Tomato domestication rather than subsequent breeding events reduces microbial associations related to phosphorus recovery.

Legacy phosphorus (P) is a reservoir of sparingly available P, and its recovery could enhance sustainable use of nonrenewable mineral fertilizers. Domestication has affected P acquisition, but it is unknown if subsequent breeding efforts, like the Green Revolution (GR), had a similar effect. We examined how domestication and breeding events altered P acquisition by growing wild, traditional (pre-GR), and modern (post-GR) tomato in soil with legacy P but low bioavailable P. Wild tomatoes, particularly accession LA0716 (Solanum pennellii), heavily cultured rhizosphere P solubilizers, suggesting reliance on microbial associations to acquire P. Wild tomato also had a greater abundance of other putatively beneficial bacteria, including those that produce chelating agents and antibiotic compounds. Although wild tomatoes had a high abundance of these P solubilizers, they had lower relative biomass and greater P stress factor than traditional or modern tomato. Compared to wild tomato, domesticated tomato was more tolerant to P deficiency, and both cultivated groups had a similar rhizosphere bacterial community composition. Ultimately, this study suggests that while domestication changed tomato P recovery by reducing microbial associations, subsequent breeding processes have not further impacted microbial P acquisition mechanisms. Selecting microbial P-related traits that diminished with domestication may therefore increase legacy P solubilization.

Harnessing Phosphorous (P) Fertilizer-Insensitive Bacteria to Enhance Rhizosphere P Bioavailability in Legumes.

Phosphorous (P) is widely used in agriculture; yet, P fertilizers are a nonrenewable resource. Thus, mechanisms to improve soil P bioavailability need to be found. Legumes are efficient in P acquisition and, therefore, could be used to develop new technologies to improve soil P bioavailability. Here, we studied different species and varieties of legumes and their rhizosphere microbiome responses to low-P stress. Some varieties of common beans, cowpeas, and peas displayed a similar biomass with and without P fertilization. The rhizosphere microbiome of those varieties grown without P was composed of unique microbes displaying different levels of P solubilization and mineralization. When those varieties were amended with P, some of the microbes involved in P solubilization and mineralization decreased in abundance, but other microbes were insensitive to P fertilization. The microbes that decreased in abundance upon P fertilization belonged to groups that are commonly used as biofertilizers such as Pseudomonas and Azospirillum. The microbes that were not affected by P fertilization constitute unique species involved in P mineralization such as Arenimonas daejeonensis, Hyphomicrobium hollandicum, Paenibacillus oenotherae, and Microlunatus speluncae. These P-insensitive microbes could be used to optimize P utilization and drive future sustainable agricultural practices to reduce human dependency on a nonrenewable resource.

Shifts of the soil microbiome composition induced by plant-plant interactions under increasing cover crop densities and diversities.

Interspecific and intraspecific competition and facilitation have been a focus of study in plant-plant interactions, but their influence on plant recruitment of soil microbes is unknown. In this greenhouse microcosm experiment, three cover crops (alfalfa, brassica, and fescue) were grown alone, in paired mixtures, and all together under different densities. For all monoculture trials, total pot biomass increased as density increased. Monoculture plantings of brassica were associated with the bacteria Azospirillum spp., fescue with Ensifer adhaerens, and alfalfa with both bacterial taxa. In the polycultures of cover crops, for all plant mixtures, total above-ground alfalfa biomass increased with density, and total above ground brassica biomass remained unchanged. For each plant mixture, differential abundances highlighted bacterial taxa which had not been previously identified in monocultures. For instance, mixtures of all three plants showed an increase in abundance of Planctomyces sp. SH-PL14 and Sandaracinus amylolyticus which were not represented in the monocultures. Facilitation was best supported for the alfalfa-fescue interaction as the total above ground biomass was the highest of any mixture. Additionally, the bulk soil microbiome that correlated with increasing plant densities showed increases in plant growth-promoting rhizobacteria such as Achromobacter xylosoxidans, Stentotrophomonas spp., and Azospirillum sp. In contrast, Agrobacterium tumefaciens, a previously known generalist phytopathogen, also increased with alfalfa-fescue plant densities. This could suggest a strategy by which, after facilitation, a plant neighbor could culture a pathogen that could be more detrimental to the other.

A Microbiological Approach to Alleviate Soil Replant Syndrome in Peaches.

Replant syndrome (RS) is a global problem characterized by reduced growth, production life, and yields of tree fruit/nut orchards. RS etiology is unclear, but repeated monoculture plantings are thought to develop a pathogenic soil microbiome. This study aimed to evaluate a biological approach that could reduce RS in peach (Prunus persica) orchards by developing a healthy soil bacteriome. Soil disinfection via autoclave followed by cover cropping and cover crop incorporation was found to distinctly alter the peach soil bacteriome but did not affect the RS etiology of RS-susceptible 'Lovell' peach seedlings. In contrast, non-autoclaved soil followed by cover cropping and incorporation altered the soil bacteriome to a lesser degree than autoclaving but induced significant peach growth. Non-autoclaved and autoclaved soil bacteriomes were compared to highlight bacterial taxa promoted by soil disinfection prior to growing peaches. Differential abundance shows a loss of potentially beneficial bacteria due to soil disinfection. The treatment with the highest peach biomass was non-autoclaved soil with a cover crop history of alfalfa, corn, and tomato. Beneficial bacterial species that were cultivated exclusively in the peach rhizosphere of non-autoclaved soils with a cover crop history were Paenibacillus castaneae and Bellilinea caldifistulae. In summary, the non-autoclaved soils show continuous enhancement of beneficial bacteria at each cropping phase, culminating in an enriched rhizosphere which may help alleviate RS in peaches.

Root exudate-derived compounds stimulate the phosphorus solubilizing ability of bacteria.

Low phosphorus (P) availability in soils is a major challenge for sustainable food production, as most soil P is often unavailable for plant uptake and effective strategies to access this P are limited. Certain soil occurring bacteria and root exudate-derived compounds that release P are in combination promising tools to develop applications that increase phosphorus use efficiency in crops. Here, we studied the ability of root exudate compounds (galactinol, threonine, and 4-hydroxybutyric acid) induced under low P conditions to stimulate the ability of bacteria to solubilize P. Galactinol, threonine, and 4-hydroxybutyric acid were incubated with the P solubilizing bacterial strains Enterobacter cloacae, Pseudomonas pseudoalcaligenes, and Bacillus thuringiensis under either inorganic (calcium phosphate) or organic (phytin) forms of plant-unavailable P. Overall, we found that the addition of individual root exudate compounds did not support bacterial growth rates. However, root exudates supplemented to the different bacterial appeared to enhance P solubilizing activity and overall P availability. Threonine and 4-hydroxybutyric acid induced P solubilization in all three bacterial strains. Subsequent exogenous application of threonine to soils improved the root growth of corn, enhanced nitrogen and P concentrations in roots and increased available levels of potassium, calcium and magnesium in soils. Thus, it appears that threonine might promote the bacterial solubilization and plant-uptake of a variety of nutrients. Altogether, these findings expand on the function of exuded specialized compounds and propose alternative approaches to unlock existing phosphorus reservoirs of P in crop lands.

Soil microbiome disruption reveals specific and general plant-bacterial relationships in three agroecosystem soils.

Soil microbiome disruption methods are regularly used to reduce populations of microbial pathogens, often resulting in increased crop growth. However, little is known about the effect of soil microbiome disruption on non-pathogenic members of the soil microbiome. Here, we applied soil microbiome disruption in the form of moist-heat sterilization (autoclaving) to reduce populations of naturally occurring soil microbiota. The disruption was applied to analyze bacterial community rearrangement mediated by four crops (corn, beet, lettuce, and tomato) grown in three historically distinct agroecosystem soils (conventional, organic, and diseased). Applying the soil disruption enhanced plant influence on rhizosphere bacterial colonization, and significantly different bacterial communities were detected between the tested crops. Furthermore, bacterial genera showed significant abundance increases in ways both unique-to and shared-by each tested crop. As an example, corn uniquely promoted abundances of Pseudomonas and Sporocytophaga, regardless of the disrupted soil in which it was grown. Whereas the promotion of Bosea, Dyadobacter and Luteoliobacter was shared by all four crops when grown in disrupted soils. In summary, soil disruption followed by crop introduction amplified the plant colonization of potential beneficial bacterial genera in the rhizosphere.

The rhizosphere microbiome: Plant-microbial interactions for resource acquisition.

While horticulture tools and methods have been extensively developed to improve the management of crops, systems to harness the rhizosphere microbiome to benefit plant crops are still in development. Plants and microbes have been coevolving for several millennia, conferring fitness advantages that expand the plant's own genetic potential. These beneficial associations allow the plants to cope with abiotic stresses such as nutrient deficiency across a wide range of soils and growing conditions. Plants achieve these benefits by selectively recruiting microbes using root exudates, positively impacting their nutrition, health and overall productivity. Advanced knowledge of the interplay between root exudates and microbiome alteration in response to plant nutrient status, and the underlying mechanisms there of, will allow the development of technologies to increase crop yield. This review summarizes current knowledge and perspectives on plant-microbial interactions for resource acquisition and discusses promising advances for manipulating rhizosphere microbiomes and root exudation.

Conditioned soils reveal plant-selected microbial communities that impact plant drought response.

Rhizobacterial communities can contribute to plant trait expression and performance, including plant tolerance against abiotic stresses such as drought. The conditioning of microbial communities related to disease resistance over generations has been shown to develop suppressive soils which aid in plant defense responses. Here, we applied this concept for the development of drought resistant soils. We hypothesized that soils conditioned under severe drought stress and tomato cultivation over two generations, will allow for plant selection of rhizobacterial communities that provide plants with improved drought resistant traits. Surprisingly, the plants treated with a drought-conditioned microbial inoculant showed significantly decreased plant biomass in two generations of growth. Microbial community composition was significantly different between the inoculated and control soils within each generation (i.e., microbial history effect) and for the inoculated soils between generations (i.e., conditioning effect). These findings indicate a substantial effect of conditioning soils on the abiotic stress response and microbial recruitment of tomato plants undergoing drought stress.

Methods for Root Exudate Collection and Analysis.

Plant root exudation has long been recognized as a vital communication system between plants and microbial communities populating the rhizosphere. Due to the high complexity of the collection process and analysis, a variety of techniques have been developed to mimic natural exudation conditions. In addition, significant progress improving existing techniques and developing new methodologies of root exudate collection and analysis have been made. However, optimal standard methods that compare closely with environmental soil conditions are not yet available. In this review, we provide an overview of all those topics and provide suggestions for improvement.

Root exudates drive soil-microbe-nutrient feedbacks in response to plant growth.

Although interactions between plants and microbes at the plant-soil interface are known to be important for plant nutrient acquisition, relatively little is known about how root exudates contribute to nutrient exchange over the course of plant development. In this study, root exudates from slow- and fast-growing stages of Arabidopsis thaliana plants were collected, chemically analysed and then applied to a sandy nutrient-depleted soil. We then tracked the impacts of these exudates on soil bacterial communities, soil nutrients (ammonium, nitrate, available phosphorus and potassium) and plant growth. Both pools of exudates shifted bacterial community structure. GeoChip analyses revealed increases in the functional gene potential of both exudate-treated soils, with similar responses observed for slow-growing and fast-growing plant exudate treatments. The fast-growing stage root exudates induced higher nutrient mineralization and enhanced plant growth as compared to treatments with slow-growing stage exudates and the control. These results suggest that plants may adjust their exudation patterns over the course of their different growth phases to help tailor microbial recruitment to meet increased nutrient demands during periods demanding faster growth.

Role of root exudates on assimilation of phosphorus in young and old Arabidopsis thaliana plants.

The role of root exudates has long been recognized for its potential to improve nutrient use efficiency in cropping systems. However, studies addressing the variability of root exudates involved in phosphorus solubilization across plant developmental stages remain scarce. Here, we grew Arabidopsis thaliana seedlings in sterile liquid culture with a low, medium, or high concentration of phosphate and measured the composition of the root exudate at seedling, vegetative, and bolting stages. The exudates changed in response to the incremental addition of phosphorus, starting from the vegetative stage. Specific metabolites decreased in relation to phosphate concentration supplementation at specific stages of development. Some of those metabolites were tested for their phosphate solubilizing activity, and 3-hydroxypropionic acid, malic acid, and nicotinic acid were able to solubilize calcium phosphate from both solid and liquid media. In summary, our data suggest that plants can release distinct compounds to deal with phosphorus deficiency needs influenced by the phosphorus nutritional status at varying developmental stages.

Differential Effects of Phosphorus Fertilization on Plant Uptake and Rhizosphere Microbiome of Cultivated and Non-cultivated Potatoes.

There is evidence that shows that phosphorus (P) fertilization has a moderate effect on the rhizosphere microbial composition of cultivated crops. But how this effect is manifested on wild species of the same crop is not clear. This study compares the impact of phosphorus fertilization with rhizosphere bacterial community composition and its predicted functions, related to P-cycling genes, in both cultivated and non-cultivated potato (Solanum sp.) plants. It was found that the biomass of non-cultivated potatoes was more responsive to P fertilization as compared with cultivated plants. Differences in general bacterial community composition patterns under increasing P amendments were subtle for both potato groups. However, potato genotype significantly influenced community composition with several bacterial families being more abundant in the cultivated plants. In addition, the predicted phosphatases had lower abundances in modern cultivars compared with non-cultivated potatoes. In summary, despite higher accumulation of differentially abundant bacteria in the rhizosphere of cultivated plants, the responsiveness of these plants to increase P levels was lower than in non-cultivated plants.

Isolation of Klebsiella pneumoniae and Pseudomonas aeruginosa from entomopathogenic nematode-insect host relationship to examine bacterial pathogenicity on Trichoplusia ni.

Klebsiella pneumoniae was isolated from infected pupae of Galleria mellonella and Pseudomonas aeruginosa was isolated from the entomopathogenic nematode Heterorhabditis bacteriophora hosted within the pupae of G. mellonella. Insect consumption and surface application of P. aeruginosa resulted in 83.33% and 81.66% mortality of Trichoplusia ni larvae, respectively. In contrast, 50% mortality was shown when T. ni larvae were fed with K. pneumoniae, and no larvae were killed when applying the bacterium to the larval cuticle. This report shows that two opportunistic human pathogens found in the insect-nematode ecosystem could kill insect pests.

A novel approach to determine generalist nematophagous microbes reveals Mortierella globalpina as a new biocontrol agent against Meloidogyne spp. nematodes.

Root-knot nematodes (RKN) such as Meloidogyne spp. are among the most detrimental pests in agriculture affecting several crops. New methodologies to manage RKN are needed such as efficient discovery of nematophagous microbes. In this study, we developed an in vitro high-throughput method relying on the free-living nematode Caenorhabditis elegans and the infection of those nematodes with a soil slurry containing a microbiome likely to house nematophagous microbes. Nematodes were monitored for presence of infection and sub-cultured repeatedly for the purpose of isolating pure cultures of the microbe responsible for conferring the nematicidal activity. Once soil microbes were confirmed to be antagonistic to C. elegans, they were tested for pathogenicity against Meloidogyne chitwoodi. Using this methodology, the fungal isolate Mortierella globalpina was confirmed to be pathogenic in vitro against M. chitwoodi by nematode trapping via hyphal adhesion to the cuticle layer, penetration of the cuticle layer, and subsequently digestion of its cellular contents. M. globalpina was also observed to reduce disease symptomology of RKNs in vivo via significant reduction of root-galls on tomato (Solanum lycopersicum var. Rutgers).

Trichoderma gamsii affected herbivore feeding behaviour on Arabidopsis thaliana by modifying the leaf metabolome and phytohormones.

Plants can re-programme their transcriptome, proteome and metabolome to deal with environmental and biotic stress. It has been shown that the rhizosphere microbiome has influence on the plant metabolome and on herbivore behaviour. In the present study, Trichoderma gamsii was isolated from Arabidopsis thaliana rhizosphere soil. The inoculation of roots of Arabidopsis thaliana with T. gamsii significantly inhibited the feeding behaviour of Trichoplusia ni and affected the metabolome as well as the content of phytohormones in Arabidopsis leaves. T. gamsii-treated plant leaves had higher levels of amino acids and lower concentrations of sugars. In addition, T. gamsii-treated plant leaves had more abscisic acid (ABA) and lower levels of salicylic acid (SA) and indole-3-acetic acid (IAA) in comparison with the untreated plants. Furthermore, the inoculation with T. gamsii on different signalling mutants showed that the induction of defences were SA-dependent. These findings indicate that T. gamsii has potential as a new type of biocontrol agent to promote plant repellence to insect attacks.

Root exudates drive the soil-borne legacy of aboveground pathogen infection.

BACKGROUND: Plants are capable of building up beneficial rhizosphere communities as is evidenced by disease-suppressive soils. However, it is not known how and why soil bacterial communities are impacted by plant exposure to foliar pathogens and if such responses might improve plant performance in the presence of the pathogen. Here, we conditioned soil by growing multiple generations (five) of Arabidopsis thaliana inoculated aboveground with Pseudomonas syringae pv tomato (Pst) in the same soil. We then examined rhizosphere communities and plant performance in a subsequent generation (sixth) grown in pathogen-conditioned versus control-conditioned soil. Moreover, we assessed the role of altered root exudation profiles in shaping the root microbiome of infected plants. RESULTS: Plants grown in conditioned soil showed increased levels of jasmonic acid and improved disease resistance. Illumina Miseq 16S rRNA gene tag sequencing revealed that both rhizosphere and bulk soil bacterial communities were altered by Pst infection. Infected plants exhibited significantly higher exudation of amino acids, nucleotides, and long-chain organic acids (LCOAs) (C > 6) and lower exudation levels for sugars, alcohols, and short-chain organic acids (SCOAs) (C ≤ 6). Interestingly, addition of exogenous amino acids and LCOA also elicited a disease-suppressive response. CONCLUSION: Collectively, our data suggest that plants can recruit beneficial rhizosphere communities via modification of plant exudation patterns in response to exposure to aboveground pathogens to the benefit of subsequent plant generations.

Plant-insect-pathogen interactions: a naturally complex ménage à trois.

Under environmental conditions, plants are constantly exposed to a wide range of biotic interactions, which include insects, and pathogens. Usually scientists are tempted to study each association individually, which reduces the complexity of the interaction. This restricted view of the problem does not consider that plants are the ballroom in which a multitude of organisms are constantly interacting with each other affecting not only plant responses but also how one organism responds to the other. Plants attacked by insects and pathogens display profound physiological, morphological and chemical changes or adaptations that result in organism attraction or avoidance, depending on the species involved. Therefore, many researchers worldwide have decided to study this phenomenon in a more holistic view, integrating genetics, ecology and physiology to depict these complex interactions. In this review, we will discuss how plant infection by pathogens may affect insect behavior and vice-versa and how plants cope with these multitude of biotic stresses.

Bacterial Microbiome and Nematode Occurrence in Different Potato Agricultural Soils.

Pratylenchus neglectus and Meloidogyne chitwoodi are the main plant-parasitic nematodes in potato crops of the San Luis Valley, Colorado. Bacterial microbiome (16S rRNA copies per gram of soil) and nematode communities (nematodes per 200 g of soil) from five different potato farms were analyzed to determine negative and positive correlations between any bacterial genus and P. neglectus and M. chitwoodi. Farms showed differences in bacterial communities, percentage of bacterivorous and fungivorous nematodes, and numbers of P. neglectus and M. chitwoodi. The farm with the lowest population of P. neglectus and M. chitwoodi had higher abundances of the bacterial genera Bacillus spp., Arthrobacter spp., and Lysobacter spp., and the soil nematode community was composed of more than 30% of fungivorous nematodes. In contrast, the farm with higher numbers of P. neglectus and M. chitwoodi had a lower abundance of the abovementioned bacterial genera, higher abundance of Burkholderia spp., and less than 25% of fungivorous nematodes. The α-Proteobacteria Rhodoplanes, Phenylobacterium, and Kaistobacter positively correlated with M. chitwoodi, and the Bacteroidia and γ-Proteobacteria positively correlated with P. neglectus. Our results, based largely on co-occurrence analyses, suggest that the abundance of Bacillus spp., Arthrobacter spp., and Lysobacter spp. in Colorado potato soils is negatively correlated with P. neglectus and M. chitwoodi abundance. Further studies will isolate and identify bacterial strains of these genera, and evaluate their nematode-antagonistic activity.

The unseen rhizosphere root-soil-microbe interactions for crop production.

The underground root-soil-microbe interactions are extremely complex, but vitally important for aboveground plant growth, health and fitness. The pressure to reduce our reliance on agrochemicals, and sustainable efforts to develop agriculture makes rhizosphere interactions' research a hotspot. Recent advances provide new insights about the signals, pathways, functions and mechanisms of these interactions. In this review, we provide an overview about recent progress in rhizosphere interaction networks in crops. We also discuss a holistic view of the root-soil-rhizomicrobiome interactions achieved through the advances of omics and bioinformatics technologies, and the potential strategies to manage the complex rhizosphere interactions for enhancing crop production.