Abstract
Dichlorprop (2-(2,4-dichlorophenoxy) propionic acid, DCPP), a commonly used herbicide for weed control, can be residually detected in soil. It is still unclear whether chiral DCPP exerts an enantioselective adverse effect on plant metabolism and the microbial community of the phyllosphere. In this study, we selected Arabidopsis thaliana as a model plant to explore the effects of R- and S-DCPP enantiomers on plant physiological activities, metabolism, and associated changes in the phyllosphere microbial community. Results indicated that the fresh weight of plants decreased by 37.6% after R-DCPP treatment, whereas it increased by 7.6% after S-DCPP treatment. The R-DCPP enantiomer also caused stronger disturbance to leaf morphology, mesophyll cell structure, and leaf metabolites compared with S-DCPP. GC–MS analysis of DCPP-treated Arabidopsis leaves pointed out a differential profile mostly in carbohydrates, organic acids, and fatty acids, between S-DCPP and R-DCPP treatments. The diversity of phyllospheric microorganisms decreased and the stability of microbial community in the phyllosphere increased after R-DCPP treatment, whereas the opposite result was detected after S-DCPP exposure. The correlation analysis revealed that chiral herbicides may affect microbial communities in the phyllosphere by influencing leaf metabolism, while sugars and terpenoids were considered the main factors in reshaping the microbial community structure in the phyllosphere. Our study provides a new perspective for evaluating the effect of residual DCPP enantiomers on plant physiology and corresponding phyllosphere microorganism changes via the regulation of leaf metabolism, and clarifies the ecological risk of DCPP enantiomer application in agriculture.
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References
Asad MAU, Lavoie M, Song H et al (2017) Interaction of chiral herbicides with soil microorganisms, algae and vascular plants. Sci Total Environ 580:1287–1299
Basheer AA (2018) Chemical chiral pollution: impact on the society and science and need of the regulations in the 21st century. Chirality 30:1088
Bauer WD, Mathesius U (2004) Plant responses to bacterial quorum sensing signals. Curr Opin Plant Biol 7:429–433
Bulgarelli D, Schlaeppi K, Spaepen S et al (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64:807–838
Caporaso J, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336
Chen ZW, Chen H, Zou YQ, Wen YZ (2016) Stomatal behaviors reflect enantioselective phytotoxicity of chiral herbicide dichlorprop in Arabidopsis thaliana. Sci Total Environ 562:73–80
Chen ZW, Wang J, Chen SY, Wen YZ (2017a) Enantioselective disturbance of chiral herbicide dichlorprop to nitrogen metabolism of Arabidopsis thaliana: Regular analysis and stable isotope attempt. Sci Total Environ 603:533–540
Chen ZW, Wang J, Chen H, Wen YZ, Liu WP (2017) Enantioselective phytotoxicity of dichlorprop to Arabidopsis thaliana: the effect of cytochrome P450 enzymes and the role of Fe. Environ Sci Technol 12007–12015
Coyte KZ, Schluter J, Foster KR (2015) The ecology of the microbiome: networks, competition, and stability. Science 350:663–666
Delmotte N, Knief C, Chaffron S et al (2009) Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Proc Natl Acad Sci USA 106:16428–16433
Dixon P (2003) VEGAN,a package of R functions for community ecology. J Veg Sci 14927–14993
Farre-Armengol G, Filella I, Llusia J, Penuelas J (2016) Bidirectional interaction between phyllospheric microbiotas and plant volatile emissions. Trends Plant Sci 21:854–860
Finkel OM, Castrillo G, Paredes SH, Gonzalez IS, Dangl JL (2017) Understanding and exploiting plant beneficial microbes. Curr Opin Plant Biol 38:155–163
Gabriela MO, Frank SC, Bernal AB et al (2020) Microhabitat heterogeneity associated with Vanilla spp. and its influences on the microbial community of leaf litter and soil. Soil Ecol Lett 3:195–208
Ginestet C (2011) Ggplot2: elegant graphics for data analysis. J R Stat Soc Ser A (stat Soc) 174:245–246
Gurdeep R, Coaker GL, Leveau JHJ (2013) New insights into the structure and function of phyllosphere microbiota through high-throughput molecular approaches. FEMS Microbiol Lett 348:1–10
Hummel I, Pantin F, Sulpice R et al (2010) Arabidopsis plants acclimate to water deficit at low cost through changes of carbon usage: an integrated perspective using growth, metabolite, enzyme, and gene expression analysis. Plant Physiol 154:357–372
Jiao S, Wang J, Wei G, Chen W, Lu Y (2019) Dominant role of abundant rather than rare bacterial taxa in maintaining agro-soil microbiomes under environmental disturbances. Chemosphere 235:248–259
Kaplan F, Kopka J, Sung DY et al (2007) Transcript and metabolite profiling during cold acclimation of Arabidopsis reveals an intricate relationship of cold-regulated gene expression with modifications in metabolite content. Plant J 50:967–981
Ke MJ, Ye Y, Li Y, Zhou Z, Qian HF (2021a) Leaf metabolic influence of glyphosate and nanotubes on the Arabidopsis thaliana phyllosphere. J Environ Sci 106:66–75
Ke MJ, Ye Y, Zhang ZY, Gillings M, Qian HF (2021) Synergistic effects of glyphosate and multiwall carbon nanotubes on Arabidopsis thaliana physiology and metabolism. Sci Total Environ 769:145156
Ke MJ, Qu Q, Peijnenburg W et al (2018) Phytotoxic effects of silver nanoparticles and silver ions to Arabidopsis thaliana as revealed by analysis of molecular responses and of metabolic pathways. Sci Total Environ 644:1070–1079
Kembel SW, O’Connor TK, Arnold HK, Hubbell SP, Wright SJ, Green JL (2014) Relationships between phyllosphere bacterial communities and plant functional traits in a neotropical forest. Proc Natl Acad Sci USA 111:13715–13720
Kembel SW, Cowan PD, Helmus MR et al (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26(11):1463–1464
Kim H, Lee KK, Jeon J, Harris WA, Lee Y-H (2020) Domestication of Oryza species eco-evolutionarily shapes bacterial and fungal communities in rice seed. Microbiome 8:20
Knief C, Delmotte N, Chaffron S et al (2012) Metaproteogenomic analysis of microbial communities in the phyllosphere and rhizosphere of rice. ISME J 6:1378–1390
Li Y, Zhang ZY, Liu WY, Ke MJ, Qian HF (2021) Phyllosphere bacterial assemblage is affected by plant genotypes and growth stages. Microbiol Res 248:126743
Li Z, Gong C, Xu Y, Yang J, Lu D, Cui W (2017) Enantioselective phytotoxicity and the relative mechanism of current chiral herbicides. Curr Protein Pept Sc 18:15–21
Lindow SE, Brandl MT (2003) Microbiology of the phyllosphere. Appl Environ Microbiol 69:1875–1883
Loewus FA, Murthy P (2000) Myo-inisitol metabolism in plants. Plant Sci 150:10–19
Lopez-Perez L, Martinez-Ballesta MD, Maurel C, Carvajal M (2009) Changes in plasma membrane lipids, aquaporins and proton pump of broccoli roots, as an adaptation mechanism to salinity. Phytochemistry 70:492–500
Lu T, Ke MJ, Lavoie M et al (2018a) Rhizosphere microorganisms can influence the timing of plant flowering. Microbiome 6:231
Lu T, Ke MJ, Peijnenburg W et al (2018b) Investigation of rhizospheric microbial communities in wheat, barley, and two rice varieties at the seedling stage. J Agric Food Chem 66:2645–2653
Mikulic-Petkovsek M, Schmitzer V, Slatnar A et al (2013) Alteration of the content of primary and secondary metabolites in strawberry fruit by colletotrichum nymphaeae infection. J Agric Food Chem 61:5987–5995
Muller DB, Vogel C, Bai Y, Vorholt JA (2016) The plant microbiota: systems-level insights and perspectives. Annu Rev Genet 50:211–234
Muller MD, Buser HR (1997) Conversion reactions of various phenoxyalkanoic acid herbicides in soil enantiomerization and enantioselective degradation of the chiral 2-phenoxypropionic acid herbicides. Environ Sci Technol 31:1953–1959
Nuccio ML, Wu J, Mowers R et al (2015) Expression of trehalose-6-phosphate phosphatase in maize ears improves yield in well-watered and drought conditions. Nat Biotechnol 33:862–869
Qian HF, Zhang Q, LuT PWJGM, Penuelas J, Zhu YG (2021) Lessons learned from COVID-19 on potentially pathogenic soil microorganisms. Soil Ecol Lett 3:1–5
Qu Q, Ke MJ, Ye YZ et al (2019a) Enantioselective oxidative stress induced by S- and Rac-metolachlor in wheat (Triticum aestivum L.) seedlings. Bull Environ Contam Toxicol 102:439–445
Qu Q, Li Y, Zhang ZZ et al (2021) Effects of S-metolachlor on wheat (Triticum aestivum L.) seedling root exudates and the rhizosphere microbiome. J Hazard Mater 411:125137
Qu Q, Zhang ZZ, Li Y et al (2019b) Comparative molecular and metabolic responses of wheat seedlings, (Triticum aestivum L.) to the imazethapyr enantiomers S-IM and R-IM. Sci Total Environ 692:723–731
Qu Q, Zhang ZY, Peijnenburg W et al (2020) Rhizosphere microbiome assembly and its impact on plant growth. J Agric Food Chem 68:5024–5038
Ratzke C, Barrere J, Gore J (2020) Strength of species interactions determines biodiversity and stability in microbial communities. Nat Ecol Evol 4:376–383
Revelle W R (2008) Psych: procedures for personality and psychological research. Softwore
Rizhsky L, Liang H, Shuman J, Shulaev V, Davletova S, Mittler R (2004) When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 134:1683–1696
Si C, Li X, Lavoie M et al (2017) Diclofop-methyl affects microbial rhizosphere community and induces systemic acquired resistance in rice. J Environ Sci 51:352–360
Takeuchi M, Hamana K, Hiraishi A (2001) Proposal of the genus Sphingomonas sensu stricto and three new genera, Sphingobium, Novosphingobium and Sphingopyxis, on the basis of phylogenetic and chemotaxonomic analyses. Int J Syst Evol Microbiol 51:1405–1417
Venturi V, Fuqua C (2013) Chemical signaling between plants and plant-pathogenic bacteria. Annu Rev Phytopathol 51:17–37
Xu L, Naylor D, Dong Z et al (2018) Drought delays development of the sorghum root microbiome and enriches for monoderm bacteria. Proc Natl Acad Sci USA 201717308
Xu NH, Qu Q, Zhang ZY et al (2020) Effects of residual S-metolachlor in soil on the phyllosphere microbial communities of wheat (Triticum aestivum L.). Sci Total Environ 748
Ye J, Zhao M, Niu L, Liu W (2015) Enantioselective environmental toxicology of chiral pesticides. Chem Res Toxicol 28:325–338
Zhang ZY, Fan XJ, Peijnenburg W et al (2021a) Alteration of dominant cyanobacteria in different bloom periods caused by abiotic factors and species interactions. J Environ Sci 99:1–9
Zhang Q, Ye YZ, Qu Q, Yu YT, Ke MJ, Lu T, Qian HF (2021) Enantioselective metabolomic modulations in Arabidopsis thaliana leaf induced by the herbicide dichlorprop. Sci Total Environ 797:149015
Zhang Q, Zhang ZZ, Zhou SYD et al (2021) Macleaya cordata extract, an antibiotic alternative, does not contribute to antibiotic resistance gene dissemination. J Hazard Mater 412:125272
Zhao QQ, Liu WY, Li Y et al (2020) Enantioselective effects of imazethapyr residues on Arabidopsis thaliana metabolic profile and phyllosphere microbial communities. J Environ Sci 93:57–65
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The authors thank the editor and anonymous reviewers for their constructive and valuable comments for enhancing the quality of our manuscript
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This work was financially supported by the National Natural Science Foundation of China (21777144, 21976161, and 41907210).
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Danyan Qiu: conceptualization, data curation, formal analysis, writing—original draft. Yizhi Ye: methodology, investigation, validation, formal analysis. Mingjing Ke: investigation, formal analysis. Nuohan Xu: investigation, formal analysis. Zhenyan Zhang: methodology, software. Fan Zhang: methodology, investigation. Jian Kang: investigation, software. Tao Lu: project administration, formal analysis. Haifeng Qian: project administration, visualization, writing—review and editing, funding acquisition.
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Qiu, D., Ye, Y., Ke, M. et al. Effects of chiral herbicide dichlorprop on Arabidopsis thaliana metabolic profile and its implications for microbial communities in the phyllosphere. Environ Sci Pollut Res 29, 28256–28266 (2022). https://doi.org/10.1007/s11356-021-17936-y
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DOI: https://doi.org/10.1007/s11356-021-17936-y