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Growth- and health-promoting bacteria can boost crop productivity in a sustainable way. Pseudomonas simiae WCS417 is such a bacterium that efficiently colonizes roots, modifies the architecture of the root system to increase its size, and induces systemic resistance to make plants more resistant to pests and pathogens. Our previous work suggested that WCS417-induced phenotypes are controlled by root cell-type-specific mechanisms. However, it remains unclear how WCS417 affects these mechanisms. In this study, we transcriptionally profiled five Arabidopsis thaliana root cell types following WCS417 colonization. We found that the cortex and endodermis have the most differentially expressed genes, even though they are not in direct contact with this epiphytic bacterium. Many of these genes are associated with reduced cell wall biogenesis, and mutant analysis suggests that this downregulation facilitates WCS417-driven root architectural changes. Furthermore, we observed elevated expression of suberin biosynthesis genes and increased deposition of suberin in the endodermis of WCS417-colonized roots. Using an endodermal barrier mutant, we showed the importance of endodermal barrier integrity for optimal plant-beneficial bacterium association. Comparison of the transcriptome profiles in the two epidermal cell types that are in direct contact with WCS417—trichoblasts that form root hairs and atrichoblasts that do not—implies a difference in potential for defense gene activation. While both cell types respond to WCS417, trichoblasts displayed both higher basal and WCS417-dependent activation of defense-related genes compared with atrichoblasts. This suggests that root hairs may activate root immunity, a hypothesis that is supported by differential immune responses in root hair mutants. Taken together, these results highlight the strength of cell-type-specific transcriptional profiling to uncover “masked” biological mechanisms underlying beneficial plant-microbe association

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 do not -- 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.

Plants have incredible developmental plasticity, enabling them to respond to a wide range of environmental conditions. Among these conditions is the presence of plant growth-promoting rhizobacteria (PGPR) in the soil. Recent studies show that PGPR affect Arabidopsis thaliana root growth and development by modulating cell division and differentiation in the primary root and influencing lateral root development. These effects lead to dramatic changes in root system architecture that significantly impact aboveground plant growth. Thus, PGPR may promote shoot growth via their effect on root developmental programs. This review focuses on contextualizing root developmental changes elicited by PGPR in light of our understanding of plant-microbe interactions and root developmental biology.