Root Microbiome Modulates Plant Growth Promotion Induced by Low Doses of Glyphosate

Root Microbiome Modulates Plant Growth Promotion Induced by Low Doses of Glyphosate
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DOI:
10.1128/msphere.00484-20
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发表时间:
2020-08
期刊:
影响因子:
4.8
通讯作者:
D. Ramirez-Villacis;Omri M. Finkel;Isai Salas-González;Connor R. Fitzpatrick;J. Dangl;Corbin D. Jones;A. Leon-Reyes
D. Ramirez-Villacis;Omri M. Finkel;Isai Salas-González;Connor R. Fitzpatrick;J. Dangl;Corbin D. Jones;A. Leon-Reyes
中科院分区:
生物学2区
文献类型:
--
作者:
D. Ramirez-Villacis;Omri M. Finkel;Isai Salas-González;Connor R. Fitzpatrick;J. Dangl;Corbin D. Jones;A. Leon-Reyes

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自从抗草甘膦作物问世以来,草甘膦已成为世界上最常见和最广泛使用的除草剂。由于其密集使用和结合土壤颗粒的能力,它可以在环境中以低浓度存在。草甘膦残留物对植物的影响尚未得到广泛研究;然而,在实验室和温室实验中,草甘膦浓度比推荐的田间剂量低1,000至100,000倍,可促进几个物种的生长。然而,这种效应在农业领域很少观察到,在农业领域,复杂的微生物群落在植物对外部线索的反应中起着核心作用。我们的研究揭示了根相关细菌如何调节拟南芥对低剂量草甘膦的反应,在生长促进和生长抑制之间转换。甘草甜素是一种常用的除草剂,作用谱广。然而,在亚致死剂量下,草甘膦可以诱导植物生长,这种现象称为毒物兴奋效应。大多数草甘膦兴奋效应研究是在无微生物或微生物多样性减少的条件下进行的;只有少数是在开放系统或农田中进行的,其中包括土壤微生物的多样性较高。在这里,我们研究了微生物如何影响低剂量草甘膦诱导的兴奋效应。为此,我们使用了拟南芥和一个充分表征的合成细菌群落的185株(SynCom),模拟拟南芥的根相关微生物组。我们发现,3.6 × 10−6克酸当量/升的剂量(低剂量的草甘膦,或LDG)使芽干重增加了约14%(即,激效作用)。出乎意料的是,在接种SynCom的植物中,LDG使芽干重降低了1.17%。我们发现LDG在根中富集了两个厚壁菌门和两个伯克霍尔德氏菌菌株。已知这些特定菌株在单缔合测定中充当根生长抑制剂(RGI)。我们测试了RGI和拍摄干重减少LDG组装一个新的合成社区缺乏RGI菌株之间的联系。将RGI菌株从群落中去除恢复了LDG的生长诱导。最后,我们表明,个别RGI菌株从几个特定的门是足以切换到LDG的反应,从生长促进生长抑制。我们的研究结果表明,草甘膦兴奋效应完全取决于根微生物组的组成,特别是根生长抑制剂菌株的存在。自从抗草甘膦作物问世以来,草甘膦已成为世界上最常见和最广泛使用的除草剂。由于其密集使用和结合土壤颗粒的能力,它可以在环境中以低浓度存在。草甘膦残留物对植物的影响尚未得到广泛研究;然而,在实验室和温室实验中,草甘膦浓度比推荐的田间剂量低1,000至100,000倍,可促进几个物种的生长。然而,这种效应在农业领域很少观察到,在农业领域,复杂的微生物群落在植物对外部线索的反应中起着核心作用。我们的研究揭示了根相关细菌如何调节拟南芥对低剂量草甘膦的反应,在生长促进和生长抑制之间转换。
Since the introduction of glyphosate-resistant crops, glyphosate has become the most common and widely used herbicide around the world. Due to its intensive use and ability to bind to soil particles, it can be found at low concentrations in the environment. The effect of these remnants of glyphosate in plants has not been broadly studied; however, glyphosate 1,000 to 100,000 times less concentrated than the recommended field dose promoted growth in several species in laboratory and greenhouse experiments. However, this effect is rarely observed in agricultural fields, where complex communities of microbes have a central role in the way plants respond to external cues. Our study reveals how root-associated bacteria modulate the responses of Arabidopsis to low doses of glyphosate, shifting between growth promotion and growth inhibition. ABSTRACT Glyphosate is a commonly used herbicide with a broad action spectrum. However, at sublethal doses, glyphosate can induce plant growth, a phenomenon known as hormesis. Most glyphosate hormesis studies have been performed under microbe-free or reduced-microbial-diversity conditions; only a few were performed in open systems or agricultural fields, which include a higher diversity of soil microorganisms. Here, we investigated how microbes affect the hormesis induced by low doses of glyphosate. To this end, we used Arabidopsis thaliana and a well-characterized synthetic bacterial community of 185 strains (SynCom) that mimics the root-associated microbiome of Arabidopsis. We found that a dose of 3.6 × 10−6 g acid equivalent/liter (low dose of glyphosate, or LDG) produced an ∼14% increase in the shoot dry weight (i.e., hormesis) of uninoculated plants. Unexpectedly, in plants inoculated with the SynCom, LDG reduced shoot dry weight by ∼17%. We found that LDG enriched two Firmicutes and two Burkholderia strains in the roots. These specific strains are known to act as root growth inhibitors (RGI) in monoassociation assays. We tested the link between RGI and shoot dry weight reduction in LDG by assembling a new synthetic community lacking RGI strains. Dropping RGI strains out of the community restored growth induction by LDG. Finally, we showed that individual RGI strains from a few specific phyla were sufficient to switch the response to LDG from growth promotion to growth inhibition. Our results indicate that glyphosate hormesis was completely dependent on the root microbiome composition, specifically on the presence of root growth inhibitor strains. IMPORTANCE Since the introduction of glyphosate-resistant crops, glyphosate has become the most common and widely used herbicide around the world. Due to its intensive use and ability to bind to soil particles, it can be found at low concentrations in the environment. The effect of these remnants of glyphosate in plants has not been broadly studied; however, glyphosate 1,000 to 100,000 times less concentrated than the recommended field dose promoted growth in several species in laboratory and greenhouse experiments. However, this effect is rarely observed in agricultural fields, where complex communities of microbes have a central role in the way plants respond to external cues. Our study reveals how root-associated bacteria modulate the responses of Arabidopsis to low doses of glyphosate, shifting between growth promotion and growth inhibition.