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

Abstract

Background 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. Results 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. Conclusion 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. Graphical abstract

Reactive Oxygen Species Partly Mediate DNA Methylation in Responses to Different Heavy Metals in Pokeweed

“…For example, Feng et al (2016) reported that Cd-responsive gene expression may be modified by DNA methylation in rice exposed to Cd. Our recent study of pokeweed also proved that DNA methylation variation induced by bacteria can regulate gene expression ( Chen et al, 2022 ). Although transcriptome analysis of P. americana L. in response to Cd stress have been reported before ( Chen et al, 2017 ), they did not pay attention to the effect of DNA methylation on gene expression and did not compare the difference of DEG under Mn and Cd stress.…”

“…Epigenetic variation which can regulate phenotypic variation could be one potentially important way for plant in response to environmental changes ( Niederhuth and Schmitz, 2014 ; Wibowo et al, 2016 ; Li et al, 2021 ). DNA methylation is one of the main epigenetic mechanisms enabling adaptation of plants in complex environments ( Niederhuth and Schmitz, 2014 ; Chang et al, 2019 ; Perrone and Martinelli, 2020 ; Li et al, 2021 ; Chen et al, 2022 ). Changes of DNA methylation in response to environmental stresses can be relatively stable, and establish a DNA methylation-dependent stress memory to the offspring ( Wibowo et al, 2016 ; Williams and Gehring, 2017 ; Sudan et al, 2018 ).…”

“…DNA methylation in gene body usually enhances genetic transcription, and DNA methylation in gene promoters and transposable elements is correlated to gene and transposon silencing ( Zhang et al, 2006 , 2018 ; Feng et al, 2016 ; Bewick and Schmitz, 2017 ). Besides, the environmental stress can cause changes in gene expression through hypomethylation or hypermethylation of DNA ( Chinnusamy and Zhu, 2009 ; Chen et al, 2022 ). Furthermore, the methylation variation induced by heavy metal stress might be functional as transgenerational memory ( Ou et al, 2012 ; Cong et al, 2019 ).…”

“…Pokeweed ( Phytolacca americana L.) is a perennial herb that thrives in heavy metal-contaminated habitats ( Chen et al, 2015 ). Pokeweed has been reported as both manganese (Mn) and Cd hyperaccumulator, and can be used for phytoremediation ( Peng et al, 2008 ; Gao et al, 2013 ; Chen et al, 2015 , 2022 ). Mn is an essential element which is necessary for plant growth as a component of many enzymes, while Cd is non-essential element.…”

“…The ability of pokeweed to flourish in Mn and Cd contaminated habitats is due to its high tolerance to both metals, despite their differing physiological functions and effects. Thus, pokeweed could be a good model to explore the DNA methylation patterns under stress caused by different types of heavy metals ( Chen et al, 2022 ). Meanwhile, the role of metal-induced ROS in DNA methylation variation can be investigated.…”