Abstract
The soil ecosystem is critical for agricultural production, affecting many aspects of human health. Soil has more unknown biodiversity and edaphic parameters than any other ecosystem especially when polluted. Metagenomics and metatranscriptomics were applied to research on toxicological characteristics of Pb and resistance mechanism of flavonols. Rhizosphere microorganisms–plants system, a unified system closely related to soil environment was taken as research object. Results emphasize gene expression changes in different test groups. Gene ontology enrichment and eggNOG showed that Pb has a toxic effect on gene and protein function which concentrated on ATPase and ATP-dependent activity. Differentially expressed genes in the flavonols group indicated that flavonols regulate amino acid transport and other transportation process related to Pb stress. Kegg analysis represents that Pb interferences energy production process via not only the upstream like glycolysis and tricarboxylic acid (TCA) circle but also oxidative phosphorylation process, which can also produce reactive oxygen species and impact the eliminating process. Flavonols have shown the ability in alleviating toxic effect of Pb and improving the resistance of plants. Flavonols can recover the electronic transmission and other process in TCA and oxidative phosphorylation via ascorbic acid-glutathione metabolism. Flavonols activated antioxidative process and non-specific immunity via vitamins B2–B6 metabolism.
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van den Broek D, Bloemberg GV, Lugtenberg B (2005): The role of phenotypic variation in rhizosphere Pseudomonas bacteria. Environ Microbiol 7, 1686–97
Akram NA, Shafiq F, Ashraf M (2017) Ascorbic acid—a potential oxidant scavenger and its role in plant development and abiotic stress tolerance. Front Plant Sci 8
Alessro DI, Antonella C, Irene M, Giulio C (2012) The role of flavonoids in root-rhizosphere signalling: opportunities and challenges for improving plant-microbe interactions. J Exp Bot 63:3429
Altermann E, Klaenhammer TR (2005) PathwayVoyager: pathway mapping using the Kyoto encyclopedia of genes and genomes (KEGG) database. BMC Genomics 6:60
Best MG, Sol N, Kooi I, Tannous J, Westerman BA, Rustenburg F, Schellen P, Verschueren H, Post E, Koster J (2015) RNA-Seq of tumor-educated platelets enables blood-based pan-cancer, multiclass, and molecular pathway cancer diagnostics. Cancer Cell 28:666–676
Bunnik EM, Chung DWD, Hamilton M, Ponts N, Saraf A, Prudhomme J, Florens L, Roch KGL (2013) Polysome profiling reveals translational control of gene expression in the human malaria parasite plasmodium falciparum. Genome Biol 14:R128
Deng B, Jin X, Yang Y, Lin Z, Zhang Y (2014) The regulatory role of riboflavin in the drought tolerance of tobacco plants depends on ROS production. Plant Growth Regul 72:269–277
Deng L, Zeng G, Fan C, Lu L, Chen X, Chen M, Wu H, He X, He Y (2015) Response of rhizosphere microbial community structure and diversity to heavy metal co-pollution in arable soil. Appl Microbiol Biotechnol 99:8259–8269
Dixon DP, Skipsey M, Edwards R (2010) Roles for glutathione transferases in plant secondary metabolism. Phytochemistry 71:338–350
Fischer M, Haase I, Feicht R, Schramek N, Köhler P, Schieberle P, Bacher A (2005) Evolution of vitamin B2 biosynthesis: riboflavin synthase of Arabidopsis thaliana and its inhibition by riboflavin. Biol Chem 34:87–428
Gao XQ, Kolomiets MV, Abbas HK (2009) Host-derived lipids and oxylipins are crucial signals in modulating mycotoxin production by fungi. Toxin Rev 28:79–88
Guo X, Xia X, Tang R, Zhou J, Zhao H, Wang K (2008) Development of a real-time PCR method for Firmicutes and Bacteroidetes in faeces and its application to quantify intestinal population of obese and lean pigs. Lett Appl Microbiol 47:367–373
Guo ZJ, Chen XJ, Wu XL, Ling JQ, Xu P (2004): Overexpression of the AP2/EREBP transcription factor OPBP1 enhances disease resistance and salt tolerance in tobacco. Plant Mol Biol. Plant Mol Biol 55, 607–618
Hasna HS, Hossain K, Mohd SH (2016) Plant growth-promoting Rhizobacteria enhance salinity stress tolerance in okra through ROS-scavenging enzymes. Biomed Res Int 2016:1–10
Hu Y, Cheng H (2013) Application of stochastic models in identification and apportionment of heavy metal pollution sources in the surface soils of a large-scale region. Environ Sci Technol 47:3752–3760
Jacobs H, Moalin M, van Gisbergen MW, Bast A, Wj VDV, Haenen GR (2011) An essential difference in the reactivity of the glutathione adducts of the structurally closely related flavonoids monoHER and quercetin. Free Radic Biol Med 51:2118–2123
Jiao J, Ma Y, Chen S, Liu C, Song Y, Qin Y, Yuan C, Liu Y (2016) Melatonin-producing endophytic bacteria from grapevine roots promote the abiotic stress-induced production of endogenous melatonin in their hosts. Front Plant Sci 7
Kaur S (2011) Transcriptome sequencing of lentil based on second-generation technology permits large-scale unigene assembly and SSR marker discovery. BMC Genomics 12:265
Knight R, Jansson J, Field D, Fierer N, Desai N, Fuhrman JA, Hugenholtz P, Van dLD, Meyer F, Stevens R (2012) Unlocking the potential of metagenomics through replicated experimental design. Nat Biotechnol 30:513–520
Korotchkina LG, Patel MS (2001) Site specificity of four pyruvate dehydrogenase kinase isoenzymes toward the three phosphorylation sites of human pyruvate dehydrogenase. J Biol Chem 276:37223–37229
Liu M, Lu S (2016, 1898) Plastoquinone and ubiquinone in plants: biosynthesis. Physiological Function and Metabolic Engineering Front Plant Sci 7
Lu C, Bucher G, Sander W (2004) Photoinduced interactions between oxidized and reduced lipoic acid and riboflavin (vitamin B2). Chemphyschem 5:47–56
Maris AJAV, Geertman JMA, Vermeulen A, Groothuizen MK, Winkler AA, Piper MDW, Dijken JPV, Pronk JT (2004) Directed evolution of pyruvate decarboxylase-negative Saccharomyces cerevisiae, yielding a C2-independent, glucose-tolerant, and pyruvate-hyperproducing yeast. Appl Environ Microbiol 70:159–166
Mendoza-Cózatl D, Loza-Tavera H, Hernández-Navarro A, Moreno-Sánchez R (2005) Sulfur assimilation and glutathione metabolism under cadmium stress in yeast, protists and plants. FEMS Microbiol Rev 29:653–671
Mitra S, Rupek P, Richter DC, Urich T, Gilbert JA, Meyer F, Wilke A, Huson DH (2011a) Functional analysis of metagenomes and metatranscriptomes using SEED and KEGG. Bmc Bioinformatics 12:S21–S21
Mitra S, Stärk M, Huson DH (2011b) Analysis of 16S rRNA environmental sequences using MEGAN. BMC Genomics 12:S17
Nakamichi N, Ito S, Oyama T, Yamashino T, Kondo T, Mizuno T (2004) Characterization of plant circadian rhythms by employing Arabidopsis cultured cells with bioluminescence reporters. Plant Cell Physiol 45:57–67
Okano T, Shimomura Y, Yamane M, Suhara Y, Kamao M, Sugiura M, Nakagawa K (2008) Conversion of phylloquinone (vitamin K1) into menaquinone-4 (vitamin K2) in mice: two possible routes for menaquinone-4 accumulation in cerebra of mice. J Biol Chem 283:11270–11279
Pan H, Zhang X, Ren B, Yang H, Ren Z, Wang W (2017) Toxic assessment of cadmium based on online swimming behavior and the continuous AChE activity in the gill of zebrafish (Danio rerio). Water Air Soil Pollut 228:355
Qin YM, Hu CY, Zhu YX (2008) The ascorbate peroxidase regulated by H(2)O(2) and ethylene is involved in cotton fiber cell elongation by modulating ROS homeostasis. Plant Signal Behav 3:194–196
Ren Z, Zhang X, Wang X, Qi P, Zhang B, Zeng Y, Fu R, Miao M (2015) AChE inhibition: one dominant factor for swimming behavior changes of Daphnia magna under DDVP exposure. Chemosphere 120:252–257
Roy S, Saha TT, Johnson L, Zhao B, Ha J, White KP, Girke T, Zou Z, Raikhel AS (2015) Regulation of gene expression patterns in mosquito reproduction. PLoS Genet 11:e1005450
Samsatly J, Chamoun R, Gluckthaler E, Jabaji S (2015) Genes of the de novo and salvage biosynthesis pathways of vitamin B6 are regulated under oxidative stress in the plant pathogen Rhizoctonia solani. Front Microbiol 6:1429
Summer EJ (2009) Preparation of a phage DNA fragment library for whole genome shotgun sequencing. Methods Mol Biol 502:27
Szydlowski N, Bürkle L, Pourcel L, Moulin M, Stolz J, Fitzpatrick TB (2013) Recycling of pyridoxine (vitamin B6) by PUP1 in Arabidopsis. Plant J 75:40–52
Tan F, Zhang K, Mujahid H, Verma DP, Peng Z (2011) Differential histone modification and protein expression associated with cell wall removal and regeneration in rice (Oryza sativa). J Proteome Res 10:551–563
Wang CH, Wu SB, Wu YT, Wei YH (2013a) Oxidative stress response elicited by mitochondrial dysfunction: implication in the pathophysiology of aging. Exp Biol Med 238:450–460
Wang J, Zeng Q, Zhu J, Liu G, Tang H (2013b) Dissimilarity of ascorbate–glutathione (AsA–GSH) cycle mechanism in two rice (Oryza sativa L.) cultivars under experimental free-air ozone exposure. Agric Ecosyst Environ 165:39–49
Wang L, Ren Z, Kim H, Xia C, Fu R, Chon T-S (2015a) Characterizing response behavior of medaka (Oryzias latipes) under chemical stress based on self-organizing map and filtering by integration. Ecological Informatics 29:107–118
Wang Y, Shen W, Chan Z, Wu Y (2015b) Endogenous cytokinin overproduction modulates ROS homeostasis and decreases salt stress resistance in Arabidopsis thaliana. Front Plant Sci 6
Wibberg D, Andersson L, Tzelepis G, Rupp O, Blom J, Jelonek L, Pühler A, Fogelqvist J, Varrelmann M, Schlüter A (2016) Genome analysis of the sugar beet pathogen Rhizoctonia solani AG2-2IIIB revealed high numbers in secreted proteins and cell wall degrading enzymes. BMC Genomics 17:245
Williams MA, Rice CW (2007) Seven years of enhanced water availability influences the physiological, structural, and functional attributes of a soil microbial community. Appl Soil Ecol 35:535–545
Xing N, Ji L, Song J, Ma J, Li S, Ren Z, Xu F, Zhu J (2017) Cadmium stress assessment based on the electrocardiogram characteristics of zebra fish (Danio rerio): QRS complex could play an important role. Aquat Toxicol 191:236–244
Yadav SK (2010) Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. S Afr J Bot 76:167–179
Yang C, Zhang M, Dong W, Cui G, Ren Z, Wang W (2017) Highly efficient photocatalytic degradation of methylene blue by PoPD/TiO2 nanocomposite. PLoS One 12:e0174104
Yin L, Yang H, Si G, Ren Q, Fu R, Zhang B, Zhang X, Wang X, Qi P, Xia C (2016) Persistence parameter: a reliable measurement for behavioral responses of medaka (Oryzias latipes) to environmental stress. Environ Model Assess 21:159–167
Zhang Q, Li Y, Phanlavong P, Wang Z, Jiao T, Qiu H, Peng Q (2017a) Highly efficient and rapid fluoride scavenger using an acid/base tolerant zirconium phosphate nanoflake: behavior and mechanism. J Clean Prod 161:317–326
Zhang Q, Li Y, Yang Q, Chen H, Chen X, Jiao T, Peng Q (2018a) Distinguished Cr (VI) capture with rapid and superior capability using polydopamine microsphere: behavior and mechanism. J Hazard Mater 342:732–740
Zhang X, Yang H, Ren Z, Cui Z (2016) The toxic effects of deltamethrin on Danio rerio: the correlation among behavior response, physiological damage and AChE. RSC Adv 6:109826–109833
Zhang X, Yang H, Cui Z (2017c) Mucor circinelloides: efficiency of bioremediation response to heavy metal pollution. Toxicol Res 6:442–447
Zhang X, Yang H, Cui Z (2017d) Alleviating effect and mechanism of flavonols in Arabidopsis resistance under Pb–HBCD stress. ACS Sustain Chem Eng 5:11034–11041
Zhang X, Li X, Yang H, Cui Z (2018b) Biochemical mechanism of phytoremediation process of lead and cadmium pollution with Mucor circinelloides and Trichoderma asperellum. Ecotoxicol Environ Saf 157:21–28
Zhang X, Yang H, Cui Z (2018c) Evaluation and analysis of soil migration and distribution characteristics of heavy metals in iron tailings. J Clean Prod 172:475–480
Zhou Y, Pijuan M, Zeng RJ, Yuan Z (2009) Involvement of the TCA cycle in the anaerobic metabolism of polyphosphate accumulating organisms (PAOs). Water Res 43:1330–1340
Acknowledgments
The authors are grateful to School of Life Sciences in Shandong University for their suggestions and support to improve the basic research. Special thanks are extended to Department of Plant and Microbial Biology in University of Zurich for technical support and article modification. Many thanks to CSC (Xu Zhang was supported by China Scholarship Council for 13 months study at University of Zurich). The authors would like to thank all the anonymous referees for their constructive comments and suggestions.
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This research was funded by Shandong University.
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Li, M., Zhang, X., Yang, H. et al. Soil sustainable utilization technology: mechanism of flavonols in resistance process of heavy metal. Environ Sci Pollut Res 25, 26669–26681 (2018). https://doi.org/10.1007/s11356-018-2485-1
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DOI: https://doi.org/10.1007/s11356-018-2485-1