Abstract
Background and aims
Imazethapyr (IM) is a chiral herbicide with two enantiomers, with a much stronger herbicidal effect of R-IM than S-IM. Pesticide residues are a common problem, and multi-generation cultivation method can reveal the consequences of long-term pesticide residues.
Methods
This study verified the effects of R-IM on the growth of Arabidopsis thaliana and rhizosphere microorganisms by treating A. thaliana with different concentrations of R-IM successively passaging experimental rhizospheres for three generations, and measured the changes of A. thaliana rhizosphere microbes.
Results
The growth of A. thaliana treated with R-IM (0.5 g/ha and 1.5 g/ha) was significantly inhibited especially after successive generations of culture. At the same time, R-IM treatment decreased chlorophyll and chlorophyll parameters to inhibit the photosynthetic efficiency, and it also reshaped the rhizosphere bacterial community structure of A. thaliana. This bio-effect was transmitted to the next generation of plants along with the soil microbiota.
Conclusions
The treatment of A. thaliana by R-IM in multi-generation culture resulted in an increasingly obvious growth inhibitory effect, the higher concentration of R-IM inhibited A. thaliana more strongly, and changed the abundance of rhizosphere microbes. With the cultivation of generations, the influence of pesticide residues on plants also became significant.
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References
Adegboye MF, Babalola OO (2016) Isolation and identification of potential antibiotic producing rare actinomycetes from rhizospheric soils. J Hum Ecol 56:31–41. https://doi.org/10.1080/09709274.2016.11907035
Arzanesh MH, Alikhani HA, Khavazi K, Rahimian HA, Miransari M (2011) Wheat (Triticum aestivum L.) growth enhancement by Azospirillum sp. under drought stress. World J Microbiol Biotechnol 27:197–205. https://doi.org/10.1007/s11274-010-0444-1
Asad MAU, Lavoie M, Song H, Jin Y, Fu Z, Qian H (2017) Interaction of chiral herbicides with soil microorganisms, algae and vascular plants. Sci Total Environ 580:1287–1299. https://doi.org/10.1016/j.scitotenv.2016.12.092
Bai L, Sun H, Zhang X, Cai B (2018) Next-generation sequencing of root fungal communities in continuous cropping soybean. Chilean J Agric Res 78:528–538. https://doi.org/10.4067/S0718-58392018000400528
Bakker P, Pieterse CMJ, de Jonge R, Berendsen RL (2018) The soil-borne legacy. Cell 172:1178–1180. https://doi.org/10.1016/j.cell.2018.02.024
Berendsen RL, Pieterse CM, Bakker PA (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486. https://doi.org/10.1016/j.tplants.2012.04.001
Berg G, Rybakova D, Grube M, Köberl M (2016) The plant microbiome explored: implications for experimental botany. J Exp Bot 67:995–1002. https://doi.org/10.1093/jxb/erv466
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303
Chen ZW, Chen H, Zou YQ, Qju JG, Wen YZ, Xu DM (2015) Are nutrient stresses associated with enantioselectivity of the chiral herbicide imazethapyr in Arabidopsis thaliana? J Agric Food Chem 63:10209–10217. https://doi.org/10.1021/acs.jafc.5b04495
Chen S, Li X, Lavoie M, Jin Y, Xu J, Fu Z et al (2017) Diclofop-methyl affects microbial rhizosphere community and induces systemic acquired resistance in rice. J Environ Sci 51:352–360. https://doi.org/10.1016/j.jes.2016.06.027
Dini-Andreote F (2020) Endophytes: the second layer of plant defense. Trends Plant Sci 25:319–322. https://doi.org/10.1016/j.tplants.2020.01.007
Edwards J, Johnson C, Santos-Medellín C, Lurie E, Podishetty NK, Bhatnagar S, Eisen JA, Sundaresan V (2015) Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci 112:911–920. https://doi.org/10.1073/pnas.1414592112
Foyer CH, Noctor G (2010) Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant 119. https://doi.org/10.1034/j.1399-3054.2003.00223.x
Gao Z, Karlsson I, Geisen S, Kowalchuk G, Jousset A (2019) Protists: puppet masters of the rhizosphere microbiome. Trends Plant Sci 24:165–176. https://doi.org/10.1016/j.tplants.2018.10.011
Hayat R, Ali S, Amara U, Khalid R, Ahmed I (2010) Soil beneficial bacteria and their role in plant growth promotion: a review. Ann Microbiol 60:579–598. https://doi.org/10.1007/s13213-010-0117-1
Inskeep WP, Bloom PR (1985) Extinction coefficients of chlorophyll a and B in n,n-dimethylformamide and 80% acetone. Plant Physiol 77:483–485. https://doi.org/10.1104/pp.77.2.483
Li Y, Zhang ZY, Liu WY, Ke MJ, Qu Q, Zhou ZG et al (2021) Phyllosphere bacterial assemblage is affected by plant genotypes and growth stages. Microbiol Res 248:7. https://doi.org/10.1016/j.micres.2021.126743
Lu T, Ke M, Lavoie M, Jin Y, Fan X, Zhang Z et al (2018a) Rhizosphere microorganisms can influence the timing of plant flowering. Microbiome 6:231. https://doi.org/10.1186/s40168-018-0615-0
Lu T, Ke M, Peijnenburg W, Zhu Y, Zhang M, Sun L 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. https://doi.org/10.1021/acs.jafc.7b06155
Lu T, Zhang Q, Zhang Z, Hu B, Chen J, Qian H (2021) Pollutant toxicology with respect to microalgae and cyanobacteria. J Environ Sci 99:175–186. https://doi.org/10.1016/j.jes.2020.06.033
Miura K, Taura K, Kodama Y, Schnabl B, Brenner DA (2008) Hepatitis C virus-induced oxidative stress suppresses hepcidin expression through increased histone deacetylase activity. Hepatology 48:1420–1429. https://doi.org/10.1002/hep.22486
Myers JP, Antoniou MN, Blumberg B, Carroll L, Colborn T, Everett LG et al (2016) Concerns over use of glyphosate-based herbicides and risks associated with exposures: a consensus statement. Environ Health 15:19. https://doi.org/10.1186/s12940-016-0117-0
Panke-Buisse K, Poole AC, Goodrich JK, Ley RE, Kao-Kniffin J (2015) Selection on soil microbiomes reveals reproducible impacts on plant function. Isme J 9:980–989. https://doi.org/10.1038/ismej.2014.196
Ping Z (2005) Laboratary manual for environmental microbiology. Zhejiang University Press 9787308041843
Qian H, Hu H, Mao Y, Ma J, Zhang A, Liu W et al (2009) Enantioselective phytotoxicity of the herbicide imazethapyr in rice. Chemosphere 76:885–892. https://doi.org/10.1016/j.chemosphere.2009.05.009
Qian H, Lu T, Peng X, Han X, Fu Z, Liu W (2011) Enantioselective phytotoxicity of the herbicide imazethapyr on the response of the antioxidant system and starch metabolism in Arabidopsis thaliana. PLoS One 6:e19451. https://doi.org/10.1371/journal.pone.0019451
Qian H, Han X, Zhang Q, Sun Z, Sun L, Fu Z (2013) Imazethapyr enantioselectively affects chlorophyll synthesis and photosynthesis in Arabidopsis thaliana. J Agric Food Chem 61:1172–1178. https://doi.org/10.1021/jf305198g
Qian H, Tsuji T, Endo T, Sato F (2014) PGR5 and NDH pathways in photosynthetic cyclic electron transfer respond differently to sublethal treatment with photosystem-interfering herbicides. J Agric Food Chem 62:4083–4089. https://doi.org/10.1021/jf500143f
Qian H, Lu H, Ding H, Lavoie M, Li Y, Liu W et al (2015) Analyzing Arabidopsis thaliana root proteome provides insights into the molecular bases of enantioselective imazethapyr toxicity. Sci Rep 5:11975. https://doi.org/10.1038/srep11975
Qian H, Zhang Q, Lu T, Peijnenburg W, Zhu YG (2021) Lessons learned from COVID-19 on potentially pathogenic soil microorganisms. Soil Ecol Lett 3(1):1–5
Qu Q, Zhang Z, Peijnenburg W, Liu W, Lu T, Hu B et al (2020) Rhizosphere microbiome assembly and its impact on plant growth. J Agric Food Chem 68:5024–5038. https://doi.org/10.1021/acs.jafc.0c00073
Rivas R, Velázquez E, Willems A, Vizcaíno N, Subba-Rao NS, Mateos PF et al (2002) A new species of Devosia that forms a unique nitrogen-fixing root-nodule symbiosis with the aquatic legume Neptunia natans (L.f.) druce. Appl Environ Microbiol 68:5217–5222. https://doi.org/10.1128/aem.68.11.5217-5222.2002
Rumschlag SL, Mahon MB, Hoverman JT, Raffel TR, Carrick HJ, Hudson PJ et al (2020) Consistent effects of pesticides on community structure and ecosystem function in freshwater systems. Nat Commun 11:6333. https://doi.org/10.1038/s41467-020-20192-2
Saha A, Bhaduri D, Pipariya A, Jain NK (2016) Influence of imazethapyr and quizalofop-p-ethyl application on microbial biomass and enzymatic activity in peanut grown soil. Environ Sci Pollut Res 23:23758–23771. https://doi.org/10.1007/s11356-016-7553-9
Sun C, Chen S, Jin Y, Song H, Ruan S, Fu Z et al (2016) Effects of the herbicide imazethapyr on photosynthesis in PGR5- and NDH-deficient Arabidopsis thaliana at the biochemical, transcriptomic, and proteomic levels. J Agric Food Chem 64:4497–4504. https://doi.org/10.1021/acs.jafc.6b01699
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267. https://doi.org/10.1128/aem.00062-07
Wille L, Messmer MM, Studer B, Hohmann P (2019) Insights to plant-microbe interactions provide opportunities to improve resistance breeding against root diseases in grain legumes. Plant Cell Environ 42:20–40. https://doi.org/10.1111/pce.13214
Wu H, Chen H, Jin C, Tang C, Zhang Y (2019) The chirality of imazethapyr herbicide selectively affects the bacterial community in soybean field soil. Environ Sci Pollut Res 26:2531–2546. https://doi.org/10.1007/s11356-018-3736-x
Yousefi S, Kartoolinejad D, Bahmani M, Naghdi R (2017) Effect of Azospirillum lipoferum and Azotobacter chroococcum on germination and early growth of hopbush shrub (Dodonaea Viscosa L.) under salinity stress. J Sustain For 36:107–120. https://doi.org/10.1080/10549811.2016.1256220
Yuan J, Zhao J, Wen T, Zhao M, Li R, Goossens P et al (2018) Root exudates drive the soil-borne legacy of aboveground pathogen infection. Microbiome 6:156. https://doi.org/10.1186/s40168-018-0537-x
Zabalza A, Gaston S, Ribas-Carbo M, Orcaray L, Igal M, Royuela M (2006) Nitrogen assimilation studies using N-15 in soybean plants treated with imazethapyr, an inhibitor of branched-chain amino acid biosynthesis. J Agric Food Chem 54:8818–8823. https://doi.org/10.1021/jf0618224
Zhang C, Xu J, Liu X, Dong F, Kong Z, Sheng Y et al (2010) Impact of imazethapyr on the microbial community structure in agricultural soils. Chemosphere 81:800–806. https://doi.org/10.1016/j.chemosphere.2010.06.079
Zhang Z, Fan X, Peijnenburg W, Zhang M, Sun L, Zhai Y et al (2021) Alteration of dominant cyanobacteria in different bloom periods caused by abiotic factors and species interactions. J Environ Sci 99:1–9. https://doi.org/10.1016/j.jes.2020.06.001
Zhang Q, Yu Y, Jin M, Deng Y, Zheng B, Lu T, Qian H (2022a) Oral azoxystrobin driving the dynamic change in resistome by disturbing the stability of the gut microbiota of Enchytraeus crypticus. J Hazard Mater 423:127252. https://doi.org/10.1016/j.jhazmat.2021.127252
Zhang Z, Zhang Q, Lu T, Zhang J, Sun L, Hu B, Hu J, Peñuelas J, Zhu L, Qian H (2022b) Residual chlorine disrupts the microbial communities and spreads antibiotic resistance in freshwater. J Hazard Mater 423:127152. https://doi.org/10.1016/j.jhazmat.2021.127152
Zhou QY, Xu C, Zhang YS, Liu WP (2009) Enantioselectivity in the phytotoxicity of herbicide imazethapyr. J Agric Food Chem 57:1624–1631. https://doi.org/10.1021/jf803673e
Zhu XF, Lei GJ, Wang ZW, Shi YZ, Braam J, Li GX et al (2013) Coordination between apoplastic and symplastic detoxification confers plant aluminum resistance. Plant Physiol 162:1947–1955. https://doi.org/10.1104/pp.113.219147
Acknowledgments
This work was financially supported by the National Natural Science Foundation of China (21976161, 21777144, 41907210).
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Binyu Zheng: Performed research, analyzed data, Wrote the paper. Qianqiu Zhao: Performed research. Lan Feng: Performed research. Zhenyan Zhang: Analyzed data. Qi Zhang: Analyzed data. Fan Zhang: Performed research. Yu Deng: Performed research. Tao Lu: Writing-review & editing. Haifeng Qian: Project administration, Writing-review & editing, Funding acquisition.
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Zheng, B., Zhao, Q., Feng, L. et al. Regulative effect of imazethapyr on Arabidopsis thaliana growth and rhizosphere microbial community through multiple generations of culture. Plant Soil 473, 625–637 (2022). https://doi.org/10.1007/s11104-022-05318-3
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DOI: https://doi.org/10.1007/s11104-022-05318-3