Many recent studies have highlighted the importance of plant growth-promoting (rhizo)bacteria (PGPR) in supporting plant’s development, particularly under biotic and abiotic stress. Most focus on the plant growth-promoting traits of selected strains and the latter’s effect on plant biomass, root architecture, leaf area, and specific metabolite accumulation. Regarding energy balance, plant growth is the outcome of an input (photosynthesis) and several outputs (i.e., respiration, exudation, shedding, and herbivory), frequently neglected in classical studies on PGPR-plant interaction. Here, we discuss the primary evidence underlying the modifications triggered by PGPR and their metabolites on the plant ecophysiology. We propose to detect PGPR-induced variations in the photosynthetic activity using leaf gas exchange and recommend setting up the correct timing for monitoring plant responses according to the specific objectives of the experiment. This research identifies the challenges and tries to provide future directions to scientists working on PGPR-plant interactions to exploit the potential of microorganisms’ application in improving plant value.

Soilless cultivation allows for the exploitation of the benefits of plant growth-promoting rhizobacteria (PGPR) without the loss of efficacy observed with soil inoculation. In this study, we investigated the effects of a PGPR consortium on the plant growth, ecophysiology, and metabolic profile of lettuce (Lactuca sativa L.) grown in an aeroponic system under a low-nutrient regime. Overall, the plant biomass increased by 25% in the PGPR-inoculated plants due to enhanced leaf and root growth. The rise in the leaf biomass was primarily due to an increase in the leaf number and average leaf mass, coupled with a higher total leaf area. In addition, the inoculated plants exhibited an altered leaf anatomy characterized by an increased palisade parenchyma thickness and reduced airspace area, suggesting an improved photosynthetic efficiency and changes in the mesophyll conductance. The root morphology was also altered, with the PGPR-inoculated plants showing higher lateral root development. Furthermore, PGPR inoculation induced significant metabolic reprogramming in the leaves, affecting several pathways related to growth, development, and stress responses. These findings provide valuable insights into the intricate metabolic dialog between plants and beneficial microbes and demonstrate that the integration of soilless culture with an analysis of the ecophysiological, anatomical, and metabolomic plant responses can be a powerful approach to accelerate the design of new PGPR consortia for use as microbial biostimulants.

Introduction: Soil microbiome transplantation is a promising technique for enhancing plant holobiont response to abiotic and biotic stresses. However, the rapid assessment of microbiome-plant functional integration in short-term experiments remains a challenge.Methods: This study investigates the potential of three evergreen sclerophyll species, Pistacia lentiscus (PL), Rosmarinus officinalis (RO), and Juniperus phoenicea (JP), to serve as a reservoir for microbial communities able to confer enhanced tolerance to drought in Salvia officinalis cultivated under water shortage, by analyzing biomass production, plant phenotype, plant ecophysiological responses, and leaf metabolome.Results: Our results showed that the inoculation with the three rhizomicrobiomes did not enhance total plant biomass, while it significantly influenced plant architecture, ecophysiology, and metabolic responses. The inoculation with the JP rhizomicrobiome led to a significant increase in root biomass, resulting in smaller leaves and a higher leaf number. These morphological changes suggest improved water acquisition and thermoregulation strategies. Furthermore, distinct stomatal conductance patterns were observed in plants inoculated with microbiomes from PJ and PL, indicating altered responses to drought stress. The metabolome analysis demonstrated that rhizomicrobiome transplantation significantly influenced the leaf metabolome of S. officinalis. All three rhizomicrobiomes promoted the accumulation of phenolic compounds, terpenoids, and alkaloids, known to play crucial roles in plant defense and stress response. Five molecules (genkwanin, beta-ionone, sumatrol, beta-peltatin-A-methyl ester, and cinnamoyl-beta-D-glucoside) were commonly accumulated in leaves of inoculated sage, independently of the microbiome. Furthermore, unique metabolic alterations were observed depending on the specific inoculated rhizomicrobiome, highlighting the specialized nature of plant-microbe interactions and the possible use of these specific molecules as biomarkers to monitor the recruitment of beneficial microorganisms.Discussion: This study provides compelling evidence that microbiome transplantation can induce phenotypic and metabolic changes in recipient plants, potentially enhancing their resilience to water scarcity. Our findings emphasize the importance of considering multiple factors, including biomass, physiology, and metabolomics, when evaluating the effectiveness of microbiome engineering for improving plant stress tolerance.

Water scarcity can negatively affect crop yield, posing a significant threat to global food security, such as drought. Plant growth-promoting rhizobacteria (PGPR), either as single strains or synthetic communities (SynComs), has shown promise in alleviating drought stress in various plant species. In this study, we examined the effects of water limitation on Salvia officinalis and the potential of a SynCom composed of five phosphate-solubilizing, auxin-producing, and/or nitrogen-fixing Gram-negative bacteria to enhance plant growth and drought tolerance. Plant growth, morphology, physiology, and leaf metabolomic profiles were assessed using a combination of physiological measurements and LC-MS untargeted metabolomics. Mild water stress induced a conservative water-use strategy in S. officinalis, characterized by increased root-to-shoot ratio and altered leaf morphology, without compromising photosynthetic performance. SynCom inoculation under well-watered conditions elicited drought-like responses, including transient reductions in stomatal conductance. Leaf metabolomic analysis revealed that inoculation influenced the abundance of several metabolites, including biogenic amines and dipeptides, under both irrigation regimes. Notably, drought stress and SynCom inoculation increased histamine and α-ketoglutaric acid levels, highlighting potential impacts on food quality. Under reduced irrigation, inoculation further modulated leaf morphology and biomass allocation, promoting thicker leaves and increased root biomass allocation. These results demonstrate the ability of the SynCom to modulate plant physiology and metabolism in response to both optimal and reduced irrigation, potentially enhancing drought resilience without directly improving growth. The study also highlights the complex interactions among microbial inoculation, plant stress responses, and leaf metabolite profiles, emphasizing the importance of considering the effects on the production of bioactive compounds when developing microbial inoculants for edible plants.