Plants recruit their microbiome from various environmental reservoirs, including the rhizosphere, phyllosphere, spermosphere, anthosphere, and carposphere (Hardoim et al., 2015). The root microbiome is mainly horizontally transferred; that is, it comes from the soil environment, containing different microorganisms (Shade et al., 2017). Nevertheless, bacteria can also transmit vertically through seeds (Fierer, 2017). Microorganisms thrive in developing plant roots, and seeds are an important source of them (Truyens et al., 2015; Nelson, 2018). Plant root system presents a unique environmental niche for the soil microbial community, which settles in the root, rhizosphere and aerial part (Berendsen et al., 2012). One of the most significant mutualistic relationships in the root microbiome is the nodule formation between leguminous plants and nitrogen-fixing bacteria such as Rhizobium (Liu et al., 2021; Granada Agudelo et al., 2023). These nodules enhance nitrogen availability, which is fundamental to plant functionality and growth (Lindström and Mousavi, 2020), ultimately improving soil fertility and supporting sustainable agriculture (Ojija and Aloo, 2023). Nodule formation represents a classic example of a mutualistic interaction where both the plant and the microbes benefit (Haldar and Sengupta, 2015).

The rhizosphere, a thin layer of soil directly influenced by plant roots, is regarded as a hot zone of microbial activity and one of the most complicated ecosystems (Raaijmakers et al., 2009). Donn et al. (2015) demonstrated that bacterial composition of wheat rhizosphere changed across years and noticed the abundance of Pseudomonads and Actinobacteria was 10-fold greater in rhizosphere than that of bulk soil. Root exudates (e.g., amino acids, fatty acids, organic acids, phenolics, nucleotides, plant growth regulators, sugars, putrescine, vitamins, and sterols) are leading factors in terms of shifting microbial composition around roots, the so-called rhizosphere effect (Mendes et al., 2013; Rasmann and Turlings, 2016; Sasse et al., 2018; Zhalnina et al., 2018; Jiang et al., 2019). For example, benzoxazinoids (BXs), a class of defensive secondary metabolites attributed to maize roots, had a critical role in changing root-associated microbiota composition. Actinobacteria and Proteobacteria are shown to be affected by BXs compounds (Hu et al., 2018). Overall, phenotype and genotype variations in plant traits are the definitive explanation for this hypothesis, which can guide specific microbial communities.

A vast range of bacterial endophytes can successfully invade plant roots. Bacterial endophytes frequently enter root tissues via passive processes such as root fractures or lateral root emergence points, as well as active mechanisms (Kandel et al., 2017) (Figure 1). Endophytes’ colonization and transmission within plants are impacted by various factors, such as plant resource allocation and the endophytes’ colonization ability. Various bacterial taxa have been found to be able to colonize inside root tissues, such as Acidobacteria, Proteobacteria, Verrucomicrobia, Bacteroidetes, Chloroflexi, Planctomycetes, Gemmatimonadetes and Firmicutes which commonly occur in grapevine roots (Burns et al., 2015; Samad et al., 2017a; Correa-Galeote et al., 2018). Additionally, the study by Correa-Galeote et al. (2018) found that Proteobacteria, Firmicutes and Bacteroidetes are the predominant phyla within the maize roots and the history of soil cultivation substantially influenced the abundance of these phyla.

Above-ground plant tissues (e.g., vegetative foliar portions, floral parts, and leaves) provide distinct habitats for epiphytes and endophytes; yet, the ecology of endosphere and episphere bacteria differs significantly. Most endophytes propagate systemically via the xylem to various plant compartments, but they can also reach plant tissues through aerial plant parts (Compant et al., 2010, 2011). Different above-ground plant compartments host distinct endophytic communities, influenced by the allocation of plant resources. According to observations, phyllobacteria also originated in the soil environment, affected by environmental and plant factors (Vorholt, 2012; Wallace et al., 2018).

Various microorganisms are found at the species and genus levels in the endosphere and phyllosphere. For example, the structural analysis of grapevine carposphere or phyllosphere microbiome revealed that the predominant genera were Sphingomonas, Frigoribacterium, Pseudomonas, Bacillus, Curtobacterium, Acinetobacter, Enterobacter, Citrobacter, Erwinia, Methylobacterium and Pantoea (Campisano et al., 2014; Kecskeméti et al., 2016; Wallace et al., 2018). Recently, Wallace et al. (2018) investigated the leaf microbiome of 300 various maize lines. They found that Methylobacteria and Sphingomonads were the predominant taxa. They also found that environmental variables mainly drove the microbial composition of the phyllosphere. The dominant taxa are found to be Pseudomonas and Enterobacteriaceae in apple flowers (Steven et al., 2018). Similarly, a number of studies have found Pseudomonas to be the most abundant genus in apples, almonds, grapefruit, tobacco and pumpkin flowers (Aleklett et al., 2014). In general, microbiota on and within the plant tissue originate mainly from seed, soil, and air, whose composition of communities was determined by several factors (e.g., environmental, farm management techniques, and soil). The unique assembly in host and compartments indicates that the plant has a strong functional interaction with its above-ground microbiota, but further research is needed to better understand the mechanisms governing this relationship. Above-ground microbiomes and endophytes are well known for their role in improving plant growth, stress mitigation, and disease resistance (Hassani et al., 2018; Stone et al., 2018).

Microorganisms that are consistently associated with specific plant species or genotypes, irrespective of environmental fluctuations, form the core plant microbiome (Toju et al., 2018). These core taxa are considered functionally critical due to their stable presence. Evolutionary selection has equipped them with essential genes that contribute to plant fitness. Notable examples include Bradyrhizobium, Sphingobium and Microvirga in potatoes (Pfeiffer et al., 2017), as well as Pseudomonadaceae, Micrococcaceae and Hyphomicrobiaceae in grapevines (Zarraonaindia et al., 2015). Keystone taxa within the core microbiome are pivotal in maintaining ecosystem stability and promoting plant health, primarily through nutrient cycling, pathogen suppression, and growth enhancement mechanisms (Lemanceau et al., 2017). Satellite taxa play critical roles in functions such as disease suppression and nutrient cycling, contributing disproportionately to the system’s overall stability (Hanski, 1982; Gera Hol et al., 2015). In contrast, satellite taxa are less abundant, displaying a transient presence across fewer environments. Although these taxa may not be as ubiquitous, their ecological contributions are significant, particularly in enhancing ecosystem resilience and stability (Jousset et al., 2017). Examples of satellite species include Lipomyces sp. (Kunito et al., 2012) and Cladorrhinum sp. (Tayyab et al., 2021), which contribute to aluminum toxicity reduction, plant growth promotion, and biological control.

Despite their transient and often rare nature, rare microorganisms are integral to the flexibility of the microbial community, enabling rapid responses to environmental perturbations. The concept of the “rare biosphere” is especially relevant here, as rare microbial taxa contribute to microbial diversity and the capacity of ecosystems to withstand biotic and abiotic stresses (Lynch and Neufeld, 2015).

The interplay between core and satellite microbiomes is essential in understanding the functional dynamics of plant health. Core taxa offer stability, providing critical support under standard environmental conditions. In contrast, satellite taxa introduce ecological flexibility, enabling the plant microbiome to adapt to environmental shifts. This synergistic interaction is fundamental to plant resilience, particularly in agriculture, where crops are exposed to diverse stresses. Case studies involving microbial inoculants have shown that targeting core taxa for long-term benefits, along with managing satellite taxa for short-term adaptations, can significantly enhance agricultural productivity and disease resistance (Compant et al., 2019). Understanding and leveraging the interactions between core and satellite microbiomes are vital for improving plant fitness and ecosystem health, especially in the face of environmental change and agricultural intensification (Figure 2).

Biological nitrogen fixation (BNF) is a key process wherein plant-associated bacteria convert atmospheric nitrogen into a usable form of ammonia for plants. This symbiotic relationship primarily occurs in leguminous plants through specialized root nodules that harbor nitrogen-fixing bacteria, such as Rhizobium and Bradyrhizobium (Irisarri et al., 2021; Prüß, 2022). Nitrogen fixation reduces the need for synthetic nitrogen fertilizers which are environmentally detrimental (Mahmud et al., 2020; Soumare et al., 2020). Furthermore, non-nodular bacteria like Gluconacetobacter diazotrophicus have expanded the scope of BNF to non-leguminous plants (Dent, 2018). Integrating nitrogen-fixing bacteria into sustainable agriculture reduces greenhouse gas emissions and enhances crop resilience, especially under drought conditions (Minamisawa, 2023).

Microorganisms also facilitate the solubilization of key nutrients like phosphorus and potassium, which are often unavailable in their natural forms. Phosphate-solubilizing bacteria (PSB) convert insoluble phosphate into bioavailable forms through organic acid production (Tahir et al., 2018). Similarly, potassium-solubilizing bacteria (KSB) enhance the availability of potassium, critical for plant water regulation and enzyme activation (Balakrishnan et al., 2021; Mei et al., 2021). For example, Bacillus megaterium and Pseudomonas fluorescens have been shown to effectively solubilize phosphate, improving plant growth in phosphorus-deficient soils (Patel et al., 2016).

Plant-associated bacteria, particularly from the genera of Bacillus and Pseudomonas, are capable of producing phytohormones such as auxins, cytokinins, and gibberellins. These hormones regulate critical aspects of plant development, including cell division and elongation. Bacillus megaterium is a prolific producer of indole-3-acetic acid (IAA), a key auxin that enhances root growth and nutrient uptake (Ahmed and Hasnain, 2010; Tanveer and Ali, 2022). In addition, cytokinins produced by Pseudomonas species promote shoot development and delay leaf senescence, contributing to plant health under stress conditions (Shahraki et al., 2022).

Ethylene, a plant hormone produced in response to stress, can inhibit plant growth. Certain bacteria mitigate the negative effects of ethylene by producing the enzyme 1-aminocyclopropane-1-carboxylate (ACC) deaminase, which breaks down ACC, the ethylene precursor. For instance, Pseudomonas stutzeri A1501 facilitates rice growth under saline conditions by reducing ethylene levels (Han et al., 2015). These ACC deaminase-producing bacteria not only promote plant growth but also improve tolerance to environmental stresses like drought and salinity (Glick and Nascimento, 2021; Ali et al., 2023).

Siderophores are iron-chelating compounds produced by bacteria and fungi to solubilize and transport iron in iron-limited environments. P. fluorescens and B. subtilis produce siderophores such as pyoverdine and bacillibactin, which improve iron acquisition in plants (Nithyapriya et al., 2021; Zhang et al., 2022). This activity not only enhances plant growth but also provides biocontrol against pathogens by limiting their access to iron, an essential nutrient (Lyng et al., 2023; Celina et al., 2024).

Exopolysaccharides are high-molecular-weight polysaccharides secreted by bacteria that form biofilms. EPS production facilitates bacterial adherence to plant roots, enhancing nutrient and water uptake. For example, Paenibacillus polymyxa produces EPS that aids in wheat root colonization and improves nutrient absorption (Yegorenkova et al., 2013). Biofilms protect the microbial community from environmental stresses, such as desiccation and salinity, and can also protect against pathogens by forming a physical barrier and competing for resources (Bokhari et al., 2021).

Microbial inoculation, central to agricultural microbiology, begins with the meticulous screening of strains for plant growth-promoting (PGP) traits under controlled conditions. Key traits include phosphate solubilization, nitrogen fixation, siderophore production, and plant hormone regulation. Fungal strains such as Purpureocillium sp. strain YZ1 have also been shown to modulate plant elemental uptake (Zheng et al., 2021). Strains that perform well in lab assays undergo greenhouse trials and subsequent field evaluations. Although microbial inoculants like Azospirillum brasilense Ab-V5 have demonstrated significant yield increases in maize and wheat under optimized conditions (Hungria et al., 2010), field efficacy remains variable, highlighting their potential when conditions are optimized (Fukami et al., 2016; Backer et al., 2018). Factors such as competition with native microflora, suboptimal strain selection, and environmental variables can undermine inoculant performance (Samad et al., 2017a). Formulation, including cell viability and niche compatibility, is crucial for sustained colonization and function (Chowdhury et al., 2015). Biocontrol agents like B. amyloliquefaciens FZB42 require early establishment and niche adaptation to trigger effective plant defenses (Chowdhury et al., 2015).

Emerging approaches advocate for using microbial consortia rather than single-strain inoculants to enhance reliability under diverse field conditions (Parnell et al., 2016; De Vrieze et al., 2018) Consortia offers complementary PGP effects and pathogen suppression, enhancing plant health and resilience (Berendsen et al., 2018). For example, P. consortia have demonstrated enhanced nutrient assimilation and stress resilience in plants (Guttieri et al., 2015; Hu et al., 2016). Tailoring consortia to specific environmental conditions and plant genotypes further enhances their efficacy, as shown by the host preference of Azospirillum (Chamam et al., 2013; Edwards et al., 2015; Santos-Medellín et al., 2017). Nonetheless, ongoing research is necessary to refine consortia selection and optimize their field performance (Herrera Paredes et al., 2018).

Effective microbial formulations are essential for maintaining inoculant viability and efficacy in the field. Techniques such as encapsulation and surfactant addition improve adherence to plant surfaces, reducing environmental stresses like drift and UV exposure (Preininger et al., 2018; Timmusk et al., 2018). Innovations such as seed microbiome modulation through flower spray inoculation hold promise for improving microbial colonization and plant growth throughout the crop cycle (Pfeiffer et al., 2017). Immobilization technology can be promising to enhance field efficacy of microbial inoculants (Wu et al., 2021).

The manipulation of existing natural microbial communities in situ is an important approach to improve plant health and productivity, which leverages the inherent diversity and functionality of microbial populations already present in the soil and plant environments. One effective strategy within this framework is the selective enhancement of beneficial microbial taxa through practices such as crop rotation, cover cropping, and organic amendments. These practices can promote the proliferation of beneficial microbes while suppressing pathogenic species, thereby enhancing plant resilience to stressors such as drought and disease (Carmen Orozco-Mosqueda et al., 2018; Wang and Haney, 2020).

In situ microbiome engineering also includes the application of microbial inoculants that are specifically tailored to enhance the native microbiome. For example, research has shown that inoculating crops with beneficial microbes can lead to significant increases in yield and stress tolerance (Lawson et al., 2019; Yang et al., 2023). Furthermore, the manipulation of root exudates through plant breeding or management practices can selectively recruit beneficial microbes, thereby optimizing the plant’s microbiome for enhanced performance (Clouse and Wagner, 2021; Nadarajah and Natasha Rahman, 2023).

Design of novel microbial systems is an emerging approach in microbiome engineering. Two notable systems in this category are the Intraspecies Cross Environmental (ICE) system and the Combinatorial CRISPR Array-Guided Engineering (CRAGE) system.

The ICE system focuses on creating synthetic microbial consortia that can thrive across different environmental conditions. By selecting and combining microbial strains that exhibit complementary traits, researchers can develop robust microbial communities capable of enhancing plant growth under varying stress conditions. This approach allows for the fine-tuning of microbial interactions to optimize nutrient cycling and plant health (Uroz et al., 2019; Afridi et al., 2022). For instance, synthetic consortia can be engineered to improve nitrogen fixation or phosphorus solubilization, directly benefiting plant growth (Kaul et al., 2021).

The CRAGE system utilizes CRISPR technology to engineer microbial genomes for specific functions that benefit plant health. By targeting genes involved in beneficial traits such as stress tolerance, nutrient uptake, or pathogen resistance, researchers can create microbial strains with enhanced capabilities. This method not only allows for precise modifications but also facilitates the study of gene function in microbial communities, paving the way for more effective microbiome engineering strategies (Dastogeer et al., 2022; Malayejerdi and Pouresmaeil, 2020).

Incorporating plant microbiomes into crop breeding programs represents a crucial frontier in enhancing stress tolerance, nutrient uptake, and productivity (Haichar et al., 2008; Bakker et al., 2012; Ofek et al., 2014; Wei and Jousset, 2017) (Figure 2). Different genotypes foster distinct microbial associations, yet the genetic mechanisms driving these interactions remain poorly understood. Domestication has reduced plant genetic and microbial diversity, limiting the ability of modern crops to interact with beneficial microbes (Haudry et al., 2007; Bitocchi et al., 2013; Gopal and Gupta, 2016). However, recent studies reveal significant differences in microbial diversity and composition across sugarcane cultivars, highlighting the potential to select cultivars that promote beneficial microbial associations (Tayyab et al., 2022). Integrating microbiome considerations into breeding practices is pivotal for advancing sustainable agriculture and optimizing productivity (Li et al., 2024).

Agricultural practices, such as intercropping, organic farming, and reduced tillage, significantly influence plant-microbe interactions (Sánchez-Cañizares et al., 2017) (Figure 2). Practices like organic farming can enhance microbial diversity and abundance, improving ecosystem resilience and plant health (Hartmann et al., 2015; Hartman et al., 2018). For example, sugarcane–legume intercropping has been shown to enhance soil fertility and microbial diversity without compromising crop yields (Pang et al., 2022). The use of bacterial biological control agents also shows promise, with studies demonstrating improved soil chemistry, enriched beneficial microbial communities, and enhanced crop productivity in ratoon sugarcane (Fallah et al., 2023).