318 (2005).
10.1104/pp.104.053793
[18]
Le Lay, P. et al. Metabolomic, proteomic and biophysical analyses of Arabidopsis thaliana cells exposed to a caesium stress. Influence of potassium supply. Biochimie 88, 1533–1547 (2006).
10.1016/j.biochi.2006.03.013
[19]
Bailey, N. J., Oven, M., Holmes, E., Nicholson, J. K. & Zenk, M. H. Metabolomic analysis of the consequences of cadmium exposure in Silene cucubalus cell cultures via 1H NMR spectroscopy and chemometrics. Phytochemistry 62, 851–858 (2003).
10.1016/s0031-9422(02)00719-7
[20]
Hédiji, H. et al. Effects of long-term cadmium exposure on growth and metabolomic profile of tomato plants. Ecotoxicol. Environ. Saf. 73, 1965–1974 (2010).
10.1016/j.ecoenv.2010.08.014
[21]
Kieffer, P. et al. Combining proteomics and metabolite analyses to unravel cadmium stress-response in poplar leaves. J. Proteome Res. 8, 400–417 (2008).
10.1021/pr800561r
[22]
Uraguchi, S. et al. Root-to-shoot Cd translocation via the xylem is the major process determining shoot and grain cadmium accumulation in rice. J. Exp. Bot. 60, 2677–2688 (2009).
10.1093/jxb/erp119
[23]
Kapourchal, S. A., Kapourchal, S. A., Pazira, E. & Homaee, M. Assessing radish (Raphanus sativus L.) potential for phytoremediation of lead-polluted soils resulting from air pollution. Plant Soil Environ. 55, 202–206 (2009).
10.17221/8/2009-pse
[24]
Wang, Y. et al. Transcriptome profiling of radish (Raphanus sativus L.) root and identification of genes involved in response to lead (Pb) stress with next generation sequencing. PloS One 8, e66539 (2013).
10.1371/journal.pone.0066539
[25]
Xu, L. et al. Genome-wide identification and characterization of cadmium-responsive microRNAs and their target genes in radish (Raphanus sativus L.) roots. J. Exp. Bot. 64, 4271–4287 (2013).
10.1093/jxb/ert240
[26]
Schauer, N. & Fernie, A. R. Plant metabolomics: towards biological function and mechanism. Trends Plant Sci. 11, 508–516 (2006).
10.1016/j.tplants.2006.08.007
[27]
Woo, H. M. et al. Mass spectrometry based metabolomic approaches in urinary biomarker study of women’s cancers. Clin. Chim. Acta 400, 63–69 (2009).
10.1016/j.cca.2008.10.014
[28]
El-Beltagi, H. & Mohamed, A. Changes in non protein thiols, some antioxidant enzymes activity and ultrastructural alteration in radish plant (Raphanus sativus L.) grown under lead toxicity. Not. Bot. Horti Agrobot. Cluj Napoca 38, 76–85 (2010).
[29]
Inoue, H. et al. Properties of lead deposits in cell walls of radish (Raphanus sativus) roots. J. Plant Res. 126, 51–61 (2013).
10.1007/s10265-012-0494-6
[30]
He, L. L. et al. Physiological responses of radish (Raphanus Sativus L.) to lead stress. In Bioinformatics and Biomedical Engineering, 2008. ICBBE 2008. The 2nd International Conference on 4602-4605 (IEEE, 2008).
10.1109/icbbe.2008.310
[31]
Wang, Y. et al. Transport, ultrastructural localization and distribution of chemical forms of lead in radish (Raphanus sativus L.). Front. Plant Sci. 6, 293 (2015).
[32]
Xu, L. et al. De novo sequencing of root transcriptome reveals complex cadmium-responsive regulatory networks in radish (Raphanus sativus L.). Plant Sci. 236, 313–323 (2015).
10.1016/j.plantsci.2015.04.015
[33]
Yang, J. et al. Cadmium uptake character and stress effect on the growth and antioxidant enzymes activities in Raphanus sativus. Acta Hortic. 767, 249 (2008).
10.17660/actahortic.2008.767.26
[34]
Arbona, V., Manzi, M., Ollas, C. d. & Gómez-Cadenas, A. Metabolomics as a tool to investigate abiotic stress tolerance in plants. Int. J. Mol. Sci. 14, 4885–4911 (2013).
10.3390/ijms14034885
[35]
Ariza, J. G., García-Barrera, T., García-Sevillano, M., González-Fernández, M. & Gómez-Jacinto, V. Metallomics and metabolomics of plants under environmental stress caused by metals. In Heavy Metal Stress in Plants (eds Dharmendra K. G., Francisco J. C. & José M. P. ) 173–201 (Springer, 2013).
10.1007/978-3-642-38469-1_10
[36]
Brunetti, C., George, R. M., Tattini, M., Field, K. & Davey, M. P. Metabolomics in plant environmental physiology. J. Exp. Bot. 64, 4011–4020 (2013).
10.1093/jxb/ert244
[37]
Tanyolac, D., Ekmekçi, Y. & Ünalan, Ş. Changes in photochemical and antioxidant enzyme activities in maize (Zea mays L.) leaves exposed to excess copper. Chemosphere 67, 89–98 (2007).
10.1016/j.chemosphere.2006.09.052
[38]
Aziz, T. et al. A mini review on lead (Pb) toxicity in plants. J. Biol. life Sci. 6, 91–101 (2015).
10.5296/jbls.v6i2.7152
[39]
Hall, J. Cellular mechanisms for heavy metal detoxification and tolerance. J. Exp. Bot. 53, 1–11 (2002).
10.1093/jexbot/53.366.1
[40]
Jones, D., Dennis, P., Owen, A. & Van Hees, P. Organic acid behavior in soils-misconceptions and knowledge gaps. Plant Soil 248, 31–41 (2003).
10.1023/a:1022304332313
[41]
Kochian, L., Pineros, M. & Hoekenga, O. The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Plant Soil 274, 175–195(2005).
10.1007/s11104-004-1158-7
[42]
Ma, J. F., Chen, Z. C. & Shen, R. F. Molecular mechanisms of Al tolerance in gramineous plants. Plant Soil 381, 1–12 (2014).
10.1007/s11104-014-2073-1
[43]
Ma, J. F., Ryan, P. R. & Delhaize, E. Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci. 6, 273–278 (2001).
10.1016/s1360-1385(01)01961-6
[44]
Kavita, B., Shukla, S., Kumar, G. N. & Archana, G. Amelioration of phytotoxic effects of Cd on mung bean seedlings by gluconic acid secreting rhizobacterium Enterobacter asburiae PSI3 and implication of role of organic acid. World J. Microbiol. Biotechnol. 24, 2965–2972 (2008).
10.1007/s11274-008-9838-8
[45]
Ghnaya, T. et al. Implication of organic acids in the long-distance transport and the accumulation of lead in Sesuvium portulacastrum and Brassica juncea. Chemosphere 90, 1449–1454 (2013).
10.1016/j.chemosphere.2012.08.061
[46]
Rai, V. Role of amino acids in plant responses to stresses. Biol. Plant. 45, 481–487 (2002).
10.1023/a:1022308229759
[47]
Hirai, M. Y. et al. Elucidation of gene-to-gene and metabolite-to-gene networks in Arabidopsis by integration of metabolomics and transcriptomics. J. Biol. Chem. 280, 25590–25595 (2005).
10.1074/jbc.m502332200
[48]
Estrella-Gómez, N. E., Sauri-Duch, E., Zapata-Pérez, O. & Santamaría, J. M. Glutathione plays a role in protecting leaves of Salvinia minima from Pb2+ damage associated with changes in the expression of SmGS genes and increased activity of GS. Environ. Exp. Bot. 75, 188–194 (2012).
10.1016/j.envexpbot.2011.09.001
[49]
Jozefczak, M., Remans, T., Vangronsveld, J. & Cuypers, A. Glutathione is a key player in metal-induced oxidative stress defenses. Int. J. Mol. Sci. 13, 3145–3175 (2012).
10.3390/ijms13033145
[50]
Sappl, P. G. et al. The Arabidopsis glutathione transferase gene family displays complex stress regulation and co-silencing multiple genes results in altered metabolic sensitivity to oxidative stress. Plant J. 58, 53–68 (2009).
10.1111/j.1365-313x.2008.03761.x
Showing 50 of 60 references
Cited By
139
The combination of red and blue light increases the biomass and steroidal saponin contents of Paris polyphylla var. yunnanensis
Industrial Crops and Products
Yi Li, Jiali Xu · 2023
A review on bioremediation approach for heavy metal detoxification and accumulation in plants
Environmental Pollution
P.R. Yaashikaa, P. Senthil Kumar · 2022
Metrics
139
Citations
60
References
Details
- Published
- Dec 17, 2015
- Vol/Issue
- 5(1)
- License
- View
Authors
Cite This Article
Yan Wang, Liang Xu, Hong Shen, et al. (2015). Metabolomic analysis with GC-MS to reveal potential metabolites and biological pathways involved in Pb & Cd stress response of radish roots. Scientific Reports, 5(1). https://doi.org/10.1038/srep18296
Related
You May Also Like
Ror2 signaling regulates Golgi structure and transport through IFT20 for tumor invasiveness
Michiru Nishita, Seung-Yeol Park · 2017
16,078 citations
SwissADME: a free web tool to evaluate pharmacokinetics, drug-likeness and medicinal chemistry friendliness of small molecules
Antoine Daina, Olivier Michielin · 2017
14,446 citations
Ultrastructural Characterization of the Lower Motor System in a Mouse Model of Krabbe Disease
Valentina Cappello, Laura Marchetti · 2016
13,254 citations
QuPath: Open source software for digital pathology image analysis
Peter Bankhead, Maurice B. Loughrey · 2017
7,659 citations
Lead Iodide Perovskite Sensitized All-Solid-State Submicron Thin Film Mesoscopic Solar Cell with Efficiency Exceeding 9%
Hui-Seon Kim, Chang-Ryul Lee · 2012
7,401 citations