Harnessing the Potential of Symbiotic Associations of Plants in Phosphate-Deficient Soil for Sustainable Agriculture

Abstract

Many plants associate with arbuscular mycorrhizal (AM) fungi for nutrient acquisition, and most legumes also associate with nitrogen-fixing rhizobial bacteria for nitrogen acquisition. The association of plants with AM fungi and rhizobia depends on the perception of lipo-chitooligosaccharides (LCOs) produced by these micro-symbionts. Recent studies reveal that cereals can perceive LCOs better in soil deprived of phosphate (Pi) and nitrogen to activate symbiosis signaling and form efficient AM symbiosis. Nevertheless, the Pi deficiency in the soil hinders the symbiotic association of legumes with rhizobia, ultimately reducing nitrogen fixation. Here, we discuss a mechanistic overview of the factors regulating root nodule symbiosis under Pi-deficient conditions and further emphasize the possible ways to overcome this hurdle. Ignoring the low Pi problem not only can compromise the functionality of the nitrogen cycle by nitrogen fixation through legumes but can also put food security at risk globally. This review aims to bring the scientific community’s attention toward the detrimental response of legumes toward Pi-deficient soil for the formation of root nodule symbiosis and hence reduced nitrogen fixation. In this review, we have highlighted the recent studies that have advanced our understanding of these critical areas and discussed some future directions. Furthermore, this review highlights the importance of communicating science with farmers and the agriculture community to fully harness the potential of the symbiotic association of plants in nutrient-deficient soil for sustainable agriculture.

Introduction

Increasing global food production for the ever-growing human population relies heavily on the continuous use of synthetic fertilizers, but overusing them is also harmful to soil and water bodies. Fertilizers are nonrenewable because their phosphorus component is exclusively mined as rock phosphate (Pi). Peak phosphorus is predicted to be reached globally as soon as 2033 (Brown 2022). This implies that food security will be compromised because of the lack of fertilizers. It is, therefore, imperative to design strategies to provide nitrogen and phosphorus, two essential macronutrients for optimal plant growth and yield, to crop plants with little or no environmental damage.

Land plants have evolved different strategies to cope with nutrient deficiency. One of these strategies implies associations with soil microorganisms. Most extant plants engage in symbiosis with arbuscular mycorrhizal (AM) fungi. Through this symbiosis, plants obtain essential mineral nutrients required for optimal growth and development, phosphorus being the most relevant (Chen et al. 2018). Symbiosis with AM fungi provides additional benefits to plants, including water uptake, nutrient homeostasis and protection against different biotic and abiotic stresses (Chen et al. 2018, Kakouridis et al. 2022). Unlike other land plants (i.e. cereals), legumes establish symbiosis with AM fungi and nitrogen-fixing bacteria collectively known as rhizobia (Oldroyd et al. 2011). Legumes host rhizobia inside cells of specialized root organs called nodules, which provides a favorable environment for nitrogen fixation (Oldroyd et al. 2011). Through this symbiosis, legumes obtain fixed nitrogen (e.g. ammonium), which allows them to grow in nitrogen-deficient soil with little to no synthetic fertilizers (Zahran 1999). In addition to this benefit, rhizobia also provide tolerance against water scarcity to the legume host (Álvarez-Aragon et al. 2023). Furthermore, few soil microorganisms can solubilize and make different mineral nutrients available to the plant (Jacoby et al. 2017). Others release numerous chemical compounds that promote plant growth and protect plants from diverse biotic and abiotic factors (Koza et al. 2022). Hence, root–microbe interactions are a climate-smart alternative to reducing our agricultural reliance on synthetic fertilizers. The use of these plant–microbe interactions under agricultural conditions requires a thorough understanding of the molecular mechanisms underlying the interaction between host plants and their microbial partners.

The symbiotic interaction of legumes with rhizobia provides fixed nitrogen to the legume for its metabolic needs and incorporates atmospheric nitrogen into the food chain. Indeed, 60 million metric tons of fixed nitrogen are produced by root nodule symbiosis worldwide (Smil 1999). This symbiosis is affected by different abiotic factors, including the availability of mineral nutrients in the soil (Hernandez et al. 2009, Isidra-Arellano et al. 2018). For example, the low availability of Pi, a key component required for the biosynthesis and activity of nitrogenase enzyme, significantly reduces root nodule symbiosis (Hernández et al. 2009, Isidra‐Arellano et al. 2020). Pi deficiency negatively affects nodule formation and nitrogen fixation activity (Hernández et al. 2009, Isidra-Arellano et al. 2018, 2020). Since Pi deficiency is a common abiotic factor in most arable soils and root nodule symbiosis is essential to feed the food chain with reduced nitrogen, it is imperative to understand the genetic mechanisms underlying the establishment of the root nodule symbiosis under low Pi conditions. With this knowledge, we will be better positioned to leverage the ecological benefits of root nodule symbiosis. Here, we review and discuss current knowledge in the communication between plants and AM fungi that can be harnessed to improve root nodule symbiosis under Pi-limiting conditions. This review also aims to bring the scientific community’s attention toward the detrimental response of legumes to Pi-deficient soil for the formation of root nodule symbiosis and hence reduced nitrogen fixation. Finally, this review aims to encourage the interaction and communication between the scientific community, farmers and the agriculture community to fully harness the potential of the symbiotic association of plants in nutrient-deficient soil for sustainable agriculture.

Nitrogen and Phosphorus: Two Essential Nutrients for Plants

Nitrogen and phosphorus are two elements required for the biosynthesis of numerous biomolecules, including proteins, nucleic acids and chlorophylls. These elements are also essential for optimal plant growth and development. Although nitrogen is abundant in the atmosphere, its reduced forms (i.e. ammonium) and nitrate, an oxidized form of nitrogen that plants exclusively take up, are scarce in the soil (Xu et al. 2012). Similarly, phosphorus is an abundant element in the soil; however, land plants take this element from the soil exclusively as Pi (Broughton et al. 2003). Furthermore, Pi rapidly interacts with cations forming complexes, making them impossible to uptake (Vance et al. 2003). Land plants overcome Pi deficiency by establishing symbiosis with AM fungi (Humphreys et al. 2010). Legumes overcome nitrogen deficiency through symbiosis with rhizobia (Vance 2001, Venkateshwaran et al. 2013). Host plants must feed the microbe symbiont with plant-derived carbon sources (i.e. photosynthates or lipids) for these nutritional benefits (Udvardi and Day 1997, Bago et al. 2000, Jiang et al. 2017, Luginbuehl et al. 2017). Hence, nutrient exchange between symbiotic partners, such as AM fungi and plants (including legumes) or legume and rhizobia, is bidirectional, meaning that both partners benefit from the relationship.

Maintaining root endosymbiosis implies a higher cost to the host plant. To avoid a metabolic and plant growth imbalance, plants tightly regulate the establishment of symbiosis with AM fungi or rhizobia (Udvardi and Day 1997, Bago et al. 2000). Legumes regulate the number of nodules per root system by activating the autoregulation of nodulation (AON) pathway (reviewed in Ferguson et al. 2019). Root-derived CLAVATA/ENDOSPERM SURROUNDING REGION (ESR)–related (CLE) peptides and leucine-rich repeat receptor-like kinases (LRR-RLK) highly similar to CLAVATA1 from Arabidopsis thaliana are critical genetic components of the AON pathway that are required to limit nodule formation (reviewed in Ferguson et al. 2019). Similarly, land plants regulate the number of interactions with AM fungi by activating the so-called autoregulation of mycorrhization (AOM) pathway (reviewed in Wang et al. 2018). Interestingly, nodulation can systemically suppress AM fungi symbiosis and vice versa, suggesting a clear overlap between the AON and AOM pathways (Catford et al. 2003). Similar results were observed in studies using a dual inoculation system in which rhizobia and AM fungi were applied to the same root system (Sakamoto et al. 2013). All these data indicate that host plants tightly control the symbiotic interactions. Furthermore, these data also inform that AON and AOM pathways share genetic components that legumes leverage to restrict simultaneous symbiosis with rhizobia and AM fungi, likely to avoid metabolic unbalance and, thereby, penalties in plant growth and development.

When Pi or nitrate are available at optimal concentrations in the soil, plants do not interact with AM fungi or rhizobia, respectively (Wang et al. 2018, Ferguson et al. 2019). Legumes use some of the AON pathway’s genetic components to inhibit rhizobia symbiosis under optimal nitrogen conditions (Wang et al. 2018). Whether the AOM pathway plays any role in inhibiting the symbiosis with AM fungi symbiosis under optimal Pi conditions remains unclear. Hence, nitrogen and Pi are the most critical evolutionary factors determining whether plants enter a symbiosis with rhizobia or AM fungi, respectively. However, other nutritional factors may likely be determinants in the modulation of these symbioses, as we discuss for the legume–rhizobia symbiosis in the following sections.

Pi in the Soil and Plant Cells Modulates Root Endosymbioses

Phosphorus is essential for protein phosphorylation, a critical step in decoding signals from both internal and external stimuli. Therefore, Pi deficiency affects signal transduction, compromising plant environmental adaptation. Because of this, plants must ensure the appropriate concentration and maintain Pi homeostasis. Land plants rely on the Pi starvation response (PSR) system (Valdés-López and Hernández 2008, Isidra-Arellano et al. 2021). The PSR is tightly controlled by phosphate starvation response (PHR), a class of Myb coiled-coil (MYB-CC) transcription factor (Rubio et al. 2001). The PHR/PSR module regulates the Pi uptake, translocation and homeostasis (Rubio et al. 2001, Isidra-Arellano et al. 2021). Land plants also deal with Pi deficiency by modifying the morphology and architecture of their roots, increasing nutrient availability in the soil through organic acid exudation and recycling nutrients from older tissues (López-Bucio et al. 2003, Péret et al. 2014). Legumes have evolved specialized responses to cope with Pi deficiency while interacting with rhizobia (Hernández et al. 2009, Lu et al. 2020). For instance, legumes regulate the activity of Pi transporters and translocators to reallocate Pi from other organs to the nodules (Hernández et al. 2009, Cabeza et al. 2014, Lu et al. 2020). This strategy ensures the functionality of the symbiotic nitrogen fixation; however, the plant development and fitness are severely affected (Hernández et al. 2009, Cabeza et al. 2014).

In addition to these responses, most land plants can cope with Pi deficiency through symbiosis with AM fungi (Vigneron et al. 2018, Shi et al. 2022). Some non-AM fungi host plants can associate with other soil microbes. For instance, A. thaliana interacts symbiotically with the endophytic fungi Colletotrichum tofieldiae to improve Pi uptake (Hiruma et al. 2016). In both cases, low Pi levels in plant cells and soil promote symbiosis with AM fungi or C. tofilediae, while optimal Pi levels inhibit these symbioses (Breuillin et al. 2010, Hiruma et al. 2016, Nouri et al. 2021). Similarly, nitrogen starvation promotes rhizobia symbiosis in legumes (Roy et al. 2020). The level of Pi in soil and cells has opposite effects on AM and root nodule symbiosis in legumes, with low Pi promoting AM symbiosis and reducing root nodule symbiosis. The association between legumes and rhizobia for nitrogen fixation depletes Pi in both soil and cells, and the lack of this nutrient reduces nodule formation and symbiotic nitrogen fixation (Hernández et al. 2009, Isidra-Arellano et al. 2020). Indeed, low Pi levels reduce the expression of genes participating in the rhizobial infection process but increase those involved in the biosynthesis of ethylene and jasmonic acid, which are negative regulators of this symbiosis (Ferguson and Mathesius 2014, Isidra-Arellano et al. 2018).

Different critical genetic regulators of the AM and root nodule symbiosis have been identified over the last decades. For instance, besides controlling the plant responses to Pi deficiency in an abiotic context, the transcription factor PHR also regulates the expression of genes participating in different steps of AM symbiosis, including pre-contact signaling, root colonization and AM function (Shi et al. 2021, Das et al. 2022). PHR2 directly binds to the promoter regions of genes participating in the nutrient exchange between AM fungi and rice plants (Das et al. 2022). Further evidence indicates that PHR2 is essential in perceiving the AM fungi at the root surface (Das et al. 2022).

PHR acts as a positive regulator of the root nodule symbiosis when legumes are growing under optimum Pi conditions by ensuring the proper amount of this nutrient that rhizobia need to fix the atmospheric nitrogen (Lu et al. 2020). However, PHR inhibits root nodule formation under low Pi conditions by activating the AON pathway (Isidra-Arellano et al. 2020). The overexpression of PHR significantly reduces the number of nodules, but the nodules increase in size (Lu et al. 2020). Interestingly, nodules overexpressing PHR exhibit high nitrogen fixation under Pi-deficient conditions (Lu et al. 2020). This observation is attributable to the PHR-high-affinity Phosphate Transporter1 (PHT1) module that keeps Pi homeostasis in legume nodules (Lu et al. 2020). All this evidence indicates that plant host Pi level is a determinant factor in establishing or inhibiting root endosymbiosis. Furthermore, these data indicate that the transcription factor PHR is a critical genetic component in shaping root endosymbiosis according to the plant host Pi levels.

Perceiving the Microbial Call for the Establishment of Root Endosymbiosis

A bidirectional exchange of chemical signals is required to associate plants with AM fungi or rhizobia (Roy et al. 2020). Rhizobia produces lipo-chitooligosaccharides (LCOs) consisting of a polymer of four to five N-acetyl glucosamine residues (the chitin backbone) with β-(1-4) linkages modified with a long-chain fatty acyl group and various other functional groups (Dénarié et al. 1996). Most rhizobia rely on LCOs to associate with their legume host, and legumes can perceive LCOs in the range of nano and picomolar concentration (Sun et al. 2015). Substitutions on the chitinous backbone are primarily responsible for the high level of host specificity observed in the rhizobia–legume symbiosis (Dénarié et al. 1996). AM fungi also produce LCOs and short chitooligosaccharides (COs) that all together are known as mycorrhization factors (Maillet et al. 2011).

Legumes perceive the rhizobial-derived LCOs [also known as Nod factors (NFs)] through RLKs with the LysM extracellular domain for downstream signaling (Roy et al. 2020). The plasma membrane–specific receptors NF RECEPTOR 1 (LjNFR1)/LysM-RLK 3 (MtLYK3), LjNFR5/NF PERCEPTION (MtNFP), perceive the NFs in the model legumes Lotus japonicus and Medicago truncatula (Fig. 1) (Arrighi et al. 2006, Limpens et al. 2003, Madsen et al. 2003, Radutoiu et al. 2003). The epidermal NF receptor (NFRe) is another receptor that participates in the rhizobial infection process by amplifying signals in root epidermal cells in L. japonicus (Murakami et al. 2018). NF perception changes the stability and localization of LysM-RLKs at the plasma membrane by compartmentalizing the receptors into nanodomains or microdomains, which partition RLKs into functionally well-defined signaling units, which is critical for rhizobial signal perception at the plasma membrane and downstream transduction of perceived signals to the nuclear machinery (Ott 2017). NF perception by LysM receptors activates the symbiosis receptor kinase (SYMRK), which is crucial for the activation of the genetic programs required to establish the root nodule symbiosis (Roy et al. 2020) (Fig. 1).

NF perception by LysM-RLKs and associated signaling for root nodule symbiosis have been reviewed extensively (Roy et al. 2020, Singh and Verma 2023). LCOs from AM fungi are perceived similarly to NFs (Fig. 1). The perception of the AM fungi symbiotic signals by land plants also requires SYMRK along with different sets of receptors such as Chitin Elicitor Receptor Kinase 1 (CERK1), Myc Factor Receptor (MYR1), Receptor-like kinase 10 (RLK10 is an NFR5 homolog in barley) and RLK2 (a close homolog of RLK10) (Miyata et al. 2016, He et al. 2019, Li et al. 2022). Rice OsCERK1 does not bind directly to chitotetraose (CO4) and chitopentaose (CO5) although it appears to be a crucial signal for symbiotic interactions between AMF and host plants (Carotenuto et al. 2017). OsMYR1/OsLYK2/OsNFR5/OsRLK2, a member of the same clade as LjNFR5/MtNFP, is the co-receptor of OsCERK1 necessary for AM symbiosis (He et al. 2019). OsMYR1 directly binds CO4 but not NF (He et al. 2019). A significant reduction in AM fungi colonization, transcription levels of AM-symbiosis-specific marker genes and in the nuclei and perinuclear calcium concentration (hereafter referred to as Ca²⁺ spiking) were observed in the Osmyr1-1/Oslyk2-1- and rlk2/rlk10-mutant plants compared to wild-type plants inoculated with AM fungi (He et al. 2019, Li et al. 2022). In contrast to the findings by He et al. (2019), the study conducted by Miyata et al. (2016) revealed different results regarding Osmyr1 (Oslyk2/Osnfr5) null mutants generated through a homologous recombination technique. According to Miyata et al. (2016), these mutants exhibited normal AM fungi colonization, while there was a significant decrease in the expression of AM marker genes. This discrepancy in the phenotype of the same gene in rice can be attributed to the utilization of a strong inoculation system by Miyata et al. (2016), involving 5,000 spores/plant. This high spore concentration might have masked the AM phenotype in the Osmyr1 mutants. In contrast, He et al. (2019) used a lower spore concentration of 400 spores/plant, aiming to better reflect natural conditions. These findings suggest that OsMYR1 functions as a binding receptor for CO4 and that OsMYR1 and OsCERK1 are then dimerized and phosphorylated to activate the symbiotic signaling pathway (Zhang et al. 2021).

Even though different sets of RLKs are involved in the perception of microbial-derived LCOs, shared genetic elements are necessary to decode the signals derived from rhizobia and AM fungi. The key components that are shared by AM symbiosis and root nodule symbiosis downstream of LysM receptors include LjSYMRK/MtDMI2, the calcium channel known as does not make infection (DMI1/ or CASTOR/POLLUX); the calcium- and calmodulin-dependent protein kinase CCaMK/MtDMI3 and the transcription factors LjCYCLOPS/MtIPD3, Nodulation Signaling Pathway1 (NSP1) and NSP2 (Roy et al. 2020).Together these components are part of the so-called ‘common symbiosis pathway’ (Roy et al. 2020) (Fig. 1). This signaling pathway is conserved in most non-legumes and legumes, allowing them to engage in symbiosis with AM fungi (both non-legumes and legumes) or with rhizobia (legumes). Hence, the unanswered question is how plants use similar receptor complexes and shared genetic components to identify and decode microbial-derived molecules deriving into different plant responses to a particular symbiont.

Difference in the Perception of the Microbial Signal under Pi- and Nitrogen-Deficient Conditions in the Root Nodule- and AM Symbiosis

Root nodule symbiosis is significantly reduced under low Pi conditions, which may be attributed to different possibilities, namely poor perception of the rhizobial signal under this detrimental soil condition, failure in decoding of rhizobial signals perceived at the plasma membrane or a significant alteration in the assembly of transcription complex consisted of CCaMK-CYCLOPS-DELLA and NSP1/NSP2 required for nodule formation (Isidra-Arellano et al. 2018) (Fig. 2). These hypotheses are supported by the fact that Pi-deficient legumes show defects in the rhizobial-triggered root hair deformations, an essential step for successful rhizobial infection, and reduced expression of genes involved in the early stage of the root nodule symbiosis (Isidra-Arellano et al. 2018). On the contrary, a recent report suggests that AM fungi–derived LCO perception in cereals (i.e. rice, barley and maize) occurs better in nitrogen- and Pi-deficient soils, which led to a successful symbiosis with AM fungi (Li et al. 2022). Additionally, Li et al. (2022) demonstrated that LCO recognition in cereals is coordinated with AM fungi LCO production via the action of the transcription factors NSP1 and NSP2, facilitating nutrient control of AM fungi colonization. Understanding how plants perceive AM fungi–derived LCOs under low Pi conditions can thus help us develop legumes that perceive rhizobial LCOs better under low nitrogen and low Pi conditions.

AM fungi colonization is suppressed in most land plants with increased Pi concentrations (Hepper 1983). Interestingly, suppression of mycorrhization in high Pi is partially mitigated by overexpression of NSP2 in barley and the model legume M. truncatula (Li et al. 2022). A similar phenotype was also observed when PHR was overexpressed in L. japonicus (Shi et al. 2021, Das et al. 2022). These findings suggest that the Pi regulation of the AM fungi symbiosis is partially controlled by NSP2 and PHR, which regulate strigolactone production (Shi et al. 2021, Das et al. 2022). Likewise, these recent findings indicate that low nitrogen and low Pi promote the perception of LCOs and adequately activate the common symbiotic pathway for establishing AM symbiosis. However, why this nutrient condition impairs the root nodule symbiosis remains poorly understood. PHR1 plays a role in chromatin remodeling, ensuring the transcriptional activation of genes required in adapting A. thalianato low Pi conditions (Barragán-Rosillo et al. 2021). With this knowledge, it is tempting to speculate that PHR may modulate the chromatin remodeling to activate positive regulators of the symbiosis with AM fungi (Fig. 2). It is also likely that under this hypothetical scenario, the PHR-mediated chromatin remodeling may block the genes required for root nodule symbiosis. Another possibility is that PHR plays a role in activating genes involved in the AON pathway to negatively regulate the nodulation in legumes, as previously reported by Isidra-Arellano et al. (2020).

A Call for the Scientific Community to Take Action

The knowledge generated in the past 2 years on AM fungi- and root nodule symbiosis can be leveraged differently. For instance, it can be used to enhance the colonization of AM fungi under suppressive Pi conditions—a particular condition generated by the overuse of inorganic fertilizers—by genetic engineering of NSP2 and PHR that have vast effects on plant function. Another option to boost nodule symbiosis in Pi-deficient soils may be using a stage-specific nodule symbiosis promoter that can induce the expression of PHR1 and PHT1 in the early stages of nodulation. This will lead to optimal Pi uptake at this stage and help legumes establish a symbiotic relationship with rhizobia under Pi-deficient conditions. However, limiting the expression of PHR1 in the late stages of nodulation is essential to avoid penalties in the legume host growth and yield. Therefore, careful regulation of the spatiotemporal expression of PHR1 and the PHR-PHT1 module is crucial for maintaining a healthy symbiotic relationship between legumes and rhizobia and ensuring optimal plant growth and development in Pi-deficient soil.

We need to simultaneously (i) expedite our search for the rhizobial community or mixed synthetic rhizobial community better adapted to form a symbiotic association with the legumes under Pi-deficient conditions and (ii) select elite cultivars of legumes that can efficiently form nodules under Pi scarcity conditions, which may be less in number but efficient enough to fix nitrogen required for plant growth and development. Because legumes interact with both AM fungi and rhizobia, it is tempting to speculate that the negative effect of Pi deficiency on nodule formation and nitrogen fixation does not exist under natural conditions where both microbes are present in the soil. This assumption can be correct in perennial legumes, in which a beneficial effect of interacting with both AM fungi and rhizobia with the host plant has been observed (Primieri et al. 2022, Tsikou et al. 2023). However, this additive and beneficial effect is not observed in annual legumes that include most agronomic crop legumes, like soybean, alfalfa, common bean and chickpea. Furthermore, as discussed in previous sections, AM symbiosis can systemically suppress nodulation in different legumes (Catford et al. 2003). Therefore, developing elite or transgenic legumes capable of forming associations with both AM fungi and rhizobia simultaneously can be a promising approach to address the problem of the adverse effects of low Pi on the root nodule symbiosis problem. PHR regulates AM association with roots, and controlling its spatiotemporal expression is crucial. Modulating the PHR-PHT1 spatiotemporal expression and activity may help legumes establish healthy symbiotic relationships with both rhizobia and AM fungi, resulting in improved nutrient acquisition and increased resilience in Pi-limited soils. However, in addition to developing elite legume cultivars, intense research is also required to understand how AM fungi and rhizobia simultaneously interact with legumes to better harness their nutritional services.

With a better understanding of the molecular mechanisms of nitrogen and Pi interactions in cereals and legumes, we will be in a better position to use molecular-assisted breeding in conjunction with cutting-edge gene-editing technology as a future strategy to develop better legume varieties with high symbiotic nitrogen fixation capacity under Pi-deficient conditions. Tackling all these questions not only will help legumes efficiently fix nitrogen in association with rhizobia, but could also help the current research oriented to make it possible fosr cereals to associate efficiently with diazotrophs because low Pi affects different plant species, including these important crop plants. Simultaneously, improving AM fungi associations in agriculture can enhance nutrient capture efficiency, reducing environmental nutrient loss.

This is high time for the research community to be univocal in communicating the research outcome on root nodule- and AM symbiosis to agriculture stakeholders and how these plant–microbe associations get impacted by the presence or absence of nitrogen and Pi in the soil. Hence, we invite the scientific community to discuss these questions in specialized meetings, conferences and workshops that are relevant to agriculture and the association of plants with these beneficial microorganisms, share their research findings and discuss the potential benefits of AM fungi- and root nodule symbiosis for agriculture with farmers and other stakeholders. To promote the use of AM and/or root nodule symbiosis in agriculture and increase agricultural productivity and sustainability, several strategies can be used to involve farmers and the agricultural community. Plant molecular biologists can work with farmers and agricultural organizations on research projects that focus on applying AM fungi- and root nodule symbiosis in agriculture. This can aid in integrating scientific research and practical knowledge for better results. The second option is for plant molecular biologists to take part in farmer training initiatives to inform farmers about the advantages of AM fungi- and root nodule symbiosis and give them practical instruction on how to use it in agriculture. The third method involves plant molecular biologists visiting farmers and agricultural communities to show how these symbioses are used and their advantages in practical situations. This can foster greater trust and comprehension among farmers regarding the use of this symbiotic association in agriculture. One such example is Kisan Mela (Krishi Jagran), a national event in India that facilitates the exchange of knowledge and ideas between farmers and scientists. In this event, lectures, presentations and demonstrations feature various agricultural topics, including showcasing high-yielding seed varieties and new technologies developed by universities to improve farming practices. Another example is Engineering the Nitrogen Fixation Symbiosis for Africa (ENSA) project, an international collaborative effort to enhance the use of beneficial microorganisms to deliver essential nutrients for crop production, focusing on making global agriculture more sustainable and equitable (ENSA). ENSA and Kisan Mela can foster meaningful interactions between scientists and agricultural stakeholders, leading to more effective solutions that improve agricultural productivity and sustainability. The methods incorporating Pi and nitrogen into the food chain that are least harmful to the environment so far are AM fungi association and symbiotic nitrogen fixation. Ignoring the issue of low Pi and low nitrogen can jeopardize the nutrient cycle’s efficiency and threaten global food security.

Data Availability

Source data for Figs. 1 and 2 are provided in the paper. No new datasets were generated or analyzed in this study.

Funding

This work was supported by the Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica (PAPIIT-UNAM grant no. IN200523) and by UNAM Posdoctoral Program (POSDOC).

Acknowledgments

J.S. received a Postdoctoral Fellowship granted by the Dirección General de Asuntos del Personal Académico (DGAPA-UNAM). M.C.I.-A. is a Royal Society Newton International Fellow . We thank Jean-Michel Ané for constructive discussions.

Disclosures

The authors have no conflicts of interest to declare.

References