{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,18]],"date-time":"2026-08-18T04:18:43Z","timestamp":1787026723727,"version":"build-2736575974"},"reference-count":51,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2024,1,11]],"date-time":"2024-01-11T00:00:00Z","timestamp":1704931200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Microbiol."],"abstract":"<jats:p>As the environmental nuclear radiation pollution caused by nuclear-contaminated water discharge and other factors intensifies, more plant\u2013microorganism\u2013soil systems will be under long-term low-dose ionizing radiation (LLR). However, the regulatory mechanisms of the plant\u2013microorganism\u2013soil system under LLR are still unclear. In this study, we study a system that has been stably exposed to low-dose ionizing radiation for 10\u2009years and investigate the response of the plant\u2013microorganism\u2013soil system to LLR based on the decay of the absorbed dose rate with distance. The results show that LLR affects the carbon and nitrogen migration process between plant\u2013microorganism\u2013soil through the \u201csymbiotic microbial effect.\u201d The increase in the intensity of ionizing radiation led to a significant increase in the relative abundance of symbiotic fungi, such as Ectomycorrhizal fungi and Rhizobiales, which is accompanied by a significant increase in soil lignin peroxidase (LiP) activity, the C\/N ratio, and C%. Meanwhile, enhanced radiation intensity causes adaptive changes in the plant functional traits. This study demonstrates that the \u201csymbiotic microbial effect\u201d of plant\u2013microorganism\u2013soil systems is an important process in terrestrial ecosystems in response to LLR.<\/jats:p>","DOI":"10.3389\/fmicb.2023.1331477","type":"journal-article","created":{"date-parts":[[2024,1,11]],"date-time":"2024-01-11T00:14:40Z","timestamp":1704932080000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":5,"title":["Plant\u2013microorganism\u2013soil interaction under long-term low-dose ionizing radiation"],"prefix":"10.3389","volume":"14","author":[{"given":"Guoqiang","family":"Zeng","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yingzi","family":"Wen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chuyang","family":"Luo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yihong","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fei","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chao","family":"Xiong","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2024,1,11]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"e248","DOI":"10.1111\/gcb.13827","article-title":"What plant functional traits can reduce nitrous oxide emissions from intensively managed grasslands?","volume":"24","author":"Abalos","year":"2018","journal-title":"Glob Change Biol."},{"key":"ref2","doi-asserted-by":"publisher","first-page":"391","DOI":"10.1111\/ele.13923","article-title":"Decay by ectomycorrhizal fungi couples soil organic matter to nitrogen availability","volume":"25","author":"Argiroff","year":"2022","journal-title":"Ecol. 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Microbiol."},{"key":"ref28","doi-asserted-by":"publisher","first-page":"900","DOI":"10.1038\/s41559-022-01756-5","article-title":"Phylotype diversity within soil fungal functional groups drives ecosystem stability","volume":"6","author":"Liu","year":"2022","journal-title":"Nat Ecol Evol"},{"key":"ref29","doi-asserted-by":"publisher","first-page":"1644","DOI":"10.1080\/00103624.2010.485473","article-title":"Wheat grain nitrogen uptake, as affected by soil total and mineral nitrogen, for the determination of optimum nitrogen fertilizer rates for wheat production","volume":"41","author":"Miransari","year":"2010","journal-title":"Commun Soil Sci Plan"},{"key":"ref30","doi-asserted-by":"publisher","first-page":"1567","DOI":"10.1007\/s13213-019-01541-z","article-title":"Shifts in microbial community composition in tannery-contaminated soil in response to increased gamma radiation","volume":"69","author":"Mohammad","year":"2019","journal-title":"Ann. 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Spectr."},{"key":"ref600","doi-asserted-by":"publisher","DOI":"10.3390\/f9060333","article-title":"Microbial taxa and soil organic carbon accumulation driven by tree roots","volume":"9","author":"Song","year":"2018","journal-title":"Forests"},{"key":"ref40","doi-asserted-by":"publisher","first-page":"8532","DOI":"10.1002\/ece3.6600","article-title":"Survival strategy of the endangered tree Acer catalpifolium Rehd., based on 13C fractionation","volume":"10","author":"Song","year":"2020","journal-title":"Ecol. Evol."},{"key":"ref41","doi-asserted-by":"publisher","first-page":"314","DOI":"10.3389\/fmicb.2020.00314","article-title":"Microbial community, newly sequestered soil organic carbon, and \u03b415N variations driven by tree roots","volume":"11","author":"Song","year":"2020","journal-title":"Front. Microbiol."},{"key":"ref42","doi-asserted-by":"publisher","first-page":"1297399","DOI":"10.3389\/fpls.2023.1297399","article-title":"Structure and function of microbiomes in the rhizosphere and endosphere response to temperature and precipitation variation in Inner Mongolia steppes","volume":"14","author":"Song","year":"2023","journal-title":"Front. Plant Sci."},{"key":"ref43","doi-asserted-by":"publisher","first-page":"105176","DOI":"10.1016\/j.catena.2021.105176","article-title":"Linking leaf \u03b415N and \u03b413C with soil fungal biodiversity, ectomycorrhizal and plant pathogenic abundance in forest ecosystems of China","volume":"200","author":"Song","year":"2021","journal-title":"Catena"},{"key":"ref44","doi-asserted-by":"publisher","first-page":"121774","DOI":"10.1016\/j.envpol.2023.121774","article-title":"Impact of ionizing radiation on the environmental microbiomes of Chornobyl wetlands","volume":"330","author":"Videvall","year":"2023","journal-title":"Environ. Pollut."},{"key":"ref45","doi-asserted-by":"publisher","first-page":"337","DOI":"10.1007\/s13199-021-00792-2","article-title":"Ectomycorrhizal fungi and trees: brothers in arms in the face of anthropogenic activities and their consequences","volume":"84","author":"Vincent","year":"2021","journal-title":"Symbiosis"},{"key":"ref46","doi-asserted-by":"publisher","first-page":"999","DOI":"10.1016\/j.foreco.2011.05.035","article-title":"Growth and carbon sequestration by ectomycorrhizal fungi in intensively fertilized Norway spruce forests","volume":"262","author":"Wallander","year":"2011","journal-title":"Forest Ecol Manag"},{"key":"ref47","doi-asserted-by":"publisher","first-page":"850917","DOI":"10.3389\/fmicb.2022.850917","article-title":"Regulating root fungal community using Mortierella alpina for fusarium oxysporum resistance in Panax ginseng","volume":"13","author":"Wang","year":"2022","journal-title":"Front. Microbiol."},{"key":"ref48","doi-asserted-by":"publisher","first-page":"33","DOI":"10.1111\/nph.15679","article-title":"Exploring the role of ectomycorrhizal fungi in soil carbon dynamics","volume":"223","author":"Zak","year":"2019","journal-title":"New Phytol."},{"key":"ref49","doi-asserted-by":"publisher","first-page":"47","DOI":"10.1016\/j.apsoil.2016.07.021","article-title":"N fertilization decreases soil organic matter decomposition in the rhizosphere","volume":"108","author":"Zang","year":"2016","journal-title":"Appl. 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