Plant-parasitic nematodes (PPNs) infect a wide range of food crops and cause severe damage (Nicol et al., 2011; Jones et al., 2013; Kantor et al., 2022). PPNs control costs several billions of dollars annually to the global agriculture industry (Elling, 2013; Gamalero and Glick, 2020; Kantor et al., 2022). Among these, root-knot nematodes (RKN) are the most economically significant plant pathogens due to the high levels of damage and infection they cause, their wide host and geographic ranges, and interaction with other plant pathogens (Rehman et al., 2012; Topalović and Geisen, 2023). The second-stage juvenile (J2) is the only infective stage of RKN. In plant roots, the J2s undergo two developmental stages (J3 and J4) before an adult stage. Adult females establish feeding sites and cause root galls (Eisenback and Triantaphyllou, 1991; Karssen and Moens, 2006; Gheysen and Mitchum, 2011).

The above-ground symptoms of RKN-infected plants include poor plant growth, necrosis on leaves, and rapid wilting under environmental stress caused by water deficiency or other factors (Bernard et al., 2017; Elnahal et al., 2022). The obvious below-ground symptom of RKN infection is the formation of galls on the roots that reduce the absorption and translocation of water and dissolved nutrients. RKN root damage also fosters access to secondary infection of roots by soil pathogens such as fungi and bacteria (Agrios, 2005; Cao et al., 2023). Because of their wide host range and distribution, effective RKN management is becoming a global priority. Effective RKN management may require an integrated application of control strategies such as chemical nematicides, resistant crops, trap crops, organic amendments, and different microbial agents (Desaeger et al., 2020; Forghani and Hajihassani, 2020; Topalović et al., 2020b). Synthetic chemical nematicides are effective in controlling RKN and are widely used around the globe but their use has been restricted due to their negative impact on human health and the environment (Katooli et al., 2010; Desaeger et al., 2020). Thus, there is a critical need for alternative nematode control methods which are both effective in controlling RKN and environmentally sustainable.

RKN management strategies using antagonistic soil microbiota would offer an ecologically sound RKN control (Zhang et al., 2017; Abd-Elgawad, 2021; Aioub et al., 2022). A broad range of soil microbiota reduced nematode infection directly or indirectly in plants (Eberlein et al., 2016; Ashrafi et al., 2017; Hamid et al., 2017; Hussain et al., 2018; Nuaima et al., 2021). These microbes use antibiosis, parasitism, induced systemic resistance (ISR) in plants, or apply a combination of different strategies that can interfere with nematode infection in plants (Chen and Dickson, 1998; Siddiqui et al., 2005; Martínez-Medina et al., 2017; Poveda et al., 2020). One subset of soil microbiota showing RKN suppression is plant growth promoting bacteria (PGPB). Here, we define PGPB as bacterial community inhabiting soil around roots (rhizosphere bacteria) and inside plant roots (endophytic bacteria) and promoting plant growth through a variety of processes such as biofertilization, phytohormone production, antipathogenic activities and ISR (Lugtenburg and Kamilova, 2009; Aioub et al., 2022; Gowda et al., 2022).

PGPB stimulate plant growth by supplying essential plant nutrients such as nitrogen (N), phosphorus (P), potassium (K), and other micronutrients such as iron (Fe), and promote soil bioremediation by secreting a variety of metabolites and hormones (Poria et al., 2022). PGPB have a direct influence on both plant development and metabolism through the production of phytohormones and plant growth regulators (Chandra et al., 2018). Microbial phytohormones and phytostimulators such as auxins, ethylene, cytokines, gibberellin, abscisic acid, salicylic acid and jasmonic acid are important in plant biological processes such as cell division and elongation (Lugtenburg and Kamilova, 2009; Tsukanova et al., 2017; Shaffique et al., 2023). Phytohormones and enzymes such as 1-aminocyclopropane-1-carboxylate (ACC) produced by PGPB also alleviate various forms of stress, including infections by pathogenic bacteria, resistance to stress induced by polyaromatic hydrocarbons, heavy metals such as Ni²⁺ and environmental stresses such as salt and drought (Glick et al., 2007; Lugtenburg and Kamilova, 2009; Zhang et al., 2020; Sharifi et al., 2022). PGPB are also involved in antipathogenic activities through antagonism, signal interference, predation, parasitism, competition, and induced systemic resistance (ISR) (Milner et al., 1996; Bassler, 1999; Ryu et al., 2003; Emmert et al., 2004; Aioub et al., 2022). Thus, the use of PGPB for RKN control is an ecologically sound strategy for suppressing RKN using naturally occurring species, introducing them to the rhizosphere or manipulating the soil through different agricultural practices that enhance their performance (Topalović et al., 2019; Topalović et al., 2020b; Eldeeb et al., 2022).

Despite several promising RKN control results under laboratory and greenhouse settings, transitioning from lab to field has been challenging due to inconsistencies in microbial agent performance in the field conditions (Topalović and Heuer, 2019). Some reasons for that are the weak competitive ability of the microbial agents and the failure to establish a high density in soil ecosystems. In soil ecosystems, host-RKN interactions are complex and can be affected by different soil physicochemical and biological properties (Cao et al., 2023). Soil physicochemical and biological properties modulate host-RKN interactions, and they are in turn affected by different agricultural practices. Therefore, the knowledge of how soil biotic and abiotic factors modulate the host-RKN-PGPB (tripartite, Figure 1 ) interactions would be critical to develop economically and ecologically sound RKN control strategies. This review emphasizes the tripartite phenomenon with respect to (i) PGPBs’ direct and indirect effect on RKN-host interactions; (ii) the host’s influence in the selection and enrichment of PGPB in the rhizosphere; (iii) the influence of the host in RKN-PGPB interactions; (iv) the role of soil microbes in enhancing RKN parasitism, and (v) the role of abiotic factors in modulating the tripartite interactions. Furthermore, the paper delves into how different agricultural practices alter the host-RKN-PGPB interactions. Finally, it concludes by emphasizing the importance of incorporating the knowledge of tripartite interactions in the integrated RKN management strategies.

PGPB have a direct and indirect effect on RKN and affect the interaction between the host and RKN ( Figure 1 ).

Different plant species selectively attract different communities of PGPB and influence their composition when grown on the same soil (Berendsen et al., 2012). The PGPB exhibit significantly higher population densities in the rhizosphere compared to the bulk soil, primarily due to plants releasing up to 40% of their photosynthates as root exudates (Bais et al., 2006). However, their diversity is low in the rhizosphere compared to the bulk soil (Berg et al., 2006; Costa et al., 2006; Hein et al., 2008; Berendsen et al., 2012) indicating PGPB community establishment is driven by host plant selection (Li et al., 2019b; Yin et al., 2021). The type and age of the host plant, and biotic and abiotic stresses influence the compositions of root exudates (Lundberg et al., 2012; Chaparro et al., 2014; Bulgarelli et al., 2015; Tkacz et al., 2015; Kantor et al., 2018; Yin et al., 2021). Thus, the composition of root exudates actively secreted by plants shape the PGPB community by stimulating or repressing the subset of the PGPB community in the soil (Doornbos et al., 2012). Components of root exudates such as sugars, organic acids, metabolites, phytohormones, and complex mucus-like polymers play a key role in shaping the composition and structure of PGPB community (Broeckling et al., 2008; Carvalhais et al., 2015; Berendsen et al., 2018; Sasse et al., 2018; Yuan et al., 2018; Wen et al., 2020, 2021; Kong et al., 2021).

For example, long-chain fatty acids and amino acids were identified to play a crucial role in attracting PGPB, including Pseudomonas populations (Yuan et al., 2018; Wen et al., 2021). Additionally, a higher release of four short-chain organic acids (citric acid, pyruvate acid, succinic acid, and fumarate) has been linked to the increased presence of PGPB such as Comamonadaceae spp (Wen et al., 2020). Root-secreted malic acid has also been linked to the attraction of Bacillus spp. to the rhizosphere (Rudrappa et al., 2008). Therefore, the particular ratios and makeup of root exudates significantly influence the PGPB composition (Badri et al., 2009; Zhou and Wu, 2012).

Secondary metabolites secreted by plant roots can also be detrimental for the growth of specific group of microbes in the rhizosphere (Bais et al., 2002; Zhang et al., 2011). Benzoxazinoids are exuded in relatively large quantities from cereal roots and can inhibit rhizosphere microbes (Berendsen et al., 2012). In maize (Zea mays), 2,4-dihydroxy- 7-methoxy-2H-1,4-benzoxazin-3(4H)-one (DIMBOA) is the main antimicrobial benzoxazinoid. In contrast, PGPB P. putida KT2440 was attracted and tolerant to DIMBOA (Berendsen et al., 2012; Neal et al., 2012). In the absence of DIMBOA, the colonization of roots by KT2440 strain was lower (Berendsen et al., 2012; Neal et al., 2012). Secondary metabolites have shown promising nematocidal activity. Notably, various metabolites synthetized by wild watermelon roots have been documented in literature for their effectiveness in controlling nematodes (Kantor et al., 2018).

Plants also produce compounds that stimulate or repress quorum-sensing (QS)-regulated responses in PGPB. These QS-interfering compounds enable the plant to manipulate gene expression in their PGPB communities (Berendsen et al., 2012). PGPB utilize QS to signal each other and regulate expression of certain genes by using diffusible N-acyl-homoserine lactones (AHLs) (Elasri et al., 2001; Berendsen et al., 2012). AHL-mediated regulation typically makes use of two proteins that resemble the LuxI and LuxR protein families. LuxI-like proteins are AHL synthases, whereas LuxR-like proteins function as receptors of AHL that can form complexes with AHL which in turn can affect gene expression of QS-target genes (Decho et al., 2011; Berendsen et al., 2012). For instance, seedling extracts and exudates of barrel clover (Medicago truncatula), pea (Pisum sativum), rice (Oryza sativum) and green algae (Chlamydomonas reinhardtii) had compounds that specifically stimulated or repressed responses in QS-reporter bacteria (Teplitski et al., 2000; Gao et al., 2003; Teplitski et al., 2004; Ferluga and Venturi, 2009). Some plant-associated PGPB have LuxR-like proteins that are stimulated by plant-derived signals, whereas they themselves do not produce AHLs (Ferluga and Venturi, 2009; Berendsen et al., 2012). Thus, plants recruit and shape the rhizosphere microbes through the composition of root exudates and secondary metabolites. These substances selectively attract or repel soil microbiota and play a role in controlling the expression of QS-regulated genes of soil microbiota.

Root exudates are important in nematode attraction to plant roots and directly affect nematode interactions with PGPB by inducing changes in the surface of PPNs. PGPB interact with PPNs through the nematode surface coat (SC). SC is a glycoprotein layer secreted by the hypodermis, or by the excretory and nervous systems (Lin and McClure, 1996; Curtis et al., 2011). Receptors on nematode SC mediate the specific interaction with the lectine-like protein molecules on PGPB surface (Bird, 2004; Davies and Curtis, 2011). Studies showed that nematode SC exposed to different root exudates and secondary metabolites also undergoes modifications which influence PGPB attachments to RKN surface (Akhkha et al., 2002; Curtis, 2008; Singh et al., 2014; Liu et al., 2017). Pasteuria penetrans endospores attachment to J2 of RKN were variable in response to root exudates from different plant species (Singh et al., 2014; Liu et al., 2017). For instance, M. incognita J2 exposed to the root exudates showed greater P. penetrans endospores attachment (Singh et al., 2014). These results indicated that the influence of specific host root exudates on RKN-PGPB interactions in the soil favors RKN antagonistic microbes attachment (Topalović et al., 2020c).

J2-attached PGPB can also increase hosts’ resistance to RKN. PGPB attaching to J2 of M. hapla prior to J2 infection enhanced their detection by upregulating several pattern-triggered immunity (PTI)-responsive defense genes (Topalović et al., 2020a). Moreover, chemicals produced by M. hapla J2 with attached Microbacterium sp. K6 strain activated a greater reactive oxygen species (ROS) response in tomato roots. Such a greater increase in ROS was not detected for nematodes without the K6 strain. Besides, hundred-fold ROS response was observed in the leaves than the roots for J2 with attached Microbacterium sp. K6 strain (Topalović et al., 2020a, b, c). Therefore, J2-attached PGPB prior penetrating roots can activate ISR that inhibits RKN establishment.

Recent research findings suggest that the success of RKN root invasion is influenced by the root exudates and PGPB in the rhizosphere which determine whether the RKN surface molecule is recognized by plant roots or not (Topalović et al., 2020c). Thus, host plant root exudates components play a key role for the communications between plants and nematodes, and nematode-PGPB interaction by modulating components of the nematode SC (Topalović et al., 2020c). Based on the host range of the nematode and the PGPB composition, RKN may either bypass plant defense responses to infiltrate the roots or be antagonized within or outside the plant. Thus, plants are utterly dependent on PGPB during nematode invasion, which results in the proliferation of a certain group of PGPB community protecting the host (Hussain et al., 2018; Topalović et al., 2020c). This suggests that the dynamic tripartite phenomenon in soil leads to nematode suppression by microbially induced systemic resistance in plants (Topalović et al., 2020a).

RKN juveniles, while actively searching for roots in the soil, are likely to encounter and attach to a functionally diverse array of soil microbes. This array includes both antagonistic and protective surface microbes (Topalović and Vestergård, 2021). The holobiont concept suggests that each macroorganism has developed a mutually beneficial relationship with specific microbiota that influences its health and survival. Additionally, it infers that the microbial moiety of a holobiont can undergo modifications in response to environmental stress (Bordenstein and Theis, 2015). Soil microbes can protect PPNs in soil by outcompeting nematode antagonists for attachment sites on the nematode’s surface, reducing nematode recognition, or by producing compounds that are toxic to nematode antagonists (Topalović and Vestergård, 2021).

RKN J2s may avoid antagonists by recruiting protective soil microbiota to their surface. A recent study revealed that J2-attached microbes’ compositions were different on actively moving J2 surface of Meloidogyne hapla and M. incognita in the presence of Pseudomonas protegens strain CHA0, a bacterial antagonist (Topalović et al., 2023). In the absence of P. protegens strain CHA0, bacterial genera such as Delftia, Variovorax and Pseudomonas attached on both active and inactive J2s but not on J2 treated with P. protegens strain CHA0. P. protegens CHA0 also activated proliferation of Flavobacterium spp. and Cutibacterium spp., and Methylophilaceae family within the Gammaproteobacteria, which might have protective role on active nematodes in M. hapla and M. incognita, respectively (Tsuru et al., 2021; Topalović et al., 2023). The presence of P. protegens CHA0 might also change the surrounding microbial community by reducing the prevalence of nematode antagonistic taxa such as Pseudomonads may be due to a release of secondary metabolites from P. protegens CHA0 (Topalović et al., 2023). Such antimicrobial compounds might play a role in reducing the abundance of nematode antagonists in the soil in the presence of RKN protective soil microbiota.

PGPB attachment to nematode surface can reduce the nematode recognition by plants during the infection process by masking the nematode receptors (Curtis, 2008; Mendy et al., 2017; Topalović et al., 2020c). RKN surface-attached microbes may also facilitate RKN establishment by helping in the creation of a feeding site and enhancing nutrition available for the nematodes (Cao et al., 2015). Community analysis of root-associated microbiomes in healthy and RKN-infected tomatoes showed that nematode infections were associated with variation and differentiation of the endophyte and rhizosphere bacterial populations in plant roots (Tian et al., 2015). Bacterial genera with N-fixing (Sinorhizobium spp. and Devosia spp.) and cellulose-degrading (Sphingomonadaceae) abilities were found associated with different life stages of M. incognita on tomato (Cao et al., 2015; Tian et al., 2015). As the plant does not recognize N-fixing bacteria as pathogens, their introduction may deter RKN recognition and immune responses against the RKN. In addition, detecting cellulose-degrading bacterial groups may suggest that the gall-enriched cellulose-degrading bacteria may help nematodes in feeding site formation (Tian et al., 2015; Yergaliyev et al., 2020). Overall, soil type, plant genotype, the specific interaction between soil microbiota and nematode surface, and the movement of J2 influence the composition of J2-attached microbial community (Adam et al., 2014; Elhady et al., 2017; Topalović et al., 2019; Elhady et al., 2021; Topalović et al., 2023).

Soil abiotic factors can affect host-RKN interactions through their impact on plant and RKN growth and development, and/or the activities of PGPB ( Figure 2 ). RKN spend a phase of their life cycle (J2) in soil, the composition, and properties of which affect J2 motility and distribution, as well as their development inside their host (Norton, 1989; Mateille et al., 2014). Soil abiotic factors (soil physical properties such as temperature, texture, structure, and moisture content; soil chemical properties such as soil pH and mineral compositions) affect RKN behavior and development and in turn host-RKN interactions (Palomares-Rius et al., 2015). They also affect host growth and development such as root size, numbers, softness and quality and quantity of root exudates, and in turn RKN behavior and development (Castillo et al., 2006; Landa et al., 2014). Soil abiotic factors also affect the movement of volatiles released from roots and PGPB and alter the interactions of host-RKN-PGPB as volatiles play key roles in mediating intra- and inter-kingdom communications (Sharifi and Ryu, 2018; Erktan et al., 2020; Wester-Larsen et al, 2020; Lee and Ryu, 2021). While soil abiotic factors affect soil microbiota which in turn can affect host-RKN interactions as aforementioned, an in-depth analysis of this topic falls beyond the scope of this review as its main theme is to discuss the role of PGPB and abiotic factors on host-RKN interactions. Rather, in the following sections we will mainly discuss the major soil abiotic factors affecting host-RKN interactions by focusing on their impact on plants and RKN.

Agricultural practices (APs) modulate the host-RKN-PGPB interactions by affecting plant and RKN development as well as altering soil’s physicochemical and biological properties (Habteweld et al., 2022). Common APs in conventional agriculture such as tillage, the use of inorganic fertilizers, and chemical pesticides and herbicides, may increase plant growth but often have harmful effects on the environment and human health (Lal, 2008; Diacono and Montemurro, 2010). For instance, conventional tillage has a negative impact on PPN populations by changing the physicochemical properties of the soil (Dick, 1992; Freckman and Ettema, 1993; Pankaj et al., 2006; Duplay et al., 2014). These changes can modify nematodes’ metabolism and reduce their mobility or access to food sources by removing weeds and altering their living habitats (e.g. living depth and soil structure) (McSorley and Dickson, 1990; Ou et al., 2005; Ekschmitt and Korthals, 2006; Mateille et al., 2014; Palomares-Rius et al., 2015; Garcia et al., 2022). The repeated use of synthetic fertilizers causes decline in soil physicochemical and biological properties (Odunze et al., 2012; Eche et al., 2013; Singh et al., 2013) that can in turn affect plant-RKN interactions. Acidic soil pH caused by the repeated application of chemical fertilizers negatively affects soil biological property which favors some pathogens. It also reduces plant growth, nutrient availability, and may affect the tripartite interactions (Singh et al., 2013; Habteweld et al., 2020a). N fertilizers, for example, promote plant growth leading to high carrying capacity for RKNs (Noronha et al., 2021) or decreasing RKN population density due to the release of nitrogenous compounds such as NH₃ (Karajeh and Al-Nasir, 2012; Wei et al., 2012; Patil et al., 2013; 2014). Moreover, the use of insecticides and fungicides and soil disturbances due to tillage could eliminate potential natural enemies of RKN such as nematophagous fungi (Stirling, 2014; Kumar et al., 2017) leading to increased RKN populations and reduced plant growth (Garcia et al., 2022).

In contrast, cultural APs such as organic amendments, mulching, crop rotation, cover cropping and conservation tillage increase the availability of nutrients, improve soil structure leading to better moisture retention and soil microbial activity, reduce fertilizer loses to the environment, and increase plant growth (Oquist et al., 2007; Forge and Kempler, 2009; Glover et al., 2010; Zhang et al., 2014, 2016; Habteweld et al., 2020a, 2020b). Compost stands as one of the most widely employed organic amendments, demonstrating its ability to enhance soil organic matter, augment nutrient content, stimulate microbial activity, suppress pests, and contribute to overall soil health improvement (Bulluck et al., 2002; Forge and Kempler, 2009; Ferris et al., 2012; Habteweld et al., 2018, 2022). Incorporating compost as soil amendment increases soil pH by forming an aluminum complex and increasing base saturation (Shiralipour et al., 1992; Van den Berghe and Hue, 1999). In addition, organic amendments (composts, plant residues, animal manures, and plant derivatives) increase plant growth parameters (shoot fresh weight or dry weight) and decrease RKNs damage attributes, i.e. soil RKNs numbers, number of root galls, and number of eggs/egg masses in roots (Peiris et al., 2020). Organic APs are also known to enhance soil microbial activities including RKN antagonists (Silva et al., 2022). Rhizosphere soil under organic cultivation recruit RKN antagonistic bacteria genera such as Pseudomonas, Serratia, Bradyrhizobium, Burkholderia and Azospirillum and fungal genera such as Beauveria, Clonostachys, Metarhizium, Purpureocillium and Arthrobotrys (Silva et al., 2022). Thus, organic APs are potential candidates to modify soil and crop management as part of integrated strategies, thus enhancing the tripartite interactions towards RKN suppression and promoting plant growth and environmental safety.

RKNs are the most widespread PPNs in agricultural soils, infecting thousands of crops and causing annual losses of billions of dollars around the globe. The currently most effective and widely used RKNs control technique is the use of chemical nematicides. However, due to human health and environmental concerns, the use of many of these nematicides was banned or restricted. Therefore, there is a pressing need for effective and environmentally friendly alternative RKN control strategies. One such alternative is the use of RKN antagonistic microorganisms. However, microbial agents that were found to be effective in controlling RKN in the laboratory and/or in the greenhouse conditions often do not replicate the same level of control in the more complex soil ecosystems. The low efficacy of microbial agents may be attributed to overlooking native microbiota that possesses protective abilities for RKN, as well as to soil abiotic factors that modulate the host-RKN-PGPB interactions. Consequently, a deeper understanding of the dynamics of host-RKN interactions in varied biotic and abiotic environments could be pivotal in devising novel RKN control strategies.

The utilization of PGPB for controlling RKN and fertilizing plants holds significant importance in agroecosystems, primarily due to their positive environmental impact. The application of PGPB, which facilitates RKNs’ control and increases soil fertility, plant growth, and crop safety, is poised to drive sustainable agriculture. However, the use of PGPB as an RKN control strategy requires a comprehensive understanding of the host-RKN-PGPB interactions and of how soil physicochemical and biological properties modulate the interactions. The concept of the holobiont indicates that plants have fostered a symbiotic relationship with specific microorganisms that play a role in their fitness, and that the microbial moiety of a holobiont can experience alterations in response to environmental stress (Bordenstein and Theis, 2015). Soil microbiota can also protect RKN in soil by outcompeting nematode antagonists for attachment sites on nematode surface, reducing nematode recognition, or by producing compounds that are toxic to nematode antagonists (Topalović and Vestergård, 2021; Topalović et al., 2023). So far, there are very limited studies to understand the role of RKN protective soil microbiota, soil edaphic factors and different agricultural practices in modulating the tripartite interactions. Hence, unraveling the tripartite interactions and understanding their relationship with soil biotic and abiotic factors may provide us with more knowledge on how to enhance PGPB efficiency in controlling RKN in agroecosystems. This knowledge may pave the way for the development of novel PGPB strains capable of competing and establishing themselves in soil ecosystems. It may also aid in selecting appropriate APs that increase PGPB efficiency. Moreover, the incorporation of PGPB into integrated RKN management strategies, particularly through APs such as organic amendments, cover cropping, and crop rotations, can improve soil physicochemical and biological properties. This, in turn, positively influences tripartite interactions, leading to more effective RKN control. However, several pressing questions remain to be addressed. For instance, how do we get deeper insight into the tripartite interactions to weaponize it for sustainable RKN management? How to find the most effective RKN-PGPB species combination that enhances host fitness? How does PGPB and RKN-protective microbiota competition influence the microbial composition in rhizosphere? What are the mechanisms RKN use to recruit protective soil microbiota in soil? What specific component of root exudates are involved in RKN and protective microbiota interactions? What abiotic factors favor RKN-protective microbes? Is RKN protective microbiota directly involved in infection and feeding site establishment? Which APs may help to enhance the abundance and activities of indigenous PGPB, and their communication through volatiles? Answers for these kinds of questions will lead to effective integration of PGPB in sustainable RKN control and ecologically sound agroecosystems.

AH: Conceptualization, Writing – original draft. MK: Conceptualization, Writing – review & editing. CK: Conceptualization, Writing – review & editing. ZH: Conceptualization, Supervision, Writing – review & editing.