Long-term effect of epigenetic modification in plant-microbe interactions: modification of DNA methylation induced by plant growth-promoting bacteria mediates promotion process.

Long-term effect of epigenetic modification in plant-microbe interactions: modification of DNA methylation induced by plant growth-promoting bacteria mediates promotion process.
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表观遗传修饰对植物-微生物相互作用的长期影响:植物促生长细菌诱导的DNA甲基化修饰介导促进过程

DOI:
10.1186/s40168-022-01236-9
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发表时间:
2022-02-24
期刊:
影响因子:
15.5
通讯作者:
Shen Z
Shen Z
中科院分区:
生物学1区
文献类型:
--
作者:
Chen C;Wang M;Zhu J;Tang Y;Zhang H;Zhao Q;Jing M;Chen Y;Xu X;Jiang J;Shen Z

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土壤微生物群被认为是下一次绿色革命的基石,而植物生长促进细菌(PGPB)是微生物组工程的关键。然而,将有益于植物的微生物从发现到农业应用仍然具有挑战性,因为在天然土壤中有益的菌株和植物之间相互作用的机制在很大程度上仍不清楚。越来越多的研究表明,引入微生物的菌株通常会在土壤中被消除,而另一些研究报告称,应用PGPB作为接种剂可以显著促进植物的生长。这一矛盾表明,需要更深入地了解微生物诱导生长促进的潜在机制。在去除土壤中的PGPB接种物后,我们显示了PGPB诱导的长期促进植物生长的作用,并探索了植物促进生长过程中的关键元素--外源接种物、本土微生物群和植物之间的三者之间的相互作用。我们发现,根际微生物群落的组装主要是由植物的发育驱动的,根的招募大大减弱了接种剂对根际微生物群落的影响。无论是根际微生物群落的变化,还是接种菌剂在根部的定植,都不是促进植物生长的必要因素。在根中,DNA甲基化对接种的响应会影响与PGPB诱导的生长促进相关的基因表达,而接种诱导的DNA甲基化模式的中断大大削弱了植物的生长促进作用。综上所述,我们的结果表明,PGPB诱导的根DNA甲基化修饰介导了促进过程,并且这些修饰在从微生物群中消除接种物后仍然起作用。本研究提出了PGPB影响根部DNA甲基化以促进植物生长的新机制,为微生物与植物的相互作用提供了重要的见解,并为植物微生物工程提供了新的策略,超越了保持接种物在土壤中持久性的角度。视频摘要在线版本包含补充材料,可在10.1186/s40168022-022-9查阅。
Soil microbiomes are considered a cornerstone of the next green revolution, and plant growth-promoting bacteria (PGPB) are critical for microbiome engineering. However, taking plant-beneficial microorganisms from discovery to agricultural application remains challenging, as the mechanisms underlying the interactions between beneficial strains and plants in native soils are still largely unknown. Increasing numbers of studies have indicated that strains introduced to manipulate microbiomes are usually eliminated in soils, while others have reported that application of PGPB as inocula significantly improves plant growth. This contradiction suggests the need for a deeper understanding of the mechanisms underlying microbe-induced growth promotion. We showed PGPB-induced long-term plant growth promotion after elimination of the PGPB inoculum in soils and explored the three-way interactions among the exogenous inoculum, indigenous microbiome, and plant, which were key elements of the plant growth-promoting process. We found the rhizosphere microbiome assembly was mainly driven by plant development and root recruitments greatly attenuated the influence of inocula on the rhizosphere microbiome. Neither changes in the rhizosphere microbiome nor colonization of inocula in roots was necessary for plant growth promotion. In roots, modification of DNA methylation in response to inoculation affects gene expression related to PGPB-induced growth promotion, and disruptions of the inoculation-induced DNA methylation patterns greatly weakened the plant growth promotion. Together, our results showed PGPB-induced DNA methylation modifications in roots mediated the promotion process and these modifications remained functional after elimination of the inoculum from the microbiome. This study suggests a new mechanism in which PGPB affect DNA methylation in roots to promote plant growth, which provides important insights into microbiome–plant interactions and offers new strategies for plant microbiome engineering beyond the perspective of maintaining inoculum persistence in soils. Video abstract The online version contains supplementary material available at 10.1186/s40168-022-01236-9.