Since the colonization of land by ancestral plant lineages 450 million years ago, plants and their associated microbes have been interacting with each other, forming an assemblage of species that is often referred to as a “holobiont.” Selective pressure acting on holobiont components has likely shaped plant-associated microbial communities and selected for host-adapted microorganisms that impact plant fitness. However, the high microbial densities detected on plant tissues, together with the fast generation time of microbes and their more ancient origin compared to their host, suggest that microbe-microbe interactions are also important selective forces sculpting complex microbial assemblages in the phyllosphere, rhizosphere, and plant endosphere compartments. Reductionist approaches conducted under laboratory conditions have been critical to decipher the strategies used by specific microbes to cooperate and compete within or outside plant tissues. Nonetheless, our understanding of these microbial interactions in shaping more complex plant-associated microbial communities, along with their relevance for host health in a more natural context, remains sparse. Using examples obtained from reductionist and community-level approaches, we discuss the fundamental role of microbe-microbe interactions (prokaryotes and micro-eukaryotes) for microbial community structure and plant health. We provide a conceptual framework illustrating that interactions among microbiota members are critical for the establishment and the maintenance of host-microbial homeostasis.

Yield losses caused by fungal pathogens represent a major threat to global food production. One of the most devastating fungal wheat pathogens isZymoseptoria tritici. Despite the importance of this fungus, the underlying mechanisms of plant–pathogen interactions are poorly understood. Here we present a conceptual framework based on coinfection assays, comparative metabolomics, and microbiome profiling to study the interaction ofZ. triticiin susceptible and resistant wheat. We demonstrate thatZ. triticisuppresses the production of immune-related metabolites in a susceptible cultivar. Remarkably, this fungus-induced immune suppression spreads within the leaf and even to other leaves, a phenomenon that we term “systemic induced susceptibility”. Using a comparative metabolomics approach, we identify defense-related biosynthetic pathways that are suppressed and induced in susceptible and resistant cultivars, respectively. We show that these fungus-induced changes correlate with changes in the wheat leaf microbiome. Our findings suggest that immune suppression by this hemibiotrophic pathogen impacts specialized plant metabolism, alters its associated microbial communities, and renders wheat vulnerable to further infections.

Fire blight, caused by Erwinia amylovora, is a devastating disease of apple. Blossom Protect, a product that contains Aureobasidium pullulans as the active ingredient, is one of the most effective biological controls of fire blight. It has been postulated that the mode of action of A. pullulans is to compete against and antagonize epiphytic growth of E. amylovora on flowers, but recent studies have found that flowers treated with Blossom Protect harbored similar to or only slightly reduced E. amylovora populations compared with nontreated flowers. In this study, we tested the hypothesis that A. pullulans-mediated biocontrol of fire blight is the result of induced host resistance. We found that PR genes in the systemic acquired resistance pathway, but not genes in the induced systemic resistance pathway, were induced in hypanthial tissue of apple flowers after the Blossom Protect treatment. Additionally, the induction of PR gene expression was coupled with an increase of plant-derived salicylic acid in this tissue. After inoculation with E. amylovora, PR gene expression was suppressed in nontreated flowers, but in flowers pretreated with Blossom Protect, the heightened PR expression offset the immune repression caused by E. amylovora, and prevented infection. Temporal and spatial analysis of PR gene induction showed that induction of PR genes occurred 2 days after the Blossom Protect treatment, and required direct flower–yeast contact. Finally, we observed deterioration of the epidermal layer of the hypanthium in some of the Blossom Protect-treated flowers, suggesting that PR gene induction in flowers may be a result of pathogenesis by A. pullulans.

Domestication has led to substantial changes in plant physiology. How this anthropogenic intervention has contributed in altering the wheat microbiota is not well understood. Here, we investigated the role of ecological selection, drift, and dispersal in shaping the bacterial and fungal communities associated with domesticated wheat Triticum aestivum and two wild relatives, T. boeoticum and T. urartu. Our study shows that the bacterial and fungal microbiota of wild and domesticated wheat species follow distinct community assembly patterns. Further, we revealed a more prominent role of neutral processes in the assembly of the microbiota of domesticated wheat and propose that domestication has relaxed selective processes in the assembly of the wheat microbiota. [ ] Copyright © 2020 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license .

Plants associate with a wide diversity of microorganisms. Some microorganisms engage in intimate associations with the plant host, collectively forming a metaorganism. Such close coexistence with plants requires specific adaptations that allow microorganisms to overcome plant defenses and inhabit plant tissues during growth and reproduction. New data suggest that the plant immune system has a broader role beyond pathogen recognition and also plays an important role in the community assembly of the associated microorganism. We propose that core microorganisms undergo coadaptation with their plant host, notably in response to the plant immune system allowing them to persist and propagate in their host. Microorganisms, which are vertically transmitted from generation to generation via plant seeds, putatively compose highly adapted species and may have plant-beneficial functions. The extent to which plant domestication has impacted the underlying genetics of plant–microbe associations remains poorly understood. We propose that the ability of domesticated plants to select and maintain advantageous microbial partners may have been affected. In this review, we discuss factors that impact plant metaorganism assembly and function. We underline the importance of microbe–microbe interactions in plant tissues, as they are still poorly studied but may have a great impact on plant health.

Plants recruit diverse microbial communities from the soil to their roots. Intermicrobial interactions and connectivity in the root microbiome play essential roles in plant health by promoting resistance to soilborne pathogens. However, the understanding of these interactions under field conditions is still scarce. Using a strawberry crop model, we characterized the prokaryotic and the fungal communities in the rhizosphere and the roots of three strawberry cultivars grown under field conditions and displaying varying degrees of resistance to the soilborne fungal pathogen Macrophomina phaseolina. We tested the hypothesis that resistant cultivars assemble distinct bacterial and fungal communities that foster microbial connectivity and mediate disease resistance. Our results show that the soilborne pathogen M. phaseolina does not alter the root microbiome of the three strawberry cultivars. Microbiome comparative analysis indicated that the highly susceptible cultivar Sweet Ann assembled a distinct rhizosphere and root microbiome, whereas the microbiome of the strawberry cultivars Marquis and Manresa were more similar and enriched with potential beneficial microbes. Cooccurrence network analysis revealed that the fungal pathogen M. phaseolina was more peripheral in the microbial network of Sweet Ann compared with Manresa and Marquis. Collectively, these results stress the role of the plant microbiome in mediating resistance against soilborne pathogens and further suggest the role of plant genetic traits in the assembly of beneficial microbiome members. Our study reinforces the eminent role of the plant microbiome as trait selection in breeding programs and the need for further understanding of the genetic and biological mechanisms that mediate microbiome assembly. Uncovering these mechanisms will be key for the future success of plant breeding programs in their fight against soilborne pathogens. [ ] Copyright © 2023 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license .