The secret life of plant-beneficial rhizosphere bacteria: insects as alternative hosts

Root-colonizing bacteria have been intensively investigated for their intimate relationship with plants and their manifold plant-beneficial activities. They can inhibit growth and activity of pathogens or induce defence responses. In recent years, evidence has emerged that several plant-beneficial rhizosphere bacteria do not only associate with plants but also with insects. Their relationships with insects range from pathogenic to mutualistic and some rhizobacteria can use insects as vectors for dispersal to new host plants. Thus, the interactions of these bacteria with their environment are even more complex than previously thought and can extend far beyond the rhizosphere. The discovery of this secret life of rhizobacteria represents an exciting new field of research that should link the fields of plant–microbe and insect–microbe interactions. In this review, we provide examples of plant-beneficial rhizosphere bacteria that use insects as alternative hosts, and of potentially rhizosphere-competent insect symbionts. We discuss the bacterial traits that may enable a host-switch between plants and insects and further set the multi-host lifestyle of rhizobacteria into an evolutionary and ecological context. Finally, we identify important open research questions and discuss perspectives on the use of these rhizobacteria in agriculture

Pseudomonas fluorescens WCS374r-Induced Systemic Resistance in Rice against Magnaporthe oryzae Is Based on Pseudobactin-Mediated Priming for a Salicylic Acid-Repressible Multifaceted Defense Response1[C][OA]

Selected strains of nonpathogenic rhizobacteria can reduce disease in foliar tissues through the induction of a defense state known as induced systemic resistance (ISR). Compared with the large body of information on ISR in dicotyledonous plants, little is known about the mechanisms underlying rhizobacteria-induced resistance in cereal crops. Here, we demonstrate the ability of Pseudomonas fluorescens WCS374r to trigger ISR in rice (Oryza sativa) against the leaf blast pathogen Magnaporthe oryzae. Using salicylic acid (SA)-nonaccumulating NahG rice, an ethylene-insensitive OsEIN2 antisense line, and the jasmonate-deficient mutant hebiba, we show that this WCS374r-induced resistance is regulated by an SA-independent but jasmonic acid/ethylene-modulated signal transduction pathway. Bacterial mutant analysis uncovered a pseudobactin-type siderophore as the crucial determinant responsible for ISR elicitation. Root application of WCS374r-derived pseudobactin (Psb374) primed naive leaves for accelerated expression of a pronounced multifaceted defense response, consisting of rapid recruitment of phenolic compounds at sites of pathogen entry, concerted expression of a diverse set of structural defenses, and a timely hyperinduction of hydrogen peroxide formation putatively driving cell wall fortification. Exogenous SA application alleviated this Psb374-modulated defense priming, while Psb374 pretreatment antagonized infection-induced transcription of SA-responsive PR genes, suggesting that the Psb374- and SA-modulated signaling pathways are mutually antagonistic. Interestingly, in sharp contrast to WCS374r-mediated ISR, chemical induction of blast resistance by the SA analog benzothiadiazole was independent of jasmonic acid/ethylene signaling and involved the potentiation of SA-responsive gene expression. Together, these results offer novel insights into the signaling circuitry governing induced resistance against M. oryzae and suggest that rice is endowed with multiple blast-effective resistance pathways

Beneficial microbes going underground of root immunity

Plant roots interact with an enormous diversity of commensal, mutualistic, and pathogenic microbes, which poses a big challenge to roots to distinguish beneficial microbes from harmful ones. Plants can effectively ward off pathogens following immune recognition of conserved microbe-associated molecular patterns (MAMPs). However, such immune elicitors are essentially not different from those of neutral and beneficial microbes that are abundantly present in the root microbiome. Recent studies indicate that the plant immune system plays an active role in influencing rhizosphere microbiome composition. Moreover, it has become increasingly clear that root-invading beneficial microbes, including rhizobia and arbuscular mycorrhiza, evade or suppress host immunity to establish a mutualistic relationship with their host. Evidence is accumulating that many free-living rhizosphere microbiota members can suppress root immune responses, highlighting root immune suppression as an important function of the root microbiome. Thus, the gate keeping functions of the plant immune system are not restricted to warding off root-invading pathogens but also extend to rhizosphere microbiota, likely to promote colonization by beneficial microbes and prevent growth-defense tradeoffs triggered by the MAMP-rich rhizosphere environment

Beneficial microbes going underground of root immunity

Plant roots interact with an enormous diversity of commensal, mutualistic, and pathogenic microbes, which poses a big challenge to roots to distinguish beneficial microbes from harmful ones. Plants can effectively ward off pathogens following immune recognition of conserved microbe-associated molecular patterns (MAMPs). However, such immune elicitors are essentially not different from those of neutral and beneficial microbes that are abundantly present in the root microbiome. Recent studies indicate that the plant immune system plays an active role in influencing rhizosphere microbiome composition. Moreover, it has become increasingly clear that root-invading beneficial microbes, including rhizobia and arbuscular mycorrhiza, evade or suppress host immunity to establish a mutualistic relationship with their host. Evidence is accumulating that many free-living rhizosphere microbiota members can suppress root immune responses, highlighting root immune suppression as an important function of the root microbiome. Thus, the gate keeping functions of the plant immune system are not restricted to warding off root-invading pathogens but also extend to rhizosphere microbiota, likely to promote colonization by beneficial microbes and prevent growth-defense tradeoffs triggered by the MAMP-rich rhizosphere environment

The secret life of plant-beneficial rhizosphere bacteria : insects as alternative hosts

Root-colonizing bacteria have been intensively investigated for their intimate relationship with plants and their manifold plant-beneficial activities. They can inhibit growth and activity of pathogens or induce defence responses. In recent years, evidence has emerged that several plant-beneficial rhizosphere bacteria do not only associate with plants but also with insects. Their relationships with insects range from pathogenic to mutualistic and some rhizobacteria can use insects as vectors for dispersal to new host plants. Thus, the interactions of these bacteria with their environment are even more complex than previously thought and can extend far beyond the rhizosphere. The discovery of this secret life of rhizobacteria represents an exciting new field of research that should link the fields of plant–microbe and insect–microbe interactions. In this review, we provide examples of plant-beneficial rhizosphere bacteria that use insects as alternative hosts, and of potentially rhizosphere-competent insect symbionts. We discuss the bacterial traits that may enable a host-switch between plants and insects and further set the multi-host lifestyle of rhizobacteria into an evolutionary and ecological context. Finally, we identify important open research questions and discuss perspectives on the use of these rhizobacteria in agriculture

Rapid evolution of trait correlation networks during bacterial adaptation to the rhizosphere

There is a growing awareness that traits do not evolve individually but rather are organized as modular networks of covarying traits. Although the importance of multi-trait correlation has been linked to the ability to evolve in response to new environmental conditions, the evolvability of the network itself has to date rarely been assessed experimentally. By following the evolutionary dynamics of a model bacterium adapting to plant roots, we demonstrate that the whole structure of the trait correlation network is highly dynamic. We experimentally evolved Pseudomonas protegens, a common rhizosphere dweller, on the roots of Arabidopsis thaliana. We collected bacteria at regular intervals and determined a range of traits linked to growth, stress resistance, and biotic interactions. We observed a rapid disintegration of the original trait correlation network. Ancestral populations showed a modular network, with the traits linked to resource use and stress resistance forming two largely independent modules. This network rapidly was restructured during adaptation, with a loss of the stress resistance module and the appearance of new modules out of previously disconnected traits. These results show that evolutionary dynamics can involve a deep restructuring of phenotypic trait organization, pointing to the emergence of novel life history strategies not represented in the ancestral phenotype

Type III secretion system of beneficial rhizobacteria Pseudomonas simiae WCS417 and Pseudomonas defensor WCS374

Plants roots host myriads of microbes, some of which enhance the defense potential of plants by activating a broad-spectrum immune response in leaves, known as induced systemic resistance (ISR). Nevertheless, establishment of this mutualistic interaction requires active suppression of local root immune responses to allow successful colonization. To facilitate host colonization, phytopathogenic bacteria secrete immune-suppressive effectors into host cells via the type III secretion system (T3SS). Previously, we searched the genomes of the ISR-inducing rhizobacteria Pseudomonas simiae WCS417 and Pseudomonas defensor WCS374 for the presence of a T3SS and identified the components for a T3SS in the genomes of WCS417 and WCS374. By performing a phylogenetic and gene cluster alignment analysis we show that the T3SS of WCS417 and WCS374 are grouped in a clade that is enriched for beneficial rhizobacteria. We also found sequences of putative novel effectors in their genomes, which may facilitate future research on the role of T3SS effectors in plant-beneficial microbe interactions in the rhizosphere

Type III secretion system of beneficial rhizobacteria Pseudomonas simiae WCS417 and Pseudomonas defensor WCS374

Plants roots host myriads of microbes, some of which enhance the defense potential of plants by activating a broad-spectrum immune response in leaves, known as induced systemic resistance (ISR). Nevertheless, establishment of this mutualistic interaction requires active suppression of local root immune responses to allow successful colonization. To facilitate host colonization, phytopathogenic bacteria secrete immune-suppressive effectors into host cells via the type III secretion system (T3SS). Previously, we searched the genomes of the ISR-inducing rhizobacteria Pseudomonas simiae WCS417 and Pseudomonas defensor WCS374 for the presence of a T3SS and identified the components for a T3SS in the genomes of WCS417 and WCS374. By performing a phylogenetic and gene cluster alignment analysis we show that the T3SS of WCS417 and WCS374 are grouped in a clade that is enriched for beneficial rhizobacteria. We also found sequences of putative novel effectors in their genomes, which may facilitate future research on the role of T3SS effectors in plant-beneficial microbe interactions in the rhizosphere

Induced Systemic Resistance and the Rhizosphere Microbiome

Microbial communities that are associated with plant roots are highly diverse and harbor tens of thousands of species. This so-called microbiome controls plant health through several mechanisms including the suppression of infectious diseases, which is especially prominent in disease suppressive soils. The mechanisms implicated in disease suppression include competition for nutrients, antibiosis, and induced systemic resistance (ISR). For many biological control agents ISR has been recognized as the mechanism that at least partly explains disease suppression. Implications of ISR on recruitment and functioning of the rhizosphere microbiome are discussed