Cell-type specific transcriptomics reveals roles for root hairs and endodermal barriers in interaction with beneficial rhizobacterium

Abstract

Growth-promoting bacteria can boost crop productivity in a sustainable way. Pseudomonas simiae WCS417 is a well-studied bacterium that promotes growth of many plant species. Upon colonization, WCS417 affects root system architecture resulting in an expanded root system. Both immunity and root system architecture, are controlled by root-cell-type specific biological mechanisms, but it is unknown how WCS417 affects these mechanisms. Therefore, here, we transcriptionally profiled five Arabidopsis thaliana root cell types following WCS417 colonization. The cortex and endodermis displayed the most differentially expressed genes, even though they were not in direct contact with this epiphytic bacterium. Many of these genes are associated with reduced cell wall biogenesis, possibly facilitating the root architectural changes observed in WCS417-colonized roots. Comparison of the transcriptome profiles in the two epidermal cell types that were in direct contact with WCS417 – trichoblasts that form root hairs and atrichoblasts that don’t – imply functional specialization. Whereas basal expression levels of nutrient uptake-related genes and defense-related genes are highest in trichoblasts and atrichoblasts, respectively, upon exposure to WCS417 these roles revert. This suggests that root hairs participate in the activation of root immunity, further supported by attenuation of immunity in a root hairless mutant. Furthermore, we observed elevated expression of suberin biosynthesis genes and increased deposition of suberin in the endodermis in WCS417-colonized roots. Using an endodermal barrier mutant we show the importance of endodermal barrier integrity for optimal plant-beneficial bacterium association. Altogether, we highlight the strength of cell-type-specific transcriptional profiling to uncover “masked” biological mechanisms underlying successful plant-microbe associations.

Microbiome-Mediated Strategies to Manage Major Soil-Borne Diseases of Tomato

“…Moreover, this effectiveness was attributed to a combination of molecular mechanisms related to plant immunity and microbial interactions, which were contributed by bacterial and fungal communities [115,116]. These findings provide insights into how microbiome dynamics affect plant immunity, and the manipulation of SynComs can be a novel strategy to mitigate FW [116]. Applying a biochar amendment can enhance plant resistance, and the existence of beneficial bacteria such as Pseudomonas can protect plants from FW [117].…”

“…A mixture of fungi and bacteria in cross-kingdom SynComs was more effective in suppressing FW than fungi or bacteria alone [115]. Moreover, this effectiveness was attributed to a combination of molecular mechanisms related to plant immunity and microbial interactions, which were contributed by bacterial and fungal communities [115,116]. These findings provide insights into how microbiome dynamics affect plant immunity, and the manipulation of SynComs can be a novel strategy to mitigate FW [116].…”

Development specifies, diversifies and empowers root immunity

“…nodule‐forming rhizobia (Dolan et al , 1993 ; Datta et al , 2011 ; Hassan & Mathesius, 2012 ; Salazar‐Henao et al , 2016 ). Interestingly, the cell type‐specific analysis of defence‐related gene expression in Arabidopsis trichoblasts versus atrichoblasts suggests a more important role for trichoblasts in immunity activation, at least in response to the beneficial rhizobacterium Pseudomonas simiae WCS417 (preprint: Verbon et al , 2022 ). Epidermis cells accumulate secondary metabolites such as dipeptides and flavonoids and regulate soil nutrient availability and microbiome composition through the exudation of organic compounds (Saslowsky & Winkel‐Shirley, 2001 ; Badri & Vivanco, 2009 ; Datta et al , 2011 ; Hassan & Mathesius, 2012 ; Moussaieff et al , 2013 ).…”

“…In addition, cortex cells of certain plant species allow for the accommodation of arbuscules and subsequent nutrient exchange in the mutualistic interaction with arbuscular mycorrhizal fungi (Lanfranco et al , 2018 ). The suberin‐containing endodermis cell layer can physically prevent pathogens from entering into the vascular stele and even limit root colonisation by beneficial microbes (Geldner, 2013 ; Robbins et al , 2014 ; Fröschel et al , 2021 ; preprint: Verbon et al , 2022 ). Recent findings indicate the endodermis‐specific synthesis of certain phenylpropanoid metabolites required for Casparian strip formation and suberin deposition in this cell type.…”

“…Interestingly, alterations in endodermal diffusion barrier functions affect plant microbiome compositions, and, vice versa, microbes can change Casparian strip and suberin depositions and thus plant mineral nutrient homeostasis. This renders the endodermis a potential regulatory hub for microbiome assembly in connection with the nutrient acquisition (Salas‐González et al , 2021 ; preprint: Verbon et al , 2022 ). It has to be noted, that Casparian strip formation and suberin deposition in the endodermis occur in distinct developmental root zones (e.g.…”