Loss of a plant receptor kinase recruits beneficial rhizosphere-associatedPseudomonas

Abstract

Maintaining microbiome structure is critical for the health of both plants and animals. In plants, enrichment of beneficial bacteria is associated with advantageous outcomes including protection from biotic and abiotic stress. However, the genetic and molecular mechanisms by which plants enrich for specific beneficial microbes without general dysbiosis have remained elusive. By rescreening a collection of Arabidopsis mutants that affect root immunity under gnotobiotic conditions, followed by microbiome sequencing in natural soil, we identified a FERONIA mutant (fer-8) with a rhizosphere microbiome enriched in Pseudomonas fluorescens without phylum-level dysbiosis. Using microbiome transplant experiments, we found that the fer-8 microbiome was beneficial and promoted plant growth. The effect of FER on rhizosphere Pseudomonads was independent of its immune coreceptor function, role in development, and jasmonic acid autoimmunity. We found that the fer-8 mutant has reduced basal levels of reactive oxygen species (ROS) in roots and that mutants deficient in NADPH oxidase showed elevated rhizosphere Pseudomonad levels. Overexpression of the ROP2 gene (encoding a client of FER and positive regulator of NADPH oxidase) in fer-8 plants suppressed Pseudomonad overgrowth. This work shows that FER-mediated ROS production regulates levels of beneficial Pseudomonads in the rhizosphere microbiome.

Protective role of the Arabidopsis leaf microbiota against a bacterial pathogen

“…This poses the more general question whether protective strains are more often associated with and/or selected for by plants. There is evidence that plants can assemble a protective community 7 , 44 , recruit beneficial microbes 46 , 47 or enrich for groups of bacteria that are mostly beneficial 48 , 49 . Interestingly, in our SynCom experiments where we observed community-dependent protection, we note that in some of the drop-out experiments where we removed the most abundant strain, we indeed eliminated the most protective strain ( Fig.…”

Multi‐dimensionality as a path forward in plant‐soil feedback research

“…If genotype‐level PSFs are common, this would shed new light on the Janzen–Connell hypothesis (Liu et al., 2015), and it would also challenge how we select soils and seeds for ‘classic’ species‐level PSF experiments. Recently, further progress also has been made by linking plant gene functions and expression profiles to metabolic pathways (Song et al., 2020; Wang et al., 2018). In combination with metatranscriptomic analysis of rhizosphere communities (Turner et al., 2013), this opens new avenues to explore the physiological links between plant roots and rhizosphere microbial communities at the level of root metabolic diversity (Fitzpatrick et al., 2020; van Dam & Bouwmeester, 2016; Figure 5).…”

New paradigms in cell adaptation: decades of discoveries on the CrRLK1L receptor kinase signalling network

“…RALF‐like peptides from nematodes can trigger rapid alkalinization and inhibit ROS production in their hosts through FER signalling (Zhang et al ., 2020a). FER‐mediated ROS production regulates the levels of beneficial pseudomonads present within the root rhizosphere microbiome (Song et al ., 2021). LET1 and LET2 activate NLR SUPPRESSOR OF MKK1 MKK2 2 (SUMM2)‐mediated autoimmunity via MAPK kinase kinase 2 (MEKK2) scaffolding (Liu et al ., 2020) and the formation of the LET1‐LET2‐LLG1 trimeric complex (Huang et al ., 2020b).…”

“…Cr RLK1L signalling also provides central contributions to PTI and ETI (Kessler et al ., 2010; Masachis et al ., 2016; Mang et al ., 2017; Merz et al ., 2017; Qu et al ., 2017; Stegmann et al ., 2017; Engelsdorf et al ., 2018; Zhang et al ., 2020a). The fer‐8 allele (which harbours a G1793A missense mutation in the FER coding sequence) shows a reduced accumulation of ROS in its roots relative to the wild‐type, which results in increased susceptibility to rhizosphere Pseudomonas infection without phylum‐level dysbiosis (Song et al ., 2021).…”