Trading on the arbuscular mycorrhiza market: from arbuscules to common mycorrhizal networks

Tansley Review: Trading on the Arbuscular Mycorrhiza Market

Summary

Arbuscular mycorrhiza (AM) symbiosis is a mutualistic relationship between Glomeromycota fungi and most land plants.
The primary benefit is the exchange of nutrients between plants and fungi.
This review outlines current concepts of nutrient exchange, focusing on phosphorus (P) and nitrogen (N) transfer to the plant and carbon (C) transfer to the fungus.
It discusses the regulation of nutrient exchanges linked to membrane dynamics and common mycorrhizal networks (CMNs).
It also explores how to integrate AM knowledge into sustainable agriculture.

I. Introduction

AM symbiosis is an ancient mutualistic relationship, dating back approximately 400 million years with the emergence of terrestrial plants.
It involves soilborne fungi (Glomeromycotina) and host plant roots.
AM symbiosis impacts $\leq$ 80% of terrestrial plants, including most cultivated species.
Process:
- AMF hyphae penetrate the root epidermis.
- They colonize cortical cells.
- They form arbuscules (fungal hyphae ensheathed in a modified cortical cell plasma membrane known as the periarbuscular membrane).
This interaction enhances plant access to soil resources, improving responses to abiotic constraints like:
- Climatic changes (Torres et al., 2018)
- Drought stress (Symanczik et al., 2018)
- Water deficit (Balestrini et al., 2018)
- Salinity (Ruiz-Lozano et al., 2012)
- Heavy metal contamination (Shi et al., 2018; Torres et al., 2018)
Mycorrhizal plants exhibit increased tolerance to pathogens due to mycorrhiza-induced resistance (Pozo & Azcon-Aguilar, 2007; Cameron et al., 2013).
Optimal management of AMF is essential for optimizing plant production with limited chemical inputs (Gianinazzi et al., 2010).

II. Nutrient Transfer Mechanisms in AM Symbiosis

1. Nutrient Transfer Mechanisms Between AMF and Host Plants

Improved mineral nutrition is a primary benefit, especially regarding P and N nutrition.
Most plants struggle with low N and P concentrations in natural environments (Elser et al., 2007).
Plants have a 'mycorrhizal phosphate uptake' (MPU) pathway in addition to direct phosphate uptake (DPU) by root epidermal cells (Fig. 1).
AMF hyphae uptake and transfer organic and inorganic N from the soil to the host plant.

Phosphorus

Improved P nutrition is the most recognized benefit.
Most soil P is bound in organic molecules or mineral surfaces, making it inaccessible to plants (Rausch & Bucher, 2002).
Plants uptake orthophosphate (Pi) from the soil solution via specific phosphate transporter proteins (DPU pathway) (Fig. 1).
Pi uptake creates a Pi-depletion zone near the root surface due to low Pi mobility in soils.
MPU pathway: AMF hyphae grow beyond the Pi depletion zone, accessing inaccessible Pi resources (Bucher, 2007).
AMF hyphae and associated microorganisms hydrolyze organic P, increasing soil organic P turnover (Fig. 1).
Inorganic P is taken up by AMF hyphae, transferred to intraradicular fungal structures, and released into the periarbuscular space in arbuscule-containing cells.
H+/Pi and putative Na+/Pi symporters are found in AMF transcripts of Rhizophagus irregularis, Funneliformis mosseae, and Rhizophagus clarus.
The mechanisms of Pi export from AMF into the apoplastic interface remain unknown (Garcia et al., 2016).
Pi transport from the rhizosphere to plant organs is mediated by P transporters (PHT) (Rausch & Bucher, 2002; Nagy et al., 2005).
The PHT family has four subfamilies (PHT1–4).
PHT1 subfamily mediates Pi uptake from the soil via DPU.
PHT1 members cluster into three subgroups; subgroup 2 is induced in AM roots (Wang et al., 2017a,b).
Phosphate transporter genes transcriptionally induced in AM roots:
- Solanum tuberosum (Rausch et al., 2001)
- Medicago truncatula (Harrison et al., 2002)
- Oryza sativa (Paszkowski et al., 2002)
- Lycopersicon esculentum (Xu et al., 2007)
- Petunia axillaris (Breuillin et al., 2010)
- Astragalus sinicus (Xie et al., 2013)
- Sorghum bicolor (Walder et al., 2015)
- Lotus japonicus (Volpe et al., 2016)
- Zea mays (Liu et al., 2018)
M. truncatula MtPT4, localized at the periarbuscular membrane, mediates Pi uptake from the periarbuscular space (Javot et al., 2007).
AM-induced PHT plant genes are suggested to have roles in:
- Arbuscule morphogenesis
- Maintaining symbiosis
- Mediating arbuscule lifespan (Breuillin-Sessoms et al., 2015)
- Pi-sensing machinery in root tips (Volpe et al., 2016)
The intensity of P flow at the arbuscule interface depends on the P supplied at the extraradical mycelium (Fiorilli et al., 2013).
It also depends on the AMF's ability to reabsorb Pi or leave it in the periarbuscular space (Balestrini et al., 2007; Walder et al., 2016).
Pi dependency is selectively different among plants and depends on the interaction between the plant and AMF species (Janos, 2007).
The PHT family are phosphate/proton symporter proteins.
Phosphate uptake requires a proton gradient across the periarbuscular membrane resulting from the activity of the plasma membrane H+-ATPase.
In AM roots, a plasma membrane H+-ATPase gene is induced (Gianinazzi-Pearson et al., 2000; Krajinski et al., 2002).
It is co-regulated with mycorrhiza-induced PHT proteins (Gaude et al., 2012).
The mycorrhiza-induced H+-ATPase was located at the periarbuscular membrane in M. truncatula and rice.
Its activity is essential for phosphate uptake from the periarbuscular space (Krajinski et al., 2014; Wang et al., 2014).

Nitrogen

Nitrogen (N) is required in significant quantities, constituting 1–5% of the plant DW.
Plant-available N is a limiting factor in ecosystems and is heterogeneously distributed in the soil (Courty et al., 2015).
Approximately one-third of root protein N could be provided by symbiotic AMF (Govindarajulu et al., 2005).
N uptake is mediated by transport systems, including inorganic N (ammonium $NH4^+$ and nitrate $NO3^−$ ) and organic N (amino acids and peptides) (Figs 1, 2).
Nitrogen ions taken up by AMF hyphae are converted into arginine and transported in this form to the host roots.
N is released into the roots without any carbon (C) links (Govindarajulu et al., 2005).
Nitrate (often the main N source in fertilized soil) is taken up via an energy-dependent process by specific transporters (Fig. 2).
These transporters belong to the NPF (NRT1/PTR family; Léran et al., 2014), NRT2, and NRT3 families (Orsel et al., 2002; Bai et al., 2013).
In plants, NPF is a large protein family, e.g., 85 members in rice, 79 in poplar, and 62 in Arabidopsis.
NPF members transport $NO_3^−$ with low affinity or di-/tripeptides (Krouk et al., 2010), and also nitrite, glucosinolates, or phytohormones (Bai et al., 2013).
In AMF, only one high-affinity transporter belonging to the NRT2 family has been described in R. irregularis (GiNT).
GiNT is expressed in all AMF tissues (spores, extra- and intraradical mycelium, arbuscules).
GiNT could play a key role at the symbiotic interface by establishing competition for $NO_3^−$ between the plant and the AMF (Tian et al., 2010; Koegel et al., 2015).
GiNT could be regulated at the plant–soil interface by the internal concentrations of $NH_4^+$ and/or glutamine (Fellbaum et al., 2012).
In roots, $NO_3^−$ assimilation depends on the presence of AMF (Gomez et al., 2009; Guether et al., 2009) and the N and P status of the two partners (Hohnjec et al., 2005; Drechsler et al., 2017).
Soil organisms often assimilate $NH4^+$ directly because it is more energy-efficient than $NO3^−$ reduction to $NH_4^+$ (Marschner, 1995).
Several plant ammonium transporters (AMTs) are upregulated during AM symbiosis (Courty et al., 2015; Garcia et al., 2016).
They are dispatched in the four AMT1/2/3/4 clades (Loqué & von Wiren, 2004) (Fig. 2).
In monocots, the AM-inducible AMT3;1 seems to be conserved among plant families (Koegel et al., 2017).
Ammonium (and sometimes $NH_3$ ) is actively transferred by AMF to the acidic periarbuscular space of arbuscule branches.
Then, the uncharged $NH_3$ is released by AM-induced AMT into the cytoplasm of arbuscule-containing cells (Kobae et al., 2010; Koegel et al., 2013, 2017).
This could reinforce the gradient of H+-dependent transport processes.
AMTs might have a sensing or signaling function, a role in the pre-penetration response, or be required for arbuscule formation and lifespan (Javot et al., 2007, 2011; Gomez et al., 2009; Breuillin-Sessoms et al., 2015).
Besides arbuscules, AMF hyphae could be involved in symbiotic N transfer; aquaporins act as low-affinity $NH_4^+$ transporters in hypha-colonized cortical cells in soybean and Medicago (Uehlein et al., 2007; Hwang et al., 2010).
AMF species vary in their abilities to uptake $NH_4^+$ and transfer N to host plants (Mader et al., 2000).
Two high-affinity AMTs (GintAMT1 (Lopez-Pedrosa et al., 2006) and GintAMT2 (Perez-Tienda et al., 2011)) and one low-affinity AMT (GintAMT3; Calabrese et al., 2016) have been identified in R. irregularis.
GintAMT1 could be involved in soil $NH4^+$ acquisition by the extraradical mycelium when $NH4^+$ is present at low concentrations (e.g., in acidic soils).
GintAMT2 could be involved in the recovery of $NH_4^+$ leakage through the fungal metabolism.
The intensity of $NH_4^+$ transfer at the symbiotic interface through GintAMT3 could be linked to access to a P source (Fig. 2).
The regulation of the three GintAMTs depends on C availability, highlighting a strong interconnection between C and N transfer during AM symbiosis (Fellbaum et al., 2012).
The NH4+ transporters are important for symbiotic nutrient exchanges independently of the N conditions (Calabrese et al., 2017).
The mechanisms involved in $NH_4^+$ transfer from the AMF into the apoplastic interface remain unknown.
$NH_4^+$ is a candidate for fungus-to-plant-cell transfer through the apoplastic space or inorganic N exported through voltage-dependent cation channels (Chalot et al., 2006).
AMF can draw N from organic forms (amino acids like glycine) and small peptides (Cliquet et al., 1997; Hodge, 2001) (Fig. 2).
An amino-acid permease (GmosAAP1) involved in transporting amino acids has been identified in F. mosseae (Jin et al., 2005; Cappellazzo et al., 2008).
Some di- and tripeptide transporter (PTR) genes are specifically induced in AM roots/arbuscule-containing cells (Casieri et al., 2013) and in R. irregularis (RiPTR2, Belmondo et al., 2014).
RiPT2 might play a role in the uptake of small peptides from the soil and the reuptake of peptides from the interfacial apoplast (Belmondo et al., 2014).

Is Plant Control of AMF Colonization Dependent Upon Inorganic Phosphate and Nitrogen Availability?

Like Pi fertilization, inorganic N fertilization (≥ 100 mg N per kg soil) reduces root colonization by AMF (Lanowska, 1966; Blanke et al., 2005).
C allocation to the fungus can be reduced under high external N concentrations (Olsson et al., 2005).
The mycorrhiza response to fertilization depends on context and availability of other nutrients.
Nitrogen addition negatively affects AMF colonization in soils with low N:P ratios but positively affects it in soils with high N:P ratios (Johnson et al., 2003, 2015).
One essential resource in limiting supply controls plant production (law of the minimum, von Liebig, 1843; van der Ploeg et al., 1999).
Relative availability of soil N and P determines whether mycorrhizal benefits outweigh their costs (Johnson et al., 2015).
N fertilization only benefits when the plant is limited by P, leading to positive effects from providing C to the roots and the AMF.
Inorganic N sources can elicit a mutualism scenario (trade-off balance model) where both plant and fungus benefit in a P-limited system (Johnson et al., 2015).
Long-term P inhibition of AM symbiosis is partially suppressed under low N conditions (Blanke et al., 2005; Nouri et al., 2014).
Premature arbuscule degeneration is relieved when plants are deprived of N, suggesting the arbuscule lifespan is partly regulated by N (Javot et al., 2011).
The recovery of AM colonization did not increase N concentrations, suggesting N starvation triggers a signal that promotes AMF colonization (Blanke et al., 2005; Nouri et al., 2014; Bucking & Kafle, 2015).
A functional periarbuscular ammonium transporter (AMT2;3) was required for the low-N suppression of premature arbuscule degeneration in pt4 mutants (Breuillin-Sessoms et al., 2015).
Pi or $NH_4^+$ transport through their symbiotic transporters delivers nutrients and initiates a signaling mechanism that promotes the maintenance of arbuscules.
Pi and nitrate exert a negative influence on AM root colonization (Nouri et al., 2014).
Other nutrients (K, Ca, Mg, sulfate, and iron) did not influence mycorrhizal development at elevated concentrations.

2. Symbiotic C Transfer to the Fungus

AMF provide greater access to soil nutrients and water (Bago et al., 2000).
The plant redirects 4–25% of its photosynthates toward mycorrhizal roots (Hobbie, 2006).
AMF are obligate biotrophic organisms because they cannot complete their life cycle without colonizing a host plant.

Sugar Transport

Sugar metabolism is key to AMF biotrophy.
AMF receive all required C from their host plants.
AMF C metabolism was once considered the main reason for the biotrophic nature of these fungi.
$^{13}C$ -NMR spectroscopy showed that R. irregularis behaves like a metabolic bipole (Pfeffer et al., 1999).
Exogenously supplied hexoses (glucose and fructose) were taken up by the fungus through intraradical hyphae, but not through extraradical ones.
Experiments using $^{14}C$ -labeled glucose in R. irregularis confirmed that the extraradical hyphae cannot take up glucose from the external medium.
Enzymatic studies revealed low activity of glycolysis enzymes (Shachar-Hill et al., 1995; Solaiman & Saito, 1997).
Neoglucogenic activity was very high.
Metabolism of extraradical hyphae is directed towards glucose anabolism, indicating that hexoses are a negligible C energy source.
Intraradical hyphae have a very different C metabolism from extraradical hyphae and act like the 'energy engine' of the organism.
However, germinating spores of R. irregularis can incorporate external glucose at very low concentrations.
This transport was inhibited by high sugar concentrations, suggesting catabolic repression of the hexose transporter(s).
The existence of hexose uptake in germinating spores was confirmed by the expression of a fungal mono-saccharide transporter (MST) (Ait Lahmidi et al., 2016).
Two AMF MSTs (RiMST5 and RiMST6) play a role in direct sugar uptake from the soil.
Spore germination and initial hyphal growth do not directly depend on the presence of host roots.
Hyphae can withdraw back into spores if no host root presence is sensed to conserve metabolic resources.
Spores can re-germinate, and novel hyphae can be formed, increasing the chances to find a symbiotic partner.
Arbuscules are involved in plant–AMF C transfer.
Even if arbuscules are probably a major player in C exchanges, functional arbuscules are not required for fungal growth and spore production.
Arbuscules might not be the only site for C transfer (Smith et al., 2001; Helber et al., 2011; Ait Lahmidi et al., 2016).
Carbohydrates were considered the major transport form of C to AMF (Casieri et al., 2013; Garcia et al., 2016).
Sugars are transferred through active or passive efflux mechanisms (Ho & Trappe, 1973; Doidy et al., 2012a,b).
Plants transport photosynthetically fixed C in the form of sucrose via the phloem into the root system (Fig. 3).
Several plant SUcrose Transporter (SUT) proteins are regulated in mycorrhizal roots (Boldt et al., 2011; Doidy et al., 2012b; Gaude et al., 2012).
No specific induction of sucrose transporter genes was found in arbuscule-containing cells, but increased promoter activity of sucrose and hexose transporter genes was found in adjacent cells (Gaude et al., 2012).
This shows a role of SUTs in C partitioning rather than direct C supply to the fungus in mycorrhizal roots.
Besides the role of plant SUTs, other plant and fungal sugar transporters are involved in sugar partitioning in AM (Casieri et al., 2013; Garcia et al., 2016).
In plant sink organs, sucrose is cleaved by plant invertases, and starch is degraded into monosaccharides transported by MSTs (Lalonde et al., 2004).
Differently regulated MSTs are potentially involved in C partitioning in AM (Harrison, 1996; Ge et al., 2008).
AMF do not take up sucrose directly but can take up hexoses (Bago et al., 2000).
Sucrose has to be cleaved into hexoses to be taken up by the fungal microsymbiont.
The AMF genome does not contain genes for known sucrose-cleaving enzymes, so sucrose has to be hydrolyzed by the host cell wall invertase.
Glucose is the major C form transferred to the AMF (Helber et al., 2011; Ait Lahmidi et al., 2016).
The plant SWEET family may include key players involved in the regulation of host–AMF exchanges (Chen, 2014).
Fungal monosaccharide transporters were recently identified in Glomeromycota (Schussler et al., 2006; Ait Lahmidi et al., 2016).
Distinct MSTs are responsible for sugar uptake at the plant–fungus and the soil–hypha interfaces and for sugar partitioning within internal fungal structures (Garcia et al., 2016).
A putative Glomeromycota sucrose transporter has been identified in AMF (Helber et al., 2011), but there is no demonstration of sucrose transfer into AM.

Lipid transport

C is also provided by the host plant to the AMF in the form of fatty acids (FAs) (Bravo et al., 2017; Jiang et al., 2017; Keymer et al., 2017; Luginbuehl et al., 2017) (Fig. 3).
In plants, de novo FA biosynthesis occurs in plastids and requires the activity of a fatty-acid synthetase complex (FAS 1).
Genes encoding potential FAS 1 are absent from the genomes or transcriptomes of the characterized AMF (R. irregularis or Gigaspora rosea).
AMF depend on host plants for de novo FA synthesis, another potential reason for the obligate biotrophy of these organisms.
The FA auxotrophy of AMF is supported by the fact that 12 genes related to lipid biosynthesis are exclusively present in the genomes of plants forming AM symbioses (Bravo et al., 2016).
R. irregularis are unable to synthesize FAs de novo from carbohydrates from isotope labeling experiments (Jiang et al., 2017).
Heterologous expression of an Umbellularia californica fatty acyl-ACP thioesterase (UcFatB) in M. truncatula produced lauric acid (Luginbuehl et al., 2017).
Lipids are the major C-storage compounds in AMF, and lipid bodies occur as prominent structures in AMF spores, pre-symbiotically grown germ tubes, and symbiotic hyphae (Bago et al., 2002).
The AM-specific plant thioesterase FatM releases 16:0 FAs (palmitic acid) which, when attached to CoA, are used as a substrate by glycerol-3-phosphate acyl transferase (GPAT) RAM2 to produce 16:0 b-monoacylglycerol (Fig. 3).
This compound can be exported across the peri-arbuscular membrane by the half-ABC transporters STR and STR2.
The mycorrhiza-specific GPAT belonged to the genes expressed in all mycorrhiza fertilized with low phosphate (Breuillin et al., 2010).
The expression of STR and STR2 also was repressed by high Pi concentrations (Wang et al., 2017a,b).
Depending on the Pi supply, the symbiont may be starved for plant lipid C.

3. Mycorrhizal Benefits: A Mutualism-to-Parasitism Continuum

Not all AMF are equally beneficial for the host (Johnson et al., 1997; Smith & Smith, 2013).
Plants can be colonized by dozens of species.
AMF are classified mainly by sequence analysis of ribosomal RNA genes (SSU or LSU).
A high intraspecific diversity is found in AMF.
The concept of species defined by Mayr (2000) is difficult to apply to Glomeromycota.
AMF hyphae are coenocytic, so intraindividual variation is difficult to distinguish from interindividual variation.
Each fungal individual shows high genetic diversity among its own nuclei (Munkvold et al., 2004; Borstler et al., 2008; Mensah et al., 2015).
Anastomosis/hyphal fusion allow for the exchange of nuclei from genetically distinct AMF and the transmission of genetic markers in newly formed spores representing the progeny (Croll et al., 2009).
AMF isolates perform self-anastomosis (Giovannetti et al., 2003), and > 90% of fusions are performed by wound healing within a same hypha (De La Providencia et al., 2005).
The capability of hyphae to perform self-anastomosis differs among AMF species (Pepe et al., 2016).
Anastomosis between AMF isolates depends on their vegetative compatibility or on their geographical origin (Giovannetti et al., 2003).
Obvious sexual structures are lacking in Glomeromycota.
Approximately 85% of the core meiotic genes (HOPP2: homologous-pairing protein 2, an MND1 (meiotic nuclear division protein 1)) are present (Halary et al., 2011; Tisserant et al., 2012).
Mycoplasma-related endobacteria (MRE) living in the AMF cytoplasm might be involved in AMF functioning (Ghignone et al., 2012) and in the pre-symbiotic growth phase (Salvioli et al., 2016).
This high intraspecific diversity among AMF may lead to high functional differences (Mensah et al., 2015; Koch et al., 2017) (Fig. 4).
Plants control the degree of AMF colonization depending on their nutrient requirements.
Pi and N have been identified as major nutritional determinants of the interaction (Nouri et al., 2014).
The nutrients delivered to the root cortical cells are believed to trigger a signal that controls C release to the fungal partner.
A symbiont unable to deliver significant amounts of soil nutrients would only have access to low C concentrations in the root apoplast (Javot et al., 2007).
Data from Pi-replete plants indicate that the plant host may restrict arbuscule development by reducing sugar and lipid delivery to the symbiont.
Knowledge about the regulation of this delivery upon high Pi or N fertilization regimes should shed light on the role of plant lipids in the regulation of AM symbiosis development.

4. The Study of the Impact of Membrane Lipids

Nutrient trades are the basis of AM symbiosis.
They are regulated by transport systems present in both partners and involved in long-distance transport of photosynthetic products and absorption/uptake of nutrients from the soil.
Incoming and outgoing nutrient flows are controlled by membrane transport proteins.
Membrane proteins and their functions are directly impacted by membrane lipids through protein–lipid interactions or through the physical properties of the lipid bilayer.
The regulation of membrane proteins via compartmentalization in specific domains of the membrane is known as 'lipid rafts' (Simon-Plas et al., 2010).
Membrane domains segregate active components inside membranes and are part of cellular processes (Rajendran & Simons, 2005).
The membrane domain concept was first established for mammalian and yeast cell membranes.
The characterization of membrane domains is related to their insolubility in detergents at cold temperatures, hence their name 'Detergent-Resistant-Membranes' (DRMs).
Membrane rafts are small (10–200 nm), heterogeneous, highly dynamic, sterol- and sphingolipid-enriched domains that compartmentalize cellular processes (Pike, 2004).
The function of rafts is related to:
- Regulation of homomeric and heteromeric interactions by the raft proteins
- Bringing-together or distancing signaling actors through lateral compartmentalization
- A direct impact of the lipid environment (Simon-Plas et al., 2010)
Plant DRMs have been characterized in several plants (Mongrand et al., 2004; Borner et al., 2005; Lefebvre et al., 2007).
Structural phospholipids are not integrated in DRMs, except polyphosphoinositides (Furt et al., 2010).
Sphingolipids also represent an important component of plant DRMs (Simon-Plas et al., 2010).
In animal cells, lipid rafts facilitate the assembly and functioning of signaling cascades.
Less is reported about plant channel localization within microdomains.
Pumps (e.g., members of the aquaporin family) are present in DRMs.
The DRM localization of pumps has to be linked to the identification of putative pump-regulating proteins (Morel et al., 2006).
Fewer reports have been issued about the regulation of plant transporters through association to DRMs.
In plant–pathogen interactions and the rhizobium–legume symbiosis, host plants need to keep stringent control at the cell level (Ott, 2017).
In both pathogenic and mutualistic PMIs, microbial molecule recognition is mediated by specific membrane-located receptors called pattern recognition receptors (PRRs).
Several of these PRRs have been localized in nanodomains (Ott, 2017).
A way to avoid cross-talk between different signaling pathways seems to be the localization of different PRRs to different nanodomains (Bucherl et al., 2017).
In the legume–rhizobium symbiosis, nod factors (NFs) are perceived by LysM-type receptor like kinases (see Zipfel & Oldroyd, 2017) that are part of complexes present in nanodomains (Ott, 2017).
There are only a few indications of a possible role of DRM association in the regulation of mycorrhizal partner transport proteins.
Simon-Plas et al. (2010) proposed that 'individual lipids and the dynamic structure and compartmentation of the bilayer as essential regulatory elements of membrane protein activity is now well established'.
Five amino-acid transporter superfamilies have been identified in animals, yeasts, and plants (Wipf et al., 2002; Lalonde et al., 2004).
Similarity of animal proteins suggests that knowledge concerning the lipid regulation of neurotransmitter transporters should help decipher this topic in plants (Butchbach et al., 2004).
Only one lysine- and histidine-specific transporter (LHT) (Morel et al., 2006; Stanislas et al., 2009) and two oligopeptide transporters (OPTs) (Stanislas et al., 2009) have been reported as being present in plant DRMs.

III. Managing Common Mycorrhizal Networks: A Tool Toward a Sustainable Agriculture

1. Common Mycorrhizal Networks?

AMF have unrestricted host ranges and can associate with most plant species (Smith & Read, 2008) (Fig. 4).
Annual plant species harbor higher AMF diversity than perennial species (Torrecillas et al., 2012).
AMF form extraradical mycelium networks that spread from colonized roots into the surrounding soil (Giovannetti & Avio, 2002; Mikkelsen et al., 2008).
The length of intact extraradical mycelium depends on the AMF and associated plant species.
The extraradical mycelium of one AMF or hyphal fusion can colonize and connect neighboring plants to form common mycorrhizal networks (CMNs) (Barto et al., 2012).
CMNs can develop among plants 12–20 cm apart (Song et al., 2010; Barto et al., 2012; Babikova et al., 2013).
CMNs benefit host plants by improving seedling establishment (van der Heijden, 2004), influencing plant and microorganism community compositions (van der Heijden & Horton, 2009), and improving interplant nutrition (He et al., 2003).
CMNs induce plant defense responses and plant communication via phytohormones (Song et al., 2010) (Fig. 4).

2. CMNs and Plant-Plant Interactions

CMNs amplify intraspecific competition (Weremijewicz & Janos, 2013).
Plants with intact CMNs showed asymmetrical competition, whereas plants with severed CMNs showed symmetrical competition (Weremijewicz & Janos, 2013).
Intact CMNs may supply N to large individuals that are highly photosynthetically active (Merrild et al., 2013).
This reciprocal reward depends on the rate of exchange of fungal mineral nutrients for host plant C (Kiers et al., 2011).
Biological market dynamics control resource exchanges in AM symbiosis, and the nutrient cost-to-benefit ratio varies among host plant species (Walder et al., 2012, 2015).
Effects of CMNs on seedling recruitment may be beneficial (van der Heijden, 2004; Walder & van der Heijden, 2015).
CMNs may provide faster mycorrhiza formation, limit the investment of seedlings in networks, give access to nutrients and water, and transfer C from one plant to another.

3. Plant–CMN–Plant Interplay and Potential for Crop Pest Control

Plant–plant signaling could be involved in food security by reducing pest-related crop losses (Fig.