转基因作物对土壤微生物群落影响的研究进展

doi:10.13560/j.cnki.biotech.bull.1985.2020-1422

摘要/Abstract

摘要：

转基因作物的安全是全球的热点问题之一。土壤微生物在土壤有机质转化、养分矿化、腐殖质形成和土壤结构改良等几个过程中发挥着重要作用。虽然转基因作物在提高农业生产方面具有巨大的潜力,但它们对土壤安全和土壤微生物的潜在影响还有待进一步的深入研究。本文综述了抗虫、抗病、抗除草剂等3类转基因作物对土壤微生物多样性和群落结构产生的影响,提出了转基因作物土壤生态安全评价中还应考虑的问题,并对今后的工作做了展望。

关键词: 转基因作物, 安全评价, 微生物多样性

Abstract:

The safety of genetically modified crops is one of the hot issues in the world. Soil microorganisms play an essential role in soil organic matter transformation,nutrient mineralization,humus formation and soil structure improvement. Although transgenic crops have great potential in improving agricultural production,their potential effects on soil security and soil microorganisms need further in-depth study. This paper reviews the effects of insect-resistant,disease-resistant and herbicide-resistant genetically modified crops on soil microbial diversity and community structure. Then the paper puts forward the issues that should be considered in the evaluation of soil ecological security of transgenic crops,and makes a prospect for the future work.

Key words: genetically modified crops, safety evaluation, microbial diversity

王婷, 杨阳, 李金萍, 杜坤. 转基因作物对土壤微生物群落影响的研究进展[J]. 生物技术通报, 2021, 37(9): 255-265.

WANG Ting, YANG Yang, LI Jin-ping, DU Kun. Research Progress in the Effects of Genetically Modified Crops on Soil Microbial Community[J]. Biotechnology Bulletin, 2021, 37(9): 255-265.

图/表 3

参考文献 76

[1]	柳晓丹, 许文涛, 黄昆仑, 等. 复合性状转基因植物安全性评价的研究进展[J]. 生物技术通报, 2016, 32(6):1-6.
	Liu XD, Xu WT, Huang KL, et al. Research progress on the safety assessment of stacked genetically modified plants[J]. Biotechnology Bulletin, 2016, 32(6):1-6.
[2]	Mandal A, Sarkar B, Owens G, et al. Impact of genetically modified crops on rhizosphere microorganisms and processes:A review focusing on Bt cotton[J]. Applied Soil Ecology, 2020, 148:103492. doi: 10.1016/j.apsoil.2019.103492 URL
[3]	Hu H, Xie M, Yu Y, et al. Transgenic Bt cotton tissues have no apparent impact on soil microorganisms[J]. Plant, Soil and Environment, 2013, 59(8):366-371. doi: 10.17221/PSE URL
[4]	Wang B, Shen H, Yang X, et al. Effects of chitinase-transgenic(McChit1)tobacco on the rhizospheric microflora and enzyme activities of the purple soil[J]. Plant, Soil and Environment, 2013, 59(6):241-246. doi: 10.17221/PSE URL
[5]	Garland JL, Mills AL. Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization[J]. Applied and Environment Microbiology, 1991, 57(8):2351-2359. doi: 10.1128/aem.57.8.2351-2359.1991 URL
[6]	Liphadzi KB, Al-Khatib K, Bensch CN, et al. Soil microbial and nematode communities as affected by glyphosate and tillage practices in a glyphosate-resistant cropping system[J]. Weed Science, 2005, 53(4):536-545. doi: 10.1614/WS-04-129R1 URL
[7]	Lupwayi NZ, Blackshaw RE. Soil microbial properties in Bt(Bacillus thuringiensis)corn cropping systems[J]. Applied Soil Ecology, 2013, 63:127-133. doi: 10.1016/j.apsoil.2012.09.005 URL
[8]	Mulder C, Wouterse M, Rutgers M, et al. Can transgenic maize affect soil microbial communities?[J]. PLoS Computational Biology, 2006, 9:e128.
[9]	Wei M, Tan F, Zhu H, et al. Impact of Bt-transgenic rice(SHK601)on soil ecosystems in the rhizosphere during crop development[J]. Plant, Soil and Environment, 2012, 58(5):217-223. doi: 10.17221/PSE URL
[10]	Haack SK, Garchow H, Klug MJ, et al. Analysis of factors affecting the accuracy, reproducibility, and interpretation of microbial community carbon source utilization patterns[J]. Applied and Environmental Microbiology, 1995, 61(4):1458-1468. doi: 10.1128/aem.61.4.1458-1468.1995 pmid: 16534996
[11]	Frostegård Å, Tunlid A, Bååth E. Use and misuse of PLFA measurements in soils[J]. Soil Biology and Biochemistry, 2011, 43(8):1621-1625. doi: 10.1016/j.soilbio.2010.11.021 URL
[12]	齐鸿雁, 薛凯, 张洪勋. 磷脂脂肪酸谱图分析方法及其在微生物生态学领域的应用[J]. 生态学报, 2003(8):1576-1582.
	Qi HY, Xue K, Zhang HX. Phospholipid fatty acid analysis and its applications in microbial ecology[J]. Acta Ecologica Sinica, 2003(8):1576-1582.
[13]	Griffiths BS, Caul S, Thompson J, et al. A comparison of soil microbial community structure, protozoa and nematodes in field plots of conventional and genetically modified maize expressing the Bacillus thuringiens is CryIAb toxin[J]. Plant and Soil, 2005, 275(1):135-146. doi: 10.1007/s11104-005-1093-2 URL
[14]	Mardis ER. Next-generation DNA sequencing methods[J]. Annual Review of Genomics and Human Genetics, 2008, 9(1):387-402. doi: 10.1146/genom.2008.9.issue-1 URL
[15]	Nielsen UN, Wall DH. The future of soil invertebrate communities in polar regions:different climate change responses in the Arctic and Antarctic?[J]. Ecology Letters, 2013, 16(3):409-419. doi: 10.1111/ele.12058 pmid: 23278945
[16]	Ranjard L, Dequiedt S, Chemidlin PN, et al. Turnover of soil bacterial diversity driven by wide-scale environmental heterogeneity[J]. Nature Communications, 2013, 4(1):1434. doi: 10.1038/ncomms2431 URL
[17]	Fahner NA, Shokralla S, Baird DJ, et al. Large-scale monitoring of plants through environmental DNA metabarcoding of soil:Recovery, resolution, and annotation of four DNA markers[J]. PLoS One, 2016, 11(6):e0157505. doi: 10.1371/journal.pone.0157505 URL
[18]	Tringe SG, Von Mering C, Kobayashi A, et al. Comparative metagenomics of microbial communities[J]. Science, 2005, 308(5721), 554-557. doi: 10.1126/science.1107851 URL
[19]	Mende DR, Waller AS, Sunagawa S, et al. Assessment of metagenomic assembly using simulated next generation sequencing data[J]. PLoS One, 2012, 7(2):e31386. doi: 10.1371/journal.pone.0031386 URL
[20]	Stewart FJ, Ottesen EA, DeLong EF. Development and quantitative analyses of a universal rRNA-subtraction protocol for microbial metatranscriptomics[J]. The ISME Journal, 2010, 4(7):896-907. doi: 10.1038/ismej.2010.18 URL
[21]	李强. 植物抗虫基因工程的研究进展[J]. 世界农业, 1995(10):23-25.
	Li Q. Advances on the insect-resistance gene engineering of plant[J]. World Agriculture, 1995(10):23-25.
[22]	Zhang YJ, Xie M, Peng DL, et al. Effects of the transgenic CrylAc and CpTI insect-resistant cotton SGK321 on rhizosphere soil microorganism populations in Northern China[J]. Plant Soil and Environment, 2014, 60(6):285-289. doi: 10.17221/PSE URL
[23]	Song YN, Su J, Chen R, et al. Diversity of microbial community in a paddy soil with cry1Ac/cpti transgenic rice[J]. Pedosphere, 2014, 24(3):349-358. doi: 10.1016/S1002-0160(14)60021-7 URL
[24]	Becker R, Bubner B, Remus R, et al. Impact of multi-resistant transgenic Bt maize on straw decomposition and the involved microbial communities[J]. Applied Soil Ecology, 2014, 73:9-18. doi: 10.1016/j.apsoil.2013.08.002 URL
[25]	Zeng HL, Tan FX, Zhang YY, et al. Effects of cultivation and return of Bacillus thuringiensis(Bt)maize on the diversity of the arbuscular mycorrhizal community in soils and roots of subsequently cultivated conventional maize[J]. Soil Biology and Biochemistry, 2014, 75:254-263. doi: 10.1016/j.soilbio.2014.04.024 URL
[26]	Katarína O, Daniel M, Andrej F, et al. Impact of genetically modified maize on the genetic diversity of rhizosphere bacteria:a two-year study in Slovakia[J]. Polish Journal of Ecology, 2014, 62(1):67-76. doi: 10.3161/104.062.0107 URL
[27]	Cheeke TE, Schütte UM, Hemmerich CM, et al. Spatial soil heterogeneity has a greater effect on symbiotic arbuscular mycorrhizal fungal communities and plant growth than genetic modification with Bacillus thuringiensis toxin genes[J]. Molecular Ecology, 2015, 24(10):2580-2593. doi: 10.1111/mec.13178 pmid: 25827202
[28]	Luo JY, Zhang S, Zhu XZ, et al. Effects of soil salinity on rhizosphere soil microbes in transgenic Bt cotton fields[J]. Journal of Integrative Agriculture, 2017, 16(7):1624-1633. doi: 10.1016/S2095-3119(16)61456-9 URL
[29]	Zaman M, Mirza MS, Irem S, et al. A temporal expression of Cry1Ac protein in cotton plant and its impact on soil health[J]. International Journal of Agriculture and Biology, 2015, 17(2):280-288.
[30]	Zhang YJ, Xie M, Wu G, et al. A 3-year field investigation of impacts of Monsanto’s transgenic Bt-cotton NC 33B on rhizosphere microbial communities in Northern China[J]. Applied Soil Ecology, 2015, 89:18-24. doi: 10.1016/j.apsoil.2015.01.003 URL
[31]	Yasin S, Asghar HN, Ahmad F, et al. Impact of Bt-cotton on soil microbiological and biochemical attributes[J]. Plant Production Science, 2016, 19(4):458-467. doi: 10.1080/1343943X.2016.1185637 URL
[32]	Dong LH, Meng Y, Wang J, et al. Effects of Transgenic Bt plus CpTI cotton on the abundance and diversity of rhizosphere ammonia oxidizing bacteria and archaea[J]. Journal of Environmental Biology, 2016, 37(5):881-8.
[33]	Wu HS, Shi X, Li J. Soil ecological safety evaluation for bivalent transgenic cotton plants:Root exudates versus soil enzyme activities and soil microbial diversity[J]. Applied Ecology and Environmental Research, 2016, 14(2):319-336. doi: 10.15666/aeer URL
[34]	王晓宜, 冯远娇, 闫帅, 等. 连续种植Bt玉米对土壤Bt蛋白含量及微生物数量的影响[J]. 生态环境学报, 2016, 25(12):1945-1952.
	Wang XY, Feng YJ, Yan S, et al. Effects of continuous planting Bt corn on Bt protein content and microbial quantity in soil[J]. Ecology and Environmental Sciences, 2016, 25(12):1945-1952.
[35]	Cotta SR, Cavalcante Franco Dias A, Seldin L, et al. The diversity and abundance of phytase genes(β-propeller phytases)in bacterial communities of the maize rhizosphere[J]. Letters in Applied Microbiology, 2016, 62(3):264-268. doi: 10.1111/lam.12535 pmid: 26661994
[36]	Lee ZL, Bu NS, Cui J, et al. Effects of long-term cultivation of transgenic Bt rice(Kefeng-6)on soil microbial functioning and C cycling[J]. Scientific Reports, 2017, 7:4647. doi: 10.1038/s41598-017-04997-8 URL
[37]	Xie M, Zhang YJ, Peng DL, et al. No significant impact of transgenic Cry1Ab/1Ac cotton on rhizosphere-soil enzyme activities and bacterial communities[J]. Agronomy Journal, 2017, 109:1271-1279. doi: 10.2134/agronj2016.10.0618 URL
[38]	范巧兰, 李永山, 王慧, 等. 转基因棉花对土壤细菌群落的影响[J]. 山西农业科学, 2017, 45(7):1124-1127.
	Fan QL, Li YS, Wang H, et al. Effects of transgenic cotton on soil bacteria community[J]. Journal of Shanxi Agricultural Sciences, 2017, 45(7):1124-1127.
[39]	Li P, Li YC, Shi JL, et al. Impact of transgenic Cry1Ac+CpTI cotton on diversity and dynamics of rhizosphere bacterial community of different root environments[J]. Science of the Total Environment, 2018, 637-638:233-243. doi: 10.1016/j.scitotenv.2018.05.013 URL
[40]	Qi XM, Liu B, Wu HP, et al. Bacterial communities under long-term conventional and transgenic cotton farming systems using V3-V5 and V5-V9 of 16S rDNA[J]. Ecotoxicology and Environmental Safety, 2018, 164:618-628. doi: 10.1016/j.ecoenv.2018.08.038 URL
[41]	Liang JG, Luan Y, Jiao Y, et al. No significant differences in rhizosphere bacterial communities between Bt maize cultivar IE09S034 and the near-isogenic non- Bt cultivar Zong31[J]. Plant, Soil and Environment, 2018, 64(9):427-434. doi: 10.17221/PSE URL
[42]	Li ZL, Bu NS, Chen XP, et al. Soil incubation studies with Cry1Ac protein indicate no adverse effect of Bt crops on soil microbial communities[J]. Ecotoxicology and Environmental Safety, 2018, 152:33-41. doi: 10.1016/j.ecoenv.2017.12.054 URL
[43]	Zeng HL, Zhong W, Tan FX, et al. The influence of Bt maize cultivation on communities of arbuscular mycorrhizal fungi revealed by MiSeq sequencing[J]. Frontiers in Microbiology, 2018, 9:3275. doi: 10.3389/fmicb.2018.03275 URL
[44]	Liu YB, Li JS, Neal Stewart C, et al. The effects of the presence of Bt-transgenic oilseed rape in wild mustard populations on the rhizosphere nematode and microbial communities[J]. Science of the Total Environment, 2015, 530-531:263-270. doi: 10.1016/j.scitotenv.2015.05.073 URL
[45]	Zhu WJ, Lu HH, Hill J, et al. ¹³C pulse-chase labeling comparative assessment of the active methanogenic archaeal community composition in the transgenic and nontransgenic parental rice rhizospheres[J]. FEMS Microbiology Ecology, 2014, 87(3):746-756. doi: 10.1111/fem.2014.87.issue-3 URL
[46]	Ahamd M, Abbasi WM, Jamil M, et al. Comparison of rhizosphere properties as affected by different Bt- and non-Bt-cotton(Gossypium hirsutum L.)genotypes and fertilization[J]. Environmental Monitoring and Assessment, 2017, 189(6):278. doi: 10.1007/s10661-017-5994-3 URL
[47]	Han C, Liu B, Zhong W. Effects of transgenic Bt rice on the active rhizospheric methanogenic archaeal community as revealed by DNA-based stable isotope probing[J]. Journal of Applied Microbiology, 2018, 125(4):1094-1107. doi: 10.1111/jam.13939 pmid: 29846995
[48]	van Wyk DAB, Adeleke R, Rhode OHJ, et al. Ecological guild and enzyme activities of rhizosphere soil microbial communities associated with Bt-maize cultivation under field conditions in North West Province of South Africa[J]. Journal of Basic Microbiology, 2017, 57(9):781-792. doi: 10.1002/jobm.v57.9 URL
[49]	Kahlon JG, Jacobsen HJ, Cahill JF, et al. Antifungal genes expressed in transgenic pea(Pisum sativum L.)do not affect root colonization of arbuscular mycorrhizae fungi[J]. Mycorrhiza, 2017, 27:683-694. doi: 10.1007/s00572-017-0781-0 URL
[50]	Khan MS, Sadat SU, Jan A, et al. Impact of transgenic Brassica napus harboring the antifungal synthetic chitinase(NiC)gene on rhizosphere microbial diversity and enzyme activities[J]. Frontiers in Plant Science, 2017, 8:1307. doi: 10.3389/fpls.2017.01307 URL
[51]	Khan MS, Ahmad H, Ullah M, et al. Allelopathic assessment for the environmental biosafety of the transgenic oilseed rape lines harboring the antifungal synthetic chitinase(NiC)gene[J]. Pakistan Journal of Botany, 2019, 51(4):1465-1472.
[52]	Shahmoradi ZS, Tohidfar M, Marashi H, et al. Cultivation effect of chitinase-transgenic cotton on functional bacteria and fungi in rhizosphere and bulk soil[J]. Iranian Journal of Biotechnology, 2019, 17(2):e1982.
[53]	Fernandez Bidondo L, Almasia N, Bazzini A, et al. The overexpression of antifungal genes enhances resistance to Rhizoctonia solani in transgenic potato plants without affecting arbuscular mycorrhizal symbiosis[J]. Crop Protection, 2019, 124:104837. doi: 10.1016/j.cropro.2019.05.031 URL
[54]	Stephan BI, Colombo RP, Silvani VA, et al. Short-term effects of genetically modified potato on arbuscular mycorrhizal fungal communities[J]. Journal of Soil Science and Plant Nutrition, 2019, 19(2):352-356. doi: 10.1007/s42729-019-00035-w
[55]	Wu JR, Yu MZ, Xu JH, et al. Impact of transgenic wheat with wheat yellow mosaic virus resistance on microbial community diversity and enzyme activity in rhizosphere soil[J]. PLoS One, 2014, 9(6):e98394. doi: 10.1371/journal.pone.0098394 URL
[56]	Zhang ZH, Liu Y, Yu CG, et al. Genetically modified WYMV-resistant wheat exerts little influence on rhizosphere microbial communities[J]. Applied Soil Ecology, 2016, 105:169-176. doi: 10.1016/j.apsoil.2016.04.016 URL
[57]	张玉池, 王晓蕾, 徐文蓉, 等. 国内外抗除草剂基因专利的分析[J]. 杂草学报, 2017, 35(2):1-22.
	Zhang YC, Wang XL, Xu WR, et al. Analysis on the patents of herbicide resistance gene at home and abroad[J]. Journal of Weed Science, 2017, 35(2):1-22.
[58]	王园园, 王敏, 相世刚, 等. 全球抗除草剂转基因作物转化事件分析[J]. 农业生物技术学报, 2018, 26(1):167-175.
	Wang YY, Wang M, Xiang SG, et al. Analysis on the event of global herbicide tolerant transgenic crops[J]. Journal of Agricultural Biotechnology, 2018, 26(1):167-175.
[59]	Vital-López L, Cruz-Hernández M, Fernández-Dávila S, et al. Bacterial diversity in the rhizosphere of a transgenic versus a conventional maize(Zea mays)[J]. Phyton-International Journal of Experimental Botany, 2016, 85(1):210-217.
[60]	Tang T, Chen GM, Liu FX, et al. Effects of transgenic glufosinate-tolerant rapeseed(Brassica napus L.)and the associated herbicide application on rhizospheric bacterial communities[J]. Physiological and Molecular Plant Pathology, 2019, 106:246-252. doi: 10.1016/j.pmpp.2019.03.004
[61]	刘慧璐, 范巧兰, 王慧, 等. 转基因大豆对土壤微生物区系的影响[J]. 山西农业科学, 2019, 47(9):1585-1587, 1608.
	Liu HL, Fan QL, Wang H, et al. Effects of transgenic soybean on soil microbial flora[J]. Journal of Shanxi Agricultural Sciences, 2019, 47(9):1585-1587, 1608.
[62]	Girgan C, Claassens S, Fourie H. Nematode assemblages and soil microbial communities in soils associated with glyphosate-resistant soybean[J]. South African Journal of Plant and Soil, 2020(1):11-22.
[63]	张卓, 刘茂炎, 王培, 等. 抗草甘膦转基因大豆AG5601对根际微生物群落功能多样性的影响[J]. 生物技术通报, 2019, 35(7):17-24.
	Zhang Z, Liu MY, Wang P, et al. Effects of roundup ready soybean AG5601 on the functional diversity of microbial community in rhizospheric soil[J]. Biotechnology Bulletin, 2019, 35(7):17-24.
[64]	Babujia LC, Silva AP, Nakatani AS, et al. Impact of long-term cropping of glyphosate-resistant transgenic soybean[Glycine max(L.)Merr. ]on soil microbiome[J]. Transgenic Research, 2016, 25:425-440. doi: 10.1007/s11248-016-9938-4 URL
[65]	Lu GH, Tang CY, Hua XM, et al. Effects of an EPSPS-transgenic soybean line ZUTS31 on root-associated bacterial communities during field growth[J]. PLoS One, 2018, 13(2):e0192008. doi: 10.1371/journal.pone.0192008 URL
[66]	He M, Zhang JC, Shen LB, et al. High-throughput sequencing analysis of microbial community diversity in response to indica and japonica bar-transgenic rice paddy soils[J]. PLoS One, 2019, 14(9):e0222191. doi: 10.1371/journal.pone.0222191 URL
[67]	Wen ZL, Yang MK, Du MH, et al. Enrichments/Derichments of root-associated bacteria related to plant growth and nutrition caused by the growth of an EPSPS-transgenic maize line in the field[J]. Frontiers in Microbiology, 2019, 10:1335. doi: 10.3389/fmicb.2019.01335 URL
[68]	Strain KE, Lydy MJ. The fate and transport of the Cry1Ab protein in an agricultural field and laboratory aquatic microcosms[J]. Chemosphere, 2015, 132:94-100. doi: 10.1016/j.chemosphere.2015.03.005 URL
[69]	LeBlanc PM, Hamelin RC, Filion M. Alteration of soil rhizosphere communities following genetic transformation of white spruce[J]. Applied and Environmental Microbiology, 2007, 73(13):4128-4134. doi: 10.1128/AEM.02590-06 URL
[70]	Lv YP, Cai HS, Yu JP, et al. Biosafety assessment of GFP transplastomic tobacco to rhizosphere microbial community[J]. Ecotoxicology, 2014, 23(4):718-725. doi: 10.1007/s10646-014-1185-y URL
[71]	Ammann K. Effects of biotechnology on biodiversity:herbicide-tolerant and insect-resistant GM crops[J]. Trends in Biotechnology, 2005, 23(8):388-394. pmid: 15979178
[72]	Klümper W, Qaim M. A meta-analysis of the impacts of genetically modified crops[J]. PLoS One, 2014, 9(11):e111629. doi: 10.1371/journal.pone.0111629 URL
[73]	Höflich G, Tauschke M, Kühn G, et al. Influence of long-term conservation tillage on soil and rhizosphere microorganisms[J]. Biology and Fertility of Soils, 1999, 29(1):81-86. doi: 10.1007/s003740050528 URL
[74]	Bolliger A, Magid J, Amado JCT, et al. Taking stock of the Brazilian “zero-till revolution”:A review of landmark research and Farmers’ practice[J]. Advances in Agronomy, 2006, 91:49-111.
[75]	Bardgett RD. Causes and consequences of biological diversity in soil[J]. Zoology, 2002, 105(4):367-375. doi: 10.1078/0944-2006-00072 URL
[76]	Tilman D, Reich PB, Knops J, et al. Diversity and productivity in a long-term grassland experiment[J]. Science, 2001, 294(5543):843-845. pmid: 11679667

转基因作物 GM plant	外源基因 Foreign gene	试验条件 Trial condition	监测期 Monitoring period/year	方法 Methods	结论 Conclusion
棉花	CrylAc、CpTI	大田	2	CFUs	对根际土壤微生物种群无显著差异^[22]
水稻	CrylAc、CpTI	大田	1	PCR-DGGE、qPCR	对根际土壤细菌和真菌群落组成及丰度没有产生显著影响^[23]
玉米	Bt	大田	3	T-RFLP	土壤有机质转化及所涉及的细菌和真菌群落没有不良影响^[24]
玉米	Bt	大田	3	T-RFLP、菌落PCR、U-焦磷酸测序	表达的Cry1Ab蛋白对连续种植Bt玉米的土壤和根系AMF群落的多样性影响较小^[25]
玉米	CrylAb	大田	2	T-RFLP、焦磷酸测序	没有对土壤生态系统有任何影响^[26]
玉米	Bt	大田	1	焦磷酸测序	土壤空间异质性对共生丛枝菌根真菌群落和植物生长发育的影响大于苏云金芽胞杆菌毒素基因的遗传修饰^[27]
棉花	Bt	大田	2	CFUs	对轻度嗜盐菌、溶磷菌、氨化菌、硝化菌和反硝化菌群落无显著影响^[28]
棉花	Cry1Ac	大田	3	CFUs	对巴基斯坦土壤安全没有较大影响^[29]
棉花	Bt	大田	3	CFUs、PCR-DGGE	对根际土壤微生物群落没有明显影响^[30]
棉花	Cry1Ac	大田	1	CFUs	对土壤的代谢、微生物活性和养分动态没有负面影响^[31]
棉花	Bt、CpTI	大田	1	qPCR、T-RFLP	对功能微生物无不良影响^[32]
棉花	Bt、CpTI	盆栽	1	PCR-DGGE	对土壤生态系统影响不大^[33]
玉米	Bt	温室	3	CFUs	对磷细菌和钾细菌影响不大^[34]
玉米	Bt	大田	1	qPCR	与对照BPP基因丰度相似^[35]
水稻	Bt	大田	8	ELISA	长期栽培Bt水稻不太可能导致Bt蛋白在土壤中的积累^[36]
棉花	CrylAb/lAc	大田	3	PCR-DGGE、qPCR、焦磷酸测序	对细菌种群大小和群落结构没有明显影响^[37]
棉花	Bt	大田	1	Illumina MiSeq测序	对土壤细菌群落结构没有影响^[38]
棉花	CrylAc、CpTI	大田	1	qPCR、Illumina MiSeq测序	对土壤细菌群落结构没有显著影响^[39]
棉花	CrylAc、CpTI	大田	3	焦磷酸测序	对土壤细菌多样性没有影响^[40]
玉米	Cry1Ie	大田	2	qPCR、Illumina MiSeq测序	对根际细菌群落没有显著差异^[41]
水稻	Bt	大田、培养皿	1	T-RFLP、qPCR	对土壤微生物群落没有不良影响^[42]
玉米	Bt	温室	2	Illumina MiSeq测序	对AMF多样性和丰富度和群落组成无显著影响^[43]
油菜	Bt	网箱	1	CFUs、Biolog微孔板	对可培养微生物数量和根际微生物碳源利用能力和功能多样性的影响不大^[44]
水稻	Cry1Ab	温室	1	RNA-SIP、SSU rRNA基因克隆文库	将cry1Ab基因插入水稻基因组,有可能改变水稻根际产甲烷菌群落的组成^[45]
棉花	Bt	大田	1	CFUs	在生长发育期和收获期根际细菌数量显著高于非Bt棉^[46]
水稻	CrylAb/lAc	温室	1	DNA-SIP、PCR-DGGE、 16S rRNA 基因克隆文库、焦磷酸测序	根际功能活性产甲烷菌的丰度与对照比显著降低^[47]
玉米	Bt	大田	1	Illumina MiSeq测序	对土壤微生物群落结构和物种多样性产生了一定影响^[48]

转基因作物 GM plant	外源基因 Foreign gene	试验条件 Trial condition	监测期 Monitoring period/year	方法 Methods	结论 Conclusion
棉花	CrylAc、CpTI	大田	2	CFUs	对根际土壤微生物种群无显著差异^[22]
水稻	CrylAc、CpTI	大田	1	PCR-DGGE、qPCR	对根际土壤细菌和真菌群落组成及丰度没有产生显著影响^[23]
玉米	Bt	大田	3	T-RFLP	土壤有机质转化及所涉及的细菌和真菌群落没有不良影响^[24]
玉米	Bt	大田	3	T-RFLP、菌落PCR、U-焦磷酸测序	表达的Cry1Ab蛋白对连续种植Bt玉米的土壤和根系AMF群落的多样性影响较小^[25]
玉米	CrylAb	大田	2	T-RFLP、焦磷酸测序	没有对土壤生态系统有任何影响^[26]
玉米	Bt	大田	1	焦磷酸测序	土壤空间异质性对共生丛枝菌根真菌群落和植物生长发育的影响大于苏云金芽胞杆菌毒素基因的遗传修饰^[27]
棉花	Bt	大田	2	CFUs	对轻度嗜盐菌、溶磷菌、氨化菌、硝化菌和反硝化菌群落无显著影响^[28]
棉花	Cry1Ac	大田	3	CFUs	对巴基斯坦土壤安全没有较大影响^[29]
棉花	Bt	大田	3	CFUs、PCR-DGGE	对根际土壤微生物群落没有明显影响^[30]
棉花	Cry1Ac	大田	1	CFUs	对土壤的代谢、微生物活性和养分动态没有负面影响^[31]
棉花	Bt、CpTI	大田	1	qPCR、T-RFLP	对功能微生物无不良影响^[32]
棉花	Bt、CpTI	盆栽	1	PCR-DGGE	对土壤生态系统影响不大^[33]
玉米	Bt	温室	3	CFUs	对磷细菌和钾细菌影响不大^[34]
玉米	Bt	大田	1	qPCR	与对照BPP基因丰度相似^[35]
水稻	Bt	大田	8	ELISA	长期栽培Bt水稻不太可能导致Bt蛋白在土壤中的积累^[36]
棉花	CrylAb/lAc	大田	3	PCR-DGGE、qPCR、焦磷酸测序	对细菌种群大小和群落结构没有明显影响^[37]
棉花	Bt	大田	1	Illumina MiSeq测序	对土壤细菌群落结构没有影响^[38]
棉花	CrylAc、CpTI	大田	1	qPCR、Illumina MiSeq测序	对土壤细菌群落结构没有显著影响^[39]
棉花	CrylAc、CpTI	大田	3	焦磷酸测序	对土壤细菌多样性没有影响^[40]
玉米	Cry1Ie	大田	2	qPCR、Illumina MiSeq测序	对根际细菌群落没有显著差异^[41]
水稻	Bt	大田、培养皿	1	T-RFLP、qPCR	对土壤微生物群落没有不良影响^[42]
玉米	Bt	温室	2	Illumina MiSeq测序	对AMF多样性和丰富度和群落组成无显著影响^[43]
油菜	Bt	网箱	1	CFUs、Biolog微孔板	对可培养微生物数量和根际微生物碳源利用能力和功能多样性的影响不大^[44]
水稻	Cry1Ab	温室	1	RNA-SIP、SSU rRNA基因克隆文库	将cry1Ab基因插入水稻基因组,有可能改变水稻根际产甲烷菌群落的组成^[45]
棉花	Bt	大田	1	CFUs	在生长发育期和收获期根际细菌数量显著高于非Bt棉^[46]
水稻	CrylAb/lAc	温室	1	DNA-SIP、PCR-DGGE、 16S rRNA 基因克隆文库、焦磷酸测序	根际功能活性产甲烷菌的丰度与对照比显著降低^[47]
玉米	Bt	大田	1	Illumina MiSeq测序	对土壤微生物群落结构和物种多样性产生了一定影响^[48]

转基因作物 GM plant	外源基因 Foreign gene	试验条件 Trial condition	监测期 Monitoring period/year	方法 Methods	结论 Conclusion
豌豆	Antifungal	大田	1	qPCR	对丛枝菌根真菌根系定殖无影响^[49]
油菜	Antifungal synthetic chitinase	温室	1	qPCR、RISA	对根际微生物多样性没有显著差异^[50]
油菜	Antifungal synthetic chitinase	温室	2	qPCR、CFUs	与对照的根际可培养真菌、放线菌和细菌的数量没有明显差异^[51]
棉花	T₂ chitinase	温室	1	CFUs、PCR-DGGE	对根际可培养细菌和真菌的数量和群落结构没有显著影响^[52]
马铃薯	4个Antifungal 基因	温室	1	CFUs	对AM真菌定殖没有不良影响^[53]
马铃薯	4个Antifungal 基因	温室	1	RFLP	对AM真菌正常定殖无不良影响^[54]
小麦	WYMV-Nib8	大田	2	PCR-DGGE、Band测序	对根际土壤微生物群落多样性和酶活性没有不良影响^[55]
小麦	WYMV RdRp	大田	1	PCR-DGGE、Biolog微孔板	与亲本间的根际微生物群落结构和功能多样性无差异^[56]

转基因作物 GM plant	外源基因 Foreign gene	试验条件 Trial condition	监测期 Monitoring period/year	方法 Methods	结论 Conclusion
豌豆	Antifungal	大田	1	qPCR	对丛枝菌根真菌根系定殖无影响^[49]
油菜	Antifungal synthetic chitinase	温室	1	qPCR、RISA	对根际微生物多样性没有显著差异^[50]
油菜	Antifungal synthetic chitinase	温室	2	qPCR、CFUs	与对照的根际可培养真菌、放线菌和细菌的数量没有明显差异^[51]
棉花	T₂ chitinase	温室	1	CFUs、PCR-DGGE	对根际可培养细菌和真菌的数量和群落结构没有显著影响^[52]
马铃薯	4个Antifungal 基因	温室	1	CFUs	对AM真菌定殖没有不良影响^[53]
马铃薯	4个Antifungal 基因	温室	1	RFLP	对AM真菌正常定殖无不良影响^[54]
小麦	WYMV-Nib8	大田	2	PCR-DGGE、Band测序	对根际土壤微生物群落多样性和酶活性没有不良影响^[55]
小麦	WYMV RdRp	大田	1	PCR-DGGE、Biolog微孔板	与亲本间的根际微生物群落结构和功能多样性无差异^[56]

转基因作物 GM plant	外源基因 Foreign gene	试验条件 Trial condition	监测期 Monitoring period/year	方法 Methods	结论 Conclusion
玉米	Pat	温室	1	PCR-DGGE	对根际细菌群落结构没有不良影响^[59]
油菜	Glufosinate tolerant	温室	1	Illumina MiSeq测序	对根际细菌群落组成没有显著差异^[60]
大豆	Herbicide tolerant	盆栽	1	CFUs	对土壤微生物种群没有影响^[61]
大豆	Glyphosate resistant	大田	1	Illumina MiSeq测序	对微生物群落结构的差异不显著^[62]
大豆	mEPSPS	大田	1	Biolog 微孔板	对根际土壤微生物群落功能多样性没有产生显著差异^[63]
大豆	EPSPS	大田	10	PCR-DGGE、焦磷酸测序	与对照间的微生物分类和功能丰度有差异^[64]
大豆	EPSPS	大田	1	Illumina MiSeq测序	在生长发育期和种子灌浆期对根际细菌群落有短暂的影响^[65]
水稻	Bar	大田	1	Illumina MiSeq测序	对土壤细菌的影响与常规稻不同^[66]
玉米	EPSPS	大田	1	Illumina MiSeq测序	根际微生物丰度存在一定差异,但对土壤细菌群落结构无显著差异^[67]