Plants host a mesmerizing diversity of microbes inside and around their roots, known as the microbiome. The microbiome is composed mostly of fungi, bacteria, oomycetes, and archaea that can be either pathogenic or beneficial for plant health and fitness. To grow healthy, plants need to surveil soil niches around the roots for the detection of pathogenic microbes, and in parallel maximize the services of beneficial microbes in nutrients uptake and growth promotion. Plants employ a palette of mechanisms to modulate their microbiome including structural modifications, the exudation of secondary metabolites and the coordinated action of different defence responses. Here, we review the current understanding on the composition and activity of the root microbiome and how different plant molecules can shape the structure of the root-associated microbial communities. Examples are given on interactions that occur in the rhizosphere between plants and soilborne fungi. We also present some well-established examples of microbiome harnessing to highlight how plants can maximize their fitness by selecting their microbiome. Understanding how plants manipulate their microbiome can aid in the design of next-generation microbial inoculants for targeted disease suppression and enhanced plant growth.

Summary: Below ground, microbe‐associated molecular patterns (MAMPs) of root‐associated microbiota can trigger costly defenses at the expense of plant growth. However, beneficial rhizobacteria, such as Pseudomonas simiae WCS417, promote plant growth and induce systemic resistance without being warded off by local root immune responses. To investigate early root responses that facilitate WCS417 to exert its plant‐beneficial functions, we performed time series RNA‐Seq of Arabidopsis roots in response to live WCS417 and compared it with MAMPs flg22⁴¹⁷ (from WCS417), flg22^Pa (from pathogenic Pseudomonas aeruginosa) and fungal chitin. The MAMP transcriptional responses differed in timing, but displayed a large overlap in gene identity. MAMP‐upregulated genes are enriched for genes with functions in immunity, while downregulated genes are enriched for genes related to growth and development. Although 74% of the transcriptional changes inflicted by live WCS417 overlapped with the flg22⁴¹⁷ profile, WCS417 actively suppressed more than half of the MAMP‐triggered transcriptional responses, possibly to allow the establishment of a mutually beneficial interaction with the host root. Interestingly, the sector of the flg22⁴¹⁷‐repressed transcriptional network that is not affected by WCS417 has a strong auxin signature. Using auxin response mutant tir1afb2afb3, we demonstrate a dual role for auxin signaling in finely balancing growth‐promoting and defense‐eliciting activities of beneficial microbes in plant roots.

Cross-talk between jasmonate (JA), ethylene (ET), and Salicylic acid (SA) signaling is thought to operate as a mechanism to fine-tune induced defenses that are activated in response to multiple attackers. Here, 43 Arabidopsis genotypes impaired in hormone signaling or defense-related processes were screened for their ability to express SA-mediated suppression of JA-responsive gene expression. Mutant cev1, which displays constitutive expression of JA and ET responses, appeared to be insensitive to SA-mediated suppression of the JA-responsive marker genes PDF1.2 and VSP2. Accordingly, strong activation of JA and ET responses by the necrotrophic pathogens Botrytis cinerea and Alternaria brassicicola prior to SA treatment counteracted the ability of SA to suppress the JA response. Pharmacological assays, mutant analysis, and studies with the ET-signaling inhibitor 1-methylcyclopropene revealed that ET signaling renders the JA response insensitive to subsequent suppression by SA. The APETALA2/ETHYLENE RESPONSE FACTOR transcription factor ORA59, which regulates JA/ET-responsive genes such as PDF1.2, emerged as a potential mediator in this process. Collectively, our results point to a model in which simultaneous induction of the JA and ET pathway renders the plant insensitive to future SA-mediated suppression of JA-dependent defenses, which may prioritize the JA/ET pathway over the SA pathway during multi-attacker interactions.

Jasmonic acid (JA) regulates plant defenses against necrotrophic pathogens and insect herbivores. Salicylic acid (SA) and abscisic acid (ABA) can antagonize JA‐regulated defenses, thereby modulating pathogen or insect resistance. We performed a genome‐wide association (GWA) study on natural genetic variation in Arabidopsis thaliana for the effect of SA and ABA on the JA pathway. We treated 349 Arabidopsis accessions with methyl JA (MeJA), or a combination of MeJA and either SA or ABA, after which expression of the JA‐responsive marker gene PLANT DEFENSIN1.2 (PDF1.2) was quantified as a readout for GWA analysis. Both hormones antagonized MeJA‐induced PDF1.2 in the majority of the accessions but with a large variation in magnitude. GWA mapping of the SA‐ and ABA‐affected PDF1.2 expression data revealed loci associated with crosstalk. GLYI4 (encoding a glyoxalase) and ARR11 (encoding an Arabidopsis response regulator involved in cytokinin signalling) were confirmed by T‐DNA insertion mutant analysis to affect SA–JA crosstalk and resistance against the necrotroph Botrytis cinerea. In addition, At1g16310 (encoding a cation efflux family protein) was confirmed to affect ABA–JA crosstalk and susceptibility to Mamestra brassicae herbivory. Collectively, this GWA study identified novel players in JA hormone crosstalk with potential roles in the regulation of pathogen or insect resistance.

Resistance conferred by biotrophic pathogens often requires salicylic acid (SA) signaling, whereas necrotrophic pathogens or wounding mainly activate the jasmonate/ethylene (JA/ET)-dependent pathway. Crosstalk connections between these two independent signaling pathways may lead to synergistic or antagonistic behavior. In order to shed some light on the crosstalk between these two hormones in Arabidopsis plants, a proteomic approach combined with a transcriptomic analysis has been used to identify molecules differentially expressed upon single or simultaneous treatment with both phytohormones. Twenty-five nonredundant differential proteins were revealed upon treatment with SA or JA alone or in combination, which are involved in general metabolic processes as well as in response to stress, in developmental processes, in protein metabolism and transport. Interestingly, gene expression study, carried out on genes involved in oxidative stress and in biotic and/or abiotic stress, highlighted the correspondence between proteomic and transcriptomic approaches, performed here by RT-PCR. Our data clearly demonstrate that almost all genes/proteins involved in oxidative stress as well as in biotic and/or abiotic stress are mainly induced upon JA treatment and only a few of them are overexpressed upon SA treatment. Moreover, we found that a substantially negative crosstalk is established upon the combined action of the two hormones and that generally SA exerts a negative crosstalk compared to the JA pathway. Our study corroborates the hypothesis that the combination of both phytohormones induces reprogramming of the plant transcriptome, but at the same time highlights the presence of a complex network of signaling that is far to be completely elucidated.