Plants grown in natural soil are colonized by phylogenetically structured communities of microbes known as the microbiota. Individual microbes can activate microbe-associated molecular pattern (MAMP)-triggered immunity (MTI), which limits pathogen proliferation but curtails plant growth, a phenomenon known as the growth–defence trade-off. Here, we report that, in monoassociations, 41% (62 out of 151) of taxonomically diverse root bacterial commensals suppress Arabidopsis thaliana root growth inhibition (RGI) triggered by immune-stimulating MAMPs or damage-associated molecular patterns. Amplicon sequencing of bacterial 16S rRNA genes reveals that immune activation alters the profile of synthetic communities (SynComs) comprising RGI-non-suppressive strains, whereas the presence of RGI-suppressive strains attenuates this effect. Root colonization by SynComs with different complexities and RGI-suppressive activities alters the expression of 174 core host genes, with functions related to root development and nutrient transport. Furthermore, RGI-suppressive SynComs specifically downregulate a subset of immune-related genes. Precolonization of plants with RGI-suppressive SynComs, or mutation of one commensal-downregulated transcription factor, MYB15, renders the plants more susceptible to opportunistic Pseudomonas pathogens. Our results suggest that RGI-non-suppressive and RGI-suppressive root commensals modulate host susceptibility to pathogens by either eliciting or dampening MTI responses, respectively. This interplay buffers the plant immune system against pathogen perturbation and defence-associated growth inhibition, ultimately leading to commensal–host homeostasis.

The plant microbiome can promote plant health and productivity through a multitude of mechanisms. Our understanding of plant–microbiome interaction relies on descriptive natural surveys and experiments performed under simplified laboratory environments. While reductionist approaches are essential to understand mechanisms of plant–microbiome interactions, they risk missing emergent community properties seen in nature. To bridge the gap between basic research and real-world deployment of the microbiome for translational application, one has to consider functional association as well as ecologic principles governing interspecies and interkingdom interactions. In this review, we discuss the beneficial potential of plant microbiomes to enhance plant growth, nutrition, stress tolerance, pathogen protection, and commercial value through the modulation of taste and flavors, using examples from model plants and agriculturally important crops. We then discuss how microbial invasion and persistence in standing communities, trade-offs under multiple stressors, and community instability under host- and environment-imposed modulation should be considered in the rational design of microbial inocula, followed by a scrutiny of the method of microbial delivery. We synthesize ideas on how multiomic data, including genomics, transcriptomes, and metabolomics, can be leveraged to identify strains or target genes of interest for functional studies and how machine learning algorithms can be incorporated to enable prediction of plant–microbiome interactions. Microbiome-based strategies hold promise for improvements in agriculture. Despite the intrinsic complexity of the underlying interactions, interdisciplinary approaches are constantly providing insight into microbiome functioning and assembly principles, which is key toward knowledge-based engineering of the microbiome for increased and sustainable crop performance.

Summary: The Tubby domain, named after the TUBBY protein in mice, binds to phosphatidylinositol 4,5‐bisphosphate. Arabidopsis has 11 Tubby domain‐containing proteins referred to as Tubby‐Like Proteins (TLPs). Of the 11 TLPs, 10 possess the N‐terminal F‐box domain, which can interact with SKP‐like proteins and form SKP1‐Cullin‐F‐box E3 ligase complexes. Although mice TUBBY has been extensively studied, plant TLPs' functions are scarcely detailed. In this study, we show that the Arabidopsis Tubby‐like protein 6 (TLP6) and its redundant homologs, TLP1, TLP2, TLP5, and TLP10, positively regulate Arabidopsis immune responses. Furthermore, in an immunoprecipitation mass spectrometry analysis to search for ubiquitination substrates of the TLPs, we identified two redundant phosphoinositide biosynthesis enzymes, phosphatidylinositol 4‐kinase β proteins (PI4Kβs), PI4Kβ1 and PI4Kβ2, as TLP interactors. Importantly, TLP6 overexpression lines fully phenocopy the phenotypes of the pi4kβ1,2 mutant, while TLP6 overexpression also leads to increased PI4Kβ2 ubiquitination and reduction in its protein level in a proteasome‐dependent manner. Most significantly, TLP6 overexpression does not further enhance the autoimmunity of the pi4kβ1,2 double mutant, supporting the hypothesis that TLP6 targets the PI4Kβs for ubiquitination and degradation. Thus, our study reveals a novel mechanism where TLPs promote plant immune responses by modulating the PI4Kβs protein levels.

Plants interact with structured microbial communities called the microbiota, which can have a profound impact on plant growth and health. However, how plants perceive and respond to specific core microbiota members at a molecular level is still unclear. We identified natural variation in Arabidopsis thaliana root responses to bacterial strains of the genus Pseudomonas , a core genus of the plant microbiota. Some A. thaliana accessions such as Van-0 show strong root responses to Pseudomonas strains, including changes in root system architecture and transcriptional reprogramming. Through a forward genetic screen using Pseudomonas isolate R569, we found that the nuo NADH dehydrogenase complex, part of the bacterial electron transport chain, contributes to the bacterial activity on Van-0 roots. Using recombinant inbred lines, we further mapped a multigenic quantitative trait locus in the host that is associated with the root responses. In Van-0, the exocyst subunit EXO70E2 positively contributes to the response, while Col-0 haplotypes of malectin-like and leucine-rich-repeat domain-containing receptor-like kinases play an inhibitory role. The identification of these components in the bacteria and the host establishes a genetic framework for how root developmental plasticity is integrated with the microbe-rich soil environment and is subject to intraspecific natural variation.

Plants must obtain all of their mineral nutrients from the soil around their roots. To complete their life cycle even if nutrients are limiting, plants have developed various strategies, such as altering their root architecture to improve nutrient scavenging or modifying their metabolism to reduce the demands for certain elements ( Li et al., 2007; Gruber et al., 2013; Aarabi et al., 2016). When sulfur is limiting, Arabidopsis (Arabidopsis thaliana) and other Brassicaceae species downregulate the biosynthesis of sulfur-rich glucosinolates. SULFUR DEFICIENCY INDUCED (SDI) proteins, induced under sulfur starvation, interact with and repress MYB transcription factors, suppressing the transcription of genes encoding glucosinolate biosynthesis enzymes.