Plants have conserved immune signaling initiated by the recognition of microbe-associated molecular patterns (MAMPs) from external microbes (Muthamilarasan and Prasad, 2013).

Pattern recognition receptors (PRRs) localized on the plant cell surface can recognize MAMPs of pathogenic or non-pathogenic microbes, triggering MAMP-triggered immunity (MTI) in plants (Boller and Felix, 2009; Muthamilarasan and Prasad, 2013). Once PRRs recognize MAMPs, they activate a mitogen-activated protein kinase (MAPK) cascade, which eventually activates WRKY family transcription factors (Pandey and Somssich, 2009; Muthamilarasan and Prasad, 2013). WRKY transcription factors induce the biosynthesis of defense-related phytohormones, such as salicylic acid (SA), jasmonic acid (JA), and ethylene (ET), and promote the production and secretion of antimicrobial compounds into vacuoles (Muthamilarasan and Prasad, 2013).

Plant hormones like SA, JA, ABA, ET, and cytokinin play roles in plant defense resistance. Notably, JA and cytokinin are reported to be mobile among leaves, from shoot to root, and root to shoot ( Figure 1A ) (Soler et al., 2013). Although SA does not move among leaves, Methyl salicylate (MeSA) moves from cell to cell among leaves or through phloem and is converted to SA in distal leaves (Park et al., 2007) ( Figure 1A ). Among other hormones, ABA is mobile among leaves and from root to shoot, while ET has been reported to move from root to shoot (Soler et al., 2013) ( Figure 1A ). As ET is gaseous hormone, it can diffuse throughout the plant. However, this diffusion refer to general movement rather than directional transport with specific orientation (Binder, 2020). These hormones could potentially induce local defense responses again upon reaching a new location.

In addition to hormones, several long-distance mobile signals have been identified as key players in SAR. These include glycolipids, which are lipid-based molecules acting as signaling compounds in plant defense responses (Chaturvedi et al., 2008). Another important signal is azelaic acid, a dicarboxylic acid that primes plants for enhanced defense activation and contributes to SAR signal generation (Jung et al., 2009). Glycerol-3-phosphate (G3P) also plays a crucial role in SAR as a metabolite synthesized in the cytosol and chloroplasts (Chanda et al., 2011; Shine et al., 2019). Pipecolic acid, a non-protein amino acid, acts as a critical regulator of plant systemic immunity (Návarová et al., 2012). It accumulates in both local and distal tissues following pathogen infection and is essential for SAR activation and priming of plant defenses (Návarová et al., 2012). These diverse molecules work in concert to establish and maintain SAR, enhancing the plant's ability to defend against subsequent pathogen attacks.

The above examples explain mobile phytohormones and small molecules that transfer and function in distal locations. Signals that migrate to the roots could potentially alter the composition of root exudates. These studies support that plant root exudates function to reshape the rhizosphere microbiome, thereby directly affecting belowground evaders or enabling the utilization of surrounding beneficial substances.

Above-ground stimuli in plants change below-ground root exudation components, which directly and indirectly lead to the reshaping of the rhizosphere, providing feedback to the plants (Lee et al., 2012; Kim et al., 2016; Hoysted et al., 2018; Friman et al., 2021). Plants with above-ground stimulation may selectively attract specific microorganisms into their rhizosphere. Interestingly, phloem-feeding aphid infestation in pepper (Capsicum annuum) leaves attracts beneficial bacteria, such as Bacillus subtilis and Paenibacillus spp., but not pathogenic bacteria like Ralstonia solanacearum, to their roots ( Figure 1B ; Table 1 ) (Lee et al., 2012; Kim et al., 2016). These results suggest that plants actively and selectively reshape the below-ground microbiome in response to above-ground stimuli. How do plants selectively recruit beneficial microbes to the rhizosphere? For example, Pst DC3000 infection in Arabidopsis leaves led to the secretion of malic acid from their roots ( Table 1 ) (Rudrappa et al., 2008). Interestingly, B. subtilis strain FB17 exhibits malic acid chemotaxis, suggesting that malic acid may be a key factor in recruiting B. subtilis strain FB17 (Rudrappa et al., 2008). Finally, the B. subtilis strain FB17 induced systemic resistance against Pst DC3000, demonstrating how sessile plants actively trigger defense responses using surrounding beneficial bacteria ( Figure 1D ) (Rudrappa et al., 2008).

Above-ground attacks on plant leaves may influence plant root exudate. Recent studies have shown that root exudate components change following above-ground infections (Doornbos et al., 2012; Kim et al., 2016). Root exudation profiles in Pseudomonas syringae pv. tomato (Pst)-infected Arabidopsis exhibited significantly higher levels of amino acids, nucleotides, and long-chain organic acids (LCOAs) (C > 6) and lower levels of sugars, alcohols, and short-chain organic acids (SCOAs) (C ≤ 6) ( Table 1 ) (Yuan et al., 2018). Interestingly, since exogenous amino acids and LCOA application to plants showed disease-suppressive responses, the pst-induced root exudation may function as plant’s defense enhancement (Yuan et al., 2018). Similarly, aphid-infested potato leaves also showed reduced sugar contents in root exudates (Hoysted et al., 2018). Root exudates from aphid-infested potato (Solanum tuberosum L.) showed reduced glucose and fructose contents, resulting in lower hatching rates of below-ground endoparasitic nematode Globodera pallida ( Table 1 ; Figure 1B ) (Hoysted et al., 2018). However, sugar supplementation did not recover the hatching potential of G. pallida, indicating that root exudation may involve other important factors for egg hatching ( Figure 1B ) (Hoysted et al., 2018). In the case of chewing insect stimuli, leaf area and biomass decrease by Spodoptera frugiperda-infested maize leaves correlated with changes in root exudate compounds (Adame-Garnica et al., 2023). The degree of S. frugiperda infestation modulated the root exudation contents, non-structural carbohydrates (NSCs), 6-methoxy-2-benzoxaxolin-2-one (MBOA), and the reactive oxygen species H₂O₂, leading to the growth inhibition of the rhizosphere fungus Trichoderma atroviride ( Table 1 ; Figure 1B ) (Adame-Garnica et al., 2023). This result clearly demonstrates the top-down effect of above-ground insect attacks, showing how they influence root exudation and, consequently, effect on rhizosphere fungus.

Recent studies have provided molecular evidence of changes in root exudates. For example, JA is a critical hormone involved in plant defense responses, has been shown to influence root exudation. Root exudates from Arabidopsis JA mutants, such as myc2 and med25, showed reduced levels of asparagine, ornithine, and tryptophan (Carvalhais et al., 2015). Additionally, these myc2 mutants had an increased abundance of Streptomyces, Bacillus, and Lysinibacillus taxa in the rhizosphere, suggesting that JA-dependent root exudates alterations affect microbiome communities (Carvalhais et al., 2015).

A recent study indicated that the ripening-inhibitor (RIN) transcription factor plays a role in assembling disease-suppressive rhizosphere microbiota by altering root exudates. RIN tomato mutant exhibited lower concentration of 3-hydroxyflavone and riboflavin in their root exudates, leading to reduction in pathogen-suppressing Actinobacteria (Streptomyces) in the rhizosphere (Yang et al., 2023). The disease suppressiveness of the rin plant microbiome was restored by complementing with 3-hydroxyflavone and riboflavin (Yang et al., 2023).

Interestingly, plant root exudates also changed in response to fusaric acid (FA), produced by Fusarium oxysporum (Jin et al., 2024). FA differently altered the root exudate components of two tomato cultivars; F. oxysporum f. sp. lycopersici resistant Z19 and susceptible D72. FA enhanced colonization of disease-suppressive bacteria, Sphingomonas sp., in the resistant cultivar Z19 (Jin et al., 2024). These microbiome changes provided feedback, leading to defense resistance to F. oxysporum in the resistant cultivar Z19 (Jin et al., 2024).

Flg22 is highly conserved domain of bacterial flagellin, recognized as a MAMP by the plant FLS2 receptor, resulting in MTI (Felix et al., 1999). Pseudomonas capeferrum WCS358, a well-known PGPM (Meziane et al., 2005), suppresses flg22-mediated Arabidopsis root immunity by producing gluconic acid and shows enhanced colonization in Arabidopsis roots compared to gluconic acid production mutants (pqqF::Tn5 and cyoB::Tn5) ( Table 1 ) (Yu et al., 2019a). Another study, using a high-throughput transposon (Tn-Seq) screening system in Pseudomonas sp. WCS365, found that morA and spuC mutants induced MTI, enhanced biofilms formation, and inhibited the growth of Arabidopsis compared to the wild type ( Table 1 ) (Liu et al., 2018). MorA (encoding phosphodiesterase) and SpuC (encoding putrescine aminotransferase) are related to the suppression of biofilm formation. This biofilm inhibition may be one of the microbes' strategies for evading MTI and fitting within the rhizosphere.

Considering that ISR occurs through the recognition of microbial-derived factors by the plant, the symbiosis between plants and microbes is crucial (Zamioudis and Pieterse, 2012). However, current studies suggest that some ISR responses might not require a symbiotic association (Vishwanathan et al., 2020). For example, the ectomycorrhizal fungus Laccaria bicolor can trigger ISR against the insect Trichoplusia ni in Arabidopsis, a nonmycorrhizal plant (Vishwanathan et al., 2020). Therefore, the crucial factor may lie more in how effectively the plant responds to ISR elicitors secreted by microbes, rather than the duration of the plant-microbes symbiotic relationship.

Plants may recognize signals from rhizosphere microbes for inducing ISR. Then, what happens in plant roots for initiating ISR signaling?

Pseudomonas fluorescens WCS417r is known for inducing ISR against a broad spectrum of pathogens in Arabidopsis. However, P. fluorescence WCS417r showed impaired ISR in myb72-1 and myb72-2 Arabidopsis mutant against Pseudomonas syringae pv tomato, Hyaloperonospora parasitica, Alternaria brassicicola, and Botrytis cinerea ( Table 1 ; Figure 1C ) (Van der Ent et al., 2008). Indeed, the root-specific transcription factor MYB72 appears to be a convergence node, as it is essential for early signaling in ISR induction by P. fluorescence WCS417r and Trichoderma asperellum T34 (Van der Ent et al., 2008; Segarra et al., 2009). The author suggest MYB72 is upstream of ET signaling, as WCS417r activated MYB72 in ethylene-insensitive ein2-1 plants, and exogeneous ethylene precursor 1-aminocyclopropane-1-carboxylate (ACC) induced ISR responses in myb72-1 mutants ( Figure 1C ) (Van der Ent et al., 2008).

Chitin, one of the MAMPs of microbes, has been shown to induce ISR (Vishwanathan et al., 2020; Takagi et al., 2022). L.bicolor triggers ISR in Arabidopsis against Trichoplusia ni ( Figure 1C ) (Vishwanathan et al., 2020). Molecular evidence suggest that chitin derived from L.bicolor is an ISR-inducing molecules, as heat-killed L. bicolor or chitin also trigger ISR, but the chitin receptor mutant cerk1-2 could not trigger ISR by L.bicolor or chitin ( Table 1 ) (Vishwanathan et al., 2020). Another study showed that chitin-induced ISR against Bipolaris oryzae in rice is related to down-regulated cytokinin signaling, resulting in alterations of cell-wall components ( Table 1 ) (Takagi et al., 2022). Therefore, chitin-induced ISR is mediated by perturbation in cell-wall biogenesis in leaves.

Regarding PGPM interactions with plant roots, the root hair is the first part of the plant to interact with microbes. Root hair-specific syntaxin gene SYP123 is suggested to be necessary for PGPM-triggered ISR, as ISR marker genes (PR1, MYC2, and PDF1.2) did not increase in syp123 Arabidopsis mutants in response to beneficial Pseudomonas species (Rodriguez-Furlán et al., 2016; Zhu et al., 2022).

In the case of root-to-shoot communications, the root-knot nematode (RNK) Meloidogyne incognita induces the transition of ROS signals from root to leaves of tomato, resulting in JA accumulation in leaves ( Figure 1C ) (Wang et al., 2019). The M. incognita-induced signal transduction involves RBOH1, GLR3.5, and MPK1/2-dependent JA accumulation, as JA accumulation in leaves was abolished in grafting experiments with scion of the mutant GLUTAMATE RECEPTOR-LIKE 3.5 (GLR3.5), RESPIRATORY BURST OXIDASE HOMOLOG1 (RBOH1), and plant silenced for mitogen-activated kinases1 (MPK1) or MPK2 (Wang et al., 2019). The RNK M. incognita induced-JA accumulation in leaves transfers to the roots, triggering resistance to RNK ( Table 1 ) (Wang et al., 2019).

Oxylipins are oxidized lipid signals that regulate plant physiological responses to abiotic and biotic stress, including defense responses against pathogens and insects (Wang et al., 2019). Several non-jasmonate oxylipins have been identified as crucial regulators for ISR in various plant species. In maize, two xylem-mobile oxylipins, 12-oxo-phytodienoic acid (12-OPDA) and an γ-ketol of octadecadienoic acid (KODA), play important roles in ISR (Wang et al., 2019; Carella, 2020). Additionally, two γ-ketols, 12-Oxo-9-hydroxy-10(E)-octadecenoic acid (9,12-KOMA) and 12-Oxo-9-hydroxy-10(E),15(Z)-octadecadienoic acid (9,12-KODA), have been identified as ISR priming agents in maize (Wang et al., 2020). The small secreted protein Sm1 from PGPM virens triggers ISR regulating 12-OPDA and KODA biosynthesis in maize plants ( Table 1 ) (Wang et al., 2019). Similarly, Pseudomonas putida BTP1 induced ISR against Botrytis cinerea by accumulating two antifungal oxylipin, free 13-hydroperoxy-octadecatrienoic (13-HPOT) and 13-hydroxy-octadecatrienoic acids (13-HOT), in tomato ( Figure 1C ; Table 1 ) (Mariutto et al., 2011).

Recently, microRNAs have also been suggested as mobile signals for plant-microbe interactions (Xie et al., 2019). Bacillus velezensis FZB42, which is reported to induce ISR, showed that four miRNAs, zma-miR169a-5p, zma-miR169c-5p, zma-miR169i-5p, and zma-miR395b-5p, belonging to the miR169 family, are associated with triggering ISR by regulating nuclear factor Y transcription factor in maize ( Table 1 ) (Xie et al., 2019).