The interplay of direct and mycorrhizal pathways for plants to efficiently acquire phosphorus from soil

Abstract

To efficiently obtain P from soil, most terrestrial plants form symbiosis with arbuscular mycorrhizal (AM) fungi and thus have two P uptake pathways, i.e., the direct pathway (DP) via roots, particularly root hairs, and the mycorrhizal pathway (MP) via AM fungal hyphae. AM fungi form an extraradical hyphal network to expand their contact area with soil and release carbon-rich compounds, which provide a high-energy habitat for soil bacteria. The bacteria affected by AM fungi support P nutrition of AM fungi by secreting extracellular phosphatases. During the P acquisition process, both DP and MP function and require C fixed by plant photosynthesis to maintain P transport. Plants make trade-offs between DP and MP based on C inputs and P benefits. This review first systematically explores the potential trade-offs between plant C inputs and P gains of DP and MP as well as the factors that influence such trade-offs. Then the response of AM fungi to soil nutrient heterogeneity and the mechanisms by which AM fungi select bacteria to mineralize organic P and increase the P contribution of MP were analyzed. Future studies need to apply emerging methods and technologies to accurately quantify the contribution of DP and MP to plant P absorption under different conditions and provide the theoretical basis for optimizing sustainable agricultural production systems.

Graphical abstract

Keywords

Arbuscular mycorrhizal fungi / direct pathway / mycorrhizal pathway / trade-offs / organic phosphorus-mineralizing bacteria

Highlight

	● Plants make potential trade-off between direct and mycorrhizal pathways based on C input and P gain.
	● AM fungi sense soil P heterogeneity and release exudates that select for organic P-mineralizing bacteria.
	● AM fungi and soil bacteria develop a C–P mutualistic exchange in organic P patches.

1 Introduction

Phosphorus is one of the essential nutrients for plants. To meet the growth and development requirement of plants and maintain high yield of crops, large amounts of P fertilizers are applied to the soil annually^[1]. However, most of the applied P becomes unavailable to plants by being converted into non-soluble complexes by soil minerals such as calcium, magnesium, iron and aluminum and through immobilization into organic P forms strongly limiting seasonal P fertilizer use efficiency^[2]. It is estimated that the P surplus of global farmland in 2021 was about 8.27 Mt, accumulating mainly as organic P and non-soluble P, which cannot be directly absorbed and used by plants, posing a potential threat to sustainable crop production. This accumulation of P in soils has been termed legacy P and tends to be the norm in systems where P fertilizer is applied. Therefore, there is a conundrum around how to produce more food with less P fertilizer inputs, utilizing some of the legacy P, while protecting the environment and improving livelihoods of farmers.

To efficiently acquire P from soil, most plants have evolved different strategies. They can absorb P directly from soil via root epidermal cells and root hairs, named the direct pathway (DP). In addition, more than two thirds of terrestrial plants form symbiosis with arbuscular mycorrhizal (AM) fungi, which acquire P beyond the rhizosphere by producing an extensive network of extraradical hyphae and accessing soil pores that are inaccessible to roots. This pathway is called the mycorrhizal pathway (MP) (Fig.1)^[3]. In addition, the extraradical hyphae of AM fungi have strong growth and unlimited branching capabilities that can extend quickly in soil. They release carbon-rich compounds (e.g., carbohydrates, amino acids and carboxylates) into soil, changing the physical, chemical and biological properties of the thin layer of soil adjacent to extraradical hyphae and forming a unique hyphosphere^[4]. A large number of bacteria colonize in the hyphosphere, and they generally have the functions of mineralizing organic P. These bacteria functionally complement AM fungi to compensate for their limited saprophytic capabilities, which has the potential to make a great contribution to the availability of soil P^[5].

For mycorrhizal plants, both DP and MP are effective pathways to obtain P from soil. These two pathways interact with each other and both require the consumption of photosynthetically fixed C to maintain nutrient transport. For DP, plants allocate C into their own roots for metabolism and thereby change root morphology to facilitate P absorption^[6]. Roots also produce phosphatases and carboxylates that are released into the rhizosphere, accelerating the mineralization of organic P and the solubilization of non-soluble P, resulting in nutrient depletion in the rhizosphere^[7,^8]. In contrast, for MP, plants allocate C to their symbiotic partner AM fungi in the form of fatty acids and sugars and obtain P via extraradical hyphae far away from the roots^[9,^10]. Both roots and hyphae can release exudates to recruit soil bacteria to colonize in the rhizosphere and hyphosphere, which increase the availability of soil P and accelerate the turnover of nutrients^[4]. Plants need to efficiently allocate limited C sources in different pathways based on C input costs (investment) and P resource benefits (return on investment)^[11]. In this review, we first explore the potential trade-offs between plant C allocation and P acquisition in DP and MP as well as the effects of biotic and abiotic factors on such potential trade-offs. Secondly, we analyze the mechanisms of AM fungi selecting bacteria that mineralize soil P and improve plant P use efficiency via MP. Finally, we discuss emerging methods and technologies for studying the DP and MP to improve the availability of soil P and provide possible directions for future research efforts.

2 Plant carbon input and phosphorus gain between the direct pathway and mycorrhizal pathway

The allocation of C by plants to roots and AM fungi drives biogeochemical cycling of soil nutrients, while also satisfying their P needs. The contribution of roots and AM fungi to plant P uptake is often positively correlated with the allocation of C in these two pathways. If AM fungi contribute more P to plants, the more C they tend to obtain. However, this process is controlled by multiple factors and is difficult to accurately estimate quantitatively.

2.1 Methods to evaluate the contribution of direct pathway and mycorrhizal pathway for plants to acquire phosphorus

Mycorrhizal symbiosis has been considered a model system for comparing P acquisition by plants via different pathways. Previous studies have evaluated the contribution of DP and MP to plant growth and P uptake by calculating the mycorrhizal growth responsiveness and mycorrhizal P responsiveness, which use shoot dry weight and shoot P content of mycorrhizal and non-mycorrhizal plants to infer the difference^[12]. This method can intuitively reflect the relative contributions of different AM fungi to host plant growth and P absorption, but cannot be used in the absence of positive responses and requires DP and MP to be mutually independent and not interfere with each other. Subsequently, the preference for plant P acquisition in the DP and MP has been further revealed by the development of integrated compartments and ³³P stable isotope labeling systems^[13]. Using this method, the MP was found to contribute 70% of P for plants in the symbiosis between Funneliformis caledonius and Solanum lycopersicum, and in the symbiosis between F. caledonius and Medicago truncatula, the plants predominantly rely on the MP to obtain P from soil^[13,^14], indicating that MP can replace DP to meet plant demand for P to a certain extent. Recently, the expression of genes encoding P transporters in DP and MP were used to characterize the relative contribution of different pathways to plant P uptake^[15,^16]. The gene ZmPHT1;6 was expressed a thousand-fold after colonized by AM fungi, which are responsible for the transport of P released by AM fungi. However, the genes ZmPHT1;1, ZmPHT1;3, and ZmPHT1;4, which are used by roots to absorb P from soil, were barely expressed^[15]. However, gene expression and function are not always in direct correspondence due to the occurrence of post-transcriptional and post-translational events. In the future, it will be necessary to comprehensively consider the expression of P transporter genes and the morphological and physiologic characteristics of these two pathways and calculate multiple indices such as the preference index of P uptake, P-transporter-based and P-efficiency-based preferential index, C investment index in different contexts to maximize the quantification of the contributions of DP and MP to plant P absorption.

2.2 The effects of biotic and abiotic factors on plant carbon allocation and phosphorus acquisition in the mycorrhizal pathway

The contribution of DP and MP to plant P absorption can affect the allocation of plant C to roots and AM fungi, which is regulated by multiple factors. The availability of nutrient (especially P) in soils can directly regulate the allocation of plant C to AM fungi^[17]. The photosynthesis of plants is inhibited in P-deficient soil and plants actively allocate C to roots to meet their own survival and growth requirements. When the P needs of plants are met by roots in P-rich soil, C allocation to AM fungi is reduced^[18]. When the availability of soil P supply is maintained within a certain range (e.g., 8–15 mg·kg^–1 for maize), plants will allocate more C to AM fungi and MP contribution to plant P uptake reaches a maximum of about 60%^[15,^16]. In addition, the application of different P forms (e.g., dicalcium phosphate and ammonium polyphosphate) can directly affect P availability in soil, thereby regulating the allocation of plant C to AM fungi and reducing the colonization of AM fungi in roots and the hyphal length density in soil^[19]. In fact, the colonization by AM fungi is not invariably beneficial to plant growth, and some studies show that AM fungi colonization cause a negative impact on host plant growth^[20,^21]. If plant photosynthetic C consumption exceeds the growth benefit gained from the increased P uptake, the growth inhibition occurs because P uptake by mycorrhizal plants via DP and MP is not entirely additive^[22]. For many plants, the mycorrhizal colonization causes a reduction in the contribution of DP to P uptake, which requires MP to maximize its effect^[3]. However, plant growth inhibition is generally attributed to cheating behavior by AM fungi. For example, the symbiosis of AM fungi with different plants can obtain larger C gains with smaller P contributions^[23], which may be due to the different characteristics of the mycorrhizal symbiosis (e.g., plant sink intensity, resource exchange surplus and environmental conditions)^[24]. The above evidence suggests the potential trade-offs between DP and MP.

In both natural and agricultural systems, AM fungal species simultaneously colonize several different plants, and a plant species is also simultaneously colonized by several different species of AM fungi^[25,^26]. These AM fungi vary in their ability to provide P to their host plants, and plants can regulate C allocation to more beneficial AM fungi than non-beneficial AM fungi^[11,^27]. This prioritization can overcome the costs of reciprocity and maximize C utilization while stabilizing mutually beneficial interactions. Using ¹⁴CO₂ stable isotope labeling^[11] explored the distribution of plant C when two different AM fungi (Entrophospora claroidea and Dentiscutata erythropus) simultaneously colonize onion Allium vineale. D. erythropus contributed more to A. vineale growth and development, and A. vineale allocated more C to D. erythropus to obtain more resources. Recently, two insightful studies demonstrated that host plants and its P status can influence the establishment of mycorrhizal symbiosis and P transfer, which is mainly regulated by the conserved P-sensing pathway, centered on phosphate starvation response (PHR) transcription factors^[28,^29]. In rice, the transcriptional regulatory network map of mycorrhizal symbiosis consists of 266 transcription factors and promoters of 47 mycorrhiza-related genes that control P uptake by the DP and MP at different P levels^[29]. Low P levels induced PHR to activate genes that are involved in several steps of AM fungi development from initiation of root colonization to its functioning in nutrient exchange. High P levels strongly inhibit the movement of PHR to the nucleus and/or its binding to promoters, impairing root colonization and the contribution of MP to plant P uptake and reducing C allocation^[28].

The C and P exchange is not just dominated by the plant, AM fungi can also determine the P supply to the plant^[27]. Recently this understanding has deepened as a consequence of the development of a method using labeling with fluorescent quantum-dot nanoparticles of different colors, which allows visualization of the P redistribution process within the hyphal network. Using this method, AM fungi were exposed to the environments with high resource heterogeneity (i.e., P availability) resulting in increased P transfer. This is due to the ability of AM fungi to translocate P from the P-rich to P-poor patches to exchange resource with plants for larger C returns^[30]. AM fungi can control P transfer in the trade with plants when P availability in the hyphal network is rapidly increased or decreased. If a mycorrhizal network was exposed to a P surge, AM fungi would store the surplus P, rather than immediately trading it, until plant demand for P increases again, thereby increasing the value of P. If P availability then declines, AM fungi can reallocate P in the mycorrhizal network, transferring P that was closer to roots for the stable trade returns with the P-starved plants^[31]. Since the mycorrhizal network can connect to different plants within its growing area, it is critical that this trade preferably occurred with the host plants which shows the higher P demand^[32]. At the genetic level, the SPX domain-containing proteins constitute a regulatory network for AM fungi to deliver P to plants, mainly composed of P signaling and transport proteins, polyphosphate (poly-P) synthesis-associated proteins and scavenging P protein^[33]. The transcription factor Pho4 and its cofactor Pho2 jointly regulate P uptake and homeostasis of AM fungi during P starvation to maintain arbuscule development by activating downstream genes of conserved phosphate (PHO) signaling pathway^[34]. The market economic theory has been raised to explain the mechanisms of C and P exchange between plants and AM fungi^[27]. Resource heterogeneity is a common feature of ecosystems, and trading partnerships (e.g., mutualistic symbiosis) between different species can help individuals of a species cope with the resource inequality and improve their adaptability in the ecosystem.

3 Bacteria in the hyphosphere facilitate phosphorus acquisition by arbuscular mycorrhizal fungi

The intraradical hyphae of AM fungi penetrate the plant cortical cells forming dendriform arbuscule structures and delimit a narrow space called the periarbuscular space between the two membranes at the symbiotic interface for nutrient exchange with plants; the extraradical hyphae of AM fungi grow into soil micropores away from the roots, interacting closely with hyphosphere bacteria and exchanging nutrients^[4,^35]. The contribution of MP to plant P uptake is closely related to the nuanced communication of these two distant interfaces via the hyphae of AM fungi and bacteria dwelling in the hyphosphere can reinforce C and P exchange between plants and AM fungi in the periarbuscular space.

3.1 Arbuscular mycorrhizal fungi respond to soil nutrient heterogeneity

Spatial heterogeneity in nutrient availability is a common phenomenon in terrestrial ecosystems, and mycorrhizal plants have explored growth strategies to adapt to such heterogeneity. They can alter C allocation in heterogeneous soil, with more C used for root proliferation in patches of high nutrient availability^[36]. Similarly, extraradical hyphae of AM fungi are also able to respond to soil nutrient heterogeneity. As early as half a century ago, it was found that “endophytic mycorrhizal” hyphae can grow into leaf litter and it was speculated that the fungi absorbed and transferred litter-bound mineral nutrients to host plants^[37]. Decades later, stable isotope labeling experiments have provided definitive evidence that AM fungi can promote the decomposition of complex organic matter (grass leaves) and N acquisition in soil, and up to a third of N is captured by AM fungi and transferred to host plants^[36,^38].

Recently, with the rapid development of omics technology, only a small number of genes encoding carbohydrate-degrading enzymes were found in the published genomes of AM fungi^[39,^40], meaning they appear incapable of producing the lytic enzymes necessary to cleave organic molecules. Therefore, AM fungi alone are unlikely to acquire organically combined nutrients. Evidence suggests that AM fungi cannot mobilize and acquire organically bound nutrients in the absence of other soil microbes. However, in the presence of other soil microbes, AM fungi can accelerate the degradation of complex organic materials^[41,^42]. In other words, AM fungi do not function in isolation and the degradation of organic materials by AM fungi is mediated by other organisms.

3.2 Arbuscular mycorrhizal fungi recruit bacteria to mineralize soil organic phosphorus in the heterogeneous soil

Soil bacteria, as decomposers in the ecosystem, significantly influence global C and nutrient cycling as well as overall ecosystem function. A single gram of surface soil contains more than 10⁹ bacterial cells^[43]. These bacteria typically remain a viable but non-active/dormant state thus slowing metabolism without easily available C inputs^[44], which weakens their ability to participate in the biogeochemical processes of many elements. AM fungi use plant-derived C for metabolism and release C sources into soil in the form of hyphal exudates, which can promote the growth of bacteria and stimulate the metabolic activity of those bacteria. The determination of hyphal exudates is usually done in the sterile bi-compartmented Petri dishes, which is the most reliable system to produce large quantities of hyphae on a gel medium free of any undesired contaminant^[45]. One compartment (both roots and AM fungal hyphae, solid) is used for culture of hairy roots that are symbiotic with AM fungi, and hyphal exudates are collected on the other compartment (only AM fungal hyphae, liquid) followed by composition analysis^[46]. Hyphal exudates are mainly found to include five categories of compounds, namely sugars, amino acids, carboxylates and nucleic acids as well as proteins and peptides^[4], all of which can be used as easily available C and energy sources for bacteria. By co-culturing collected hyphal exudates with extracted soil bacterial communities, Toljander et al.^[47] obtained the first evidence that hyphal exudates of AM fungi can directly influence soil bacterial community composition. Several Gammaproteobacteria, including a taxon within the Enterobacteriaceae, increased in frequency in the presence of hyphal exudates. However, AM fungi do not benefit all bacteria. AM fungus Glomus hoi was found to actively recruit taxa from Firmicutes, while taxa from the Actinobacteria and Comamonadaceae were repelled^[48], which may be due to the bacterial preference for specific components of hyphal exudates.

Hyphal exudates of AM fungi actively facilitate soil bacteria to colonize in the hyphosphere, largely compensating for their limited saprophytic ability. Many studies have shown that the bacteria (i.e., P-releasing bacteria) positively influenced by AM fungi typically have phoD and/or gcd genes encoding alkaline phosphatase and gluconic acid in their genome, which can accelerate the mineralization and solubilization of soil organic P and non-soluble inorganic P^[49,^50]. A typical example is the exchange of C and P between AM fungus Rhizophagus irregularis and organic P-mineralizing bacterium Rahnella aquatilis to improve the availability of P for AM fungi. Each gram of R. irregularis hyphae (dry weight) released about 30 mg C in 4 weeks, which can be taken up by R. aquatilis^[51]. At the transcriptional level, hyphal exudates significantly induced the expression of key genes involved in the tricarboxylic acid cycle as well as phosphatase genes, greatly stimulating R. aquatilis growth and enhancing the ability of R. aquatilis to mineralize organic P^[52,^53]. In addition, R. aquatilis has been shown to swim along R. irregularis hyphae in a water film, nourished by the hyphal exudates on its way toward an organic P patch, where it extends the capability of R. irregularis to efficiently utilize this otherwise inaccessible P resource^[54]. Recently, two pioneering studies have shown the existence of a taxonomically conserved core microbiome in the hyphosphere, which does not change dramatically with the species of AM fungi and some external environmental factors^[55,^56]. The study results consistently showed that the core members were co-enriched in the hyphosphere, which dominated by Alphaproteobacteria and Gammaproteobacteria and highlighted the dominance of Myxococcales, Betaproteobacteriales, Fibrobacterales, Cytophagales and Chloroflexales^[5,^56]. Importantly, the relative abundance of hyphosphere core microbiome members was significantly positively correlated with soil phosphatase activity, contributing to soil P turnover and nutrient availability.

3.3 Hyphosphere interactions promote carbon and phosphorus exchange between plants and arbuscular mycorrhizal fungi

In plants, β-monoacylglycerols (β-MAGs) is synthesized from acetyl-CoA via the catalysis of multiple fatty acid synthases (e.g., FatM and RAM2), which is regulated by the master transcriptional regulatory factors WRI5a and RAM1^[57,^58]. β-MAGs can enter the periarbuscular space via the fatty acid transporters STR/STR2 located on the periarbuscular membrane and then are absorbed and metabolized by AM fungi^[59]. Phosphate is first taken up by the extraradical hyphae of AM fungi via high-affinity P transporters belonging to the Phosphate Transporter 1 family and moves to the intraradical hyphae via poly-P polymerized by the vacuolar transporter chaperone complex^[60]. In the intraradical hyphae, poly-P is hydrolyzed to P and enters the periarbuscular space via two different P transporters (PHO91 on the vacuole membrane and PT7 on the perifungal membrane)^[61]. Finally, P is acquired by plants via another P transporter (e.g., MtPT4 from M. truncatula) located on the periarbuscular membrane^[62]. A study focusing on the transcriptional level found that R. aquatilis dwelling in the hyphosphere facilitated C and P exchange between M. truncatula and R. irregularis as well as supported the formation and development of mycorrhizal symbiosis. The expression of genes involved in fatty acid synthesis (FatM and RAM2), transport (STR) and regulation (RAM1 and WRI5a) in M. truncatula and genes involved in P transporters (RiPHO84, RiPHO91, and RiVTC4) in R. irregularis are significantly increased in the presence of R. aquatilis, which ultimately promoted M. truncatula and R. irregularis growth as well as M. truncatula P absorption efficiency^[63]. The evidence clearly shows that mycorrhizae and mycorrhizae-associated bacteria increase plant P use efficiency. This fundamental interaction may provide promise for sustainable agriculture and their successful application may improve soil P status and reduce the dependence of crop on P fertilizers. Together plant and AM fungi as a holobiont have an evolutionary history of nearly 450 million years and this holobiont must also include the bacteria tightly related to AM fungal hyphae in the future.

4 Conclusions and future prospects

Plants absorb P from soil via DP and MP, and regulate both pathways through the distribution of carbohydrates. AM fungi serve as reliable symbiotic partners of plants, profoundly affecting soil P turnover and plant P absorption in terrestrial ecosystems, while bacteria colonizing in the hyphosphere can accelerate this process. The mechanism of MP for plants to effectively acquire soil P can provide the theoretical basis for the application of P fertilizers and the development of new fertilizers. However, the contribution of DP and MP for plant P absorption needs to be accurately quantified under different conditions such as soil P availability and P resource heterogeneity and the critical and active hyphosphere interactions still requires further research. The following are some research questions that we consider to be the most pressing, but also recognize additional lines of inquiry could validly be formulated.

(1) What is the mechanism of mycorrhizal plants allocating C within their roots and mycorrhizae? How to accurately distinguish the contribution of DP and MP to plant nutrient acquisition?

(2) How to maximize the effect of mycorrhizae on plant P absorption while reducing P fertilizer application in the field?

(3) How do plants precisely control C input and P gain between DP and MP? Is there a priority between the two pathways?

(4) How soil bacteria accurately sense AM fungal signals? Are there other regulatory mechanisms regulating the delicate communication between AM fungi and bacteria that promote soil P availability?

It should be possible to comprehensively answer these questions with a wide range of interdisciplinary collaboration and the application of emerging technologies. For example, botanists, ecologists and statisticians can quantitatively estimate the C flow from plants to AM fungi as well as the C flow from AM fungi to bacteria using data set analysis. Quantum-dot technology visualizes the movement of P through hyphae and even soil to analyze the strategies of interaction between plants and AM fungi focusing on C and P exchange. High throughput stable isotope probing (HT-SIP) and nanoscale secondary ion mass spectrometry (NanoSIMS) imaging are helpful to improve the understanding of plant C allocation within hyphae and even elucidating the mechanisms of how the hyphosphere bacteria assist AM fungi in mineralizing organic P. Combining multi-omics (e.g., genome, transcriptome and metabolome) approaches can further elucidate potential signaling substances in hyphal exudates in regulating the hyphosphere microbiome and help explore the functions of the hyphosphere microbiome. All of these provide both research opportunities and a theoretical basis for efficient soil P utilization.

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