Arbuscular mycorrhizal associations and the major regulators

Abstract

Plants growing in natural soils encounter diverse biotic and abiotic stresses and have adapted with sophisticated strategies to deal with complex environments such as changing root system structure, evoking biochemical responses and recruiting microbial partners. Under selection pressure, plants and their associated microorganisms assemble into a functional entity known as a holobiont. The commonest cooperative interaction is between plant roots and arbuscular mycorrhizal (AM) fungi. About 80% of terrestrial plants can form AM symbiosis with the ancient phylum Glomeromycota. A very large network of extraradical and intraradical mycelium of AM fungi connects the underground biota and the nearby carbon and nutrient fluxes. Here, we discuss recent progress on the regulators of AM associations with plants, AM fungi and their surrounding environments, and explore further mechanistic insights.

Keywords

AM symbiosis / signal / regulators / nutrients / phosphate / microbiota

1 Progression of arbuscular mycorrhizal (AM) symbiosis

AM fungi can develop potentially symbiotic relationships with the majority of land plant species based on bidirectional nutrient transfer between host plants and fungi^[1]. AM fungi can supply host plants with essential mineral nutrients such as phosphorus (P) and nitrogen (N)^[2], and a large amount of carbon fixed by the plants flows to the fungal symbiont mainly in the form of fatty acids^[3–5]. The establishment of AM symbiosis starts from the molecular dialog between plant and mycorrhizal fungi. AM fungi form hyphopodia on the root surface, invade cortical cells through a pre-penetration apparatus (PPA) and develop highly branched structures termed arbuscules in inner cortical cells^[6] (Fig. 1). Arbuscules are mainly responsible for the bidirectional nutrient exchange. This symbiotic process is precisely regulated by the host plant, the mycorrhizal fungi and the surrounding environment.

1.1 Signals from roots

Plant root exudates and phytohormones. Plant root exudates play an important role in the signaling communications between host plant and AM fungi and can stimulate morphological changes in fungal spores and hyphae. The active compounds in root exudates include strigolactones, flavonoids and 2-hydroxy fatty acids (2-OH-FA).

Strigolactones are derived from carotenoid metabolism. Despite their multiple roles as endogenous phytohormones in suppression of shoot branching, regulation of root architecture and acceleration of leaf senescence (reviewed by Waters et al.^[7]), their contribution as exogenous signals at different stages of AM formation have also been documented, such as stimulating the germination of AM fungal spores, hyphal branching in the pre-symbiotic phase and promoting hyphopodium formation in the later stages^[8–10]. However, it is unclear how strigolactones are recognized by AM fungi. Phosphorus starvation induces strigolactones biosynthesis and the gene expression of the key SL synthesis enzyme D27, which is depending on GIBBERELLIC ACID-INSENSITIVE, REPRESSOR of GAI, and SCARECROW (GRAS) transcription factors NSP1 and NSP2^[11], while the direct targets of NSP1/NSP2 and the mechanism of regulation remain unknown. Exogenous GR24, a synthetic and biologically active SL analog, leads to increased release of short-chain chitooligosaccharides (COs) from germinated spores of Rhizophagus irregularis^[12]. Exposure to COs increases the expression of strigolactones biosynthesis genes in host plants^[13], indicating a positive feedback regulation of the signal dialog between host plant and mycorrhizal fungi.

Fig.1 Schematic of the development of the arbuscular mycorrhizal (AM) symbiosis and the major regulators involved at different stages. AM development is roughly characterized as four steps: (1) spore germination; (2) hyphal branching; (3) PPA and hyphopodium formation; and (4) arbuscule development. AM fungi facilitate nutrient uptake, meanwhile Pi and N starvation also contribute as master regulators in AM development. Strigolactones secreted from host roots induce fungal spore germination and hyphal branching (steps 1 and 2), while the biosynthesis of strigolactones is controlled by inorganic P (Pi) status, chitooligosaccharides (COs), zaxinone and autoregulation of mycorrhizal symbiosis (AOM) feedback signal CLE53. AM fungi produced chitinaceous molecules (COs and LCOs) to promote pre-symbiosis signaling and effectors/peptides (RiCRN, RiSLM, SIS and RiCLE) to increase fungal colonization (step 3). DELLA, the well-known negative regulator in gibberellin acid (GA) signaling, acts as a positive regulator in arbuscule development. CBX1/WRI5a regulate the gene module related to carbon-Pi exchange between plant and fungi in the arbuscule-containing cells (step 4).

Full size|PPT slide

Flavonoids derived from the phenylpropanoid pathway are known active compounds from legume root exudates that attract potentially symbiotic bacteria^[14–16]. It has been shown that flavonoids exhibit stimulatory effects on hyphal tip elongation of AM fungi, especially when CO₂ is present mimicking the situation in the rhizosphere^[17]. Moreover, flavonoid biosynthesis is regulated by AM fungi^[14], although the type of active flavonoids that act as general signals in AM associations remain uncertain.

2-hydroxy fatty acids (2-OH-FA) were first characterized from carrot root exudates. Exogenous addition of 2-OH-FA promotes lateral branching of AM fungal hyphae^[18], suggesting the possible role of 2-OH-FA as signals in the rhizosphere. Another potential fatty acid signal is cutin. Cutin is the main component of cuticle, the waxy coat of the aboveground parts of plants^[19]. Addition of cutin monomers directly enhances hyphopodium/appressorium formation of beneficial AM fungi and pathogenic oomycetes, indicating a general role of cutin in fungal development^[20].

Zaxinone is a newly identified carotenoid-derived product that is formed by the carotenoid cleavage dioxygenase (OsZAS) in rice^[21]. In addition to its growth-regulating activity, exogenous application of zaxinone suppresses strigolactones biosynthesis but increases mycorrhization, indicating a dual role of zaxinone in plant growth and in associations with beneficial fungi^[21]. The contribution and crosstalk between zaxinone and strigolactones in plant growth and AM symbiosis merit further study.

Karrikins are smoke-derived organic compounds that can stimulate the seed germination of many fire-prone plants^[22]. Notably, the karrikins signaling pathway is closely related to that of strigolactones. Both karrikins and strigolactones are perceived by the closely-related α/β hydrolase receptors KAI2/DWARF14LIKE (D14L) and DWARF14 (D14), respectively, requiring F-box proteins (KAI1/DWARF3 and MAX2, respectively) and triggering proteasome-mediated degradation of class I Clp-ATPase SMAX/DWARF53 to regulate development^[23]. Surprisingly, D14L is required for the initial colonization by AM associations in rice^[24], indicating the existence of currently unidentified endogenous karrikins-mimic hormones in plants. Although the functions of KAI2 and D14 signaling pathways have been well dissected in root and root hair development^[25] the contribution of and the interplay between D14L and D14 signaling pathways in mycorrhizal plants remain unknown.

Gibberellins (GA) are a large class of cyclic diterpenoid phytohormones and function not merely in various aspects of plant growth but also in symbiosis^[26]. Phosphorus starvation leads to a reduction in bioactive GA levels and accumulation of DELLA protein^[27]. Addition of GA decreases fungal penetration and arbuscule development, while DELLA, a suppressor of GA signaling, is a positive regulator in AM symbiosis, as arbuscule development is greatly reduced in DELLA mutants including Medicago della1della2 double mutant and rice slr1^[28,29]. Importantly, GA also suppress root nodulation and DELLA is required for nodule symbiosis^[30]. The CCaMK-CYCLOPS-DELLA complex regulates transcriptional expression of RAM1 in mycorrhization and ERN1 in nodulation, respectively^[30,31]. Moreover, DELLA interacts with multiple transcription factors/regulators such as MYB1, MIG1, DIP1, NSP2 and RAD1^{[29,30,32–34]}, along with the capacity for interactions with GRAS proteins^[29,35–37], suggesting a integrator role of DELLA in symbiotic associations and a complicated network in the regulation of downstream genes depending on the context.

1.2 Signals from AM fungi

Chitooligosaccharide and lipochitooligosaccharide signals and LysM receptor-like kinases. Molecular signals from exudates of germinated spores and mycorrhizal carrot roots have been identified playing an essential role in pre-symbiotic communication. Rapid turnover of mycelium in soil may release photo-assimilates into the soil and provide more signals for plant-microbe and microbe-microbe interactions. The fungal cell wall consists mainly of chitin and chitin degradation generates COs which are homopolymers of β-1,4-linked N-acetyl-D-glucosamine (GlcNAc)^[38]. Chitinaceous molecules of various fungi serve as microbe-associated molecular patterns (MAMP) monitored by plant immunity^[39]. Apart from COs, mycorrhizal fungi also produce lipochitooligosaccharides (LCOs). LCOs possess the COs backbone but with lipid modification and further modifications such as sulfate on the reducing and nonreducing ends, and can stimulate early symbiotic responses^[12,40]. Recently, COs (especially CO8) have been reported to activate symbiotic signaling as well. Moreover, the combination of CO8 and LCOs can enhance the symbiotic response but suppress immunity^[41]. In addition, Nod-factors from rhizobacteria, acting as nodulation symbiotic signals, also belong to LCOs^[42], raising the question of how plants perceive and distinguish these signals to elicit the subsequent divergent downstream responses. Lysin motif receptor-like kinases (LysM-RLKs) are responsible for the recognition of COs from fungal pathogens and Nod-factors from rhizobacteria^[43]. Nod-factors are perceived by the LjNFR1/MtLYK3 and LjNFR5/MtNFP complex in Lotus japonicus and M. truncatula^[44,45]. LysM-RLK CERK1 associates with LYK4/LYK5 in Arabidopsis thaliana or CEBiP in rice for activation of immune signaling^[46,47]. CERK1 is also required for mycorrhizal symbiosis^[48,49]. In Medicago, MtCERK1 is essential for COs-induced response genes both in defense and in symbiosis^[41], and this is in line with the dual function of CERK1 in immunity and mycorrhization^[48,49]. MtNFP contributes mainly to LCOs-induced expression of symbiotic response genes, while LCOs-mediated suppression of the CO8-induced defense response depends on MtNFP rather than the common symbiosis signaling pathway (CSSP)^[41,50]. Although MtCERK1 binds COs and MtNFP binds LCOs, considering the normal mycorrhization in the Mtnfp mutant and the lower colonization still occurring in the Mtnfp Mtcerk1 double mutant^[41], additional COs and LCOs receptors are proposed to exist. Consistently, LysM-RLKs OsMYR/OsLYK2 was reported to act as a Myc-factor receptor, as reduced mycorrhization was observed in an OsMYR defective mutant and OsMYR directly binds CO4 so as to enhance the association with OsCERK1^[51]. CO4 enhances the phosphorylation of OsMYR and OsCERK1^[51]. Notably, the variation in the second LysM of OsCERK1 was found to be important for the mycorrhization^[52]. LjNFR5/MtNFP orthologs in petunia and tomato, PhLYK10 and SlLYK10, showed higher binding affinity toward LCOs and are required for mycorrhizal symbiosis. PhLYK10 and SlLYK10 can also rescue the nodule formation in the Mtnfp mutant^[53]. These findings provide novel insights into the signal recognition in pre-symbiosis in natural contexts when AM fungal-secreted COs/LCOs signal cocktail triggers integrated output of immune and symbiotic responses through various LysM-RLKs, some of which are multifunctional.

Chitin is the second most abundant polysaccharide in nature after cellulose and is rich in nitrogen. In addition to serving as an elicitor in defense and symbiosis in the form of oligomers, the monomer for chitin may also act as an alternative source of nutrients for AM fungi or as potential signals exuded by plants in symbiotic associations. The GlcNAc transporter RiGNT from R. irregularis is able to take up GlcNAc from yeast and the RiGNT gene is highly expressed in intraradical hyphae together with GlcNAc metabolic genes, suggesting that R. irregularis may recycle COs as N nutrients in degenerated arbuscules^[54]. The plant GlcNAc transporter NOPE1 was first identified in rice and maize and is required for initiation of AM symbiosis^[55]. The distinct transcriptional responses in R. irregularis spores treated with exudates from the wild type or Osnope1 rice mutant support the proposition that NOPE1 is essential for priming AM fungi at the pre-symbiotic stage through the release of unknown bioactive components (GlcNAc derivatives) as early signals^[55].

1.3 Proteins and effectors secreted by AM fungi

A genome-wide survey reveals that R. irregularis and Gigaspora rosea possess a large set of putative secreted proteins (SPs). Some of these SPs are commonly upregulated during the colonization of different hosts and might be important in establishing and maintaining the AM symbiosis^[56]. Most of the SPs are small proteins of unknown function and may serve as effectors regulating plant-AM fungal interactions. Numerous SPs in R. irregularis have been predicted to be cleaved by KEX2, the conserved endoprotease in fungi that recognizes specific motifs and produces small peptides that are released into the extracellular spaces^[57]. Through AM fungal genome sequencing in combination with bioinformatic analysis, a total of 220 effector candidates were identified in R. irregularis and about 95% of these showed homologs in Rhizophagus clarus^[58]. It appears that AM fungi can provide the potential candidates of secreted effectors in a host- and stage-dependent manner^[59]. Although effectors are known to counter MAMP-triggered immunity and facilitate colonization in pathogenesis, very few effectors have been well investigated in AM symbiosis.

The SP7 effector from R. irregularis interacts with the pathogenesis-related transcription factor MtERF19 in M. truncatula and constitutive expression of SP7 in roots leads to increased mycorrhization and reduced expression of plant defense genes^[60]. A group of Crinkler effectors present in R. irregularis and silencing of RiCRN1 by host-induced gene silence (HIGS) lead to reduced mycorrhization in M. truncatula^[61]. SL-induced putative SP SIS1 is required for mycorrhizal symbiosis, as knockdown of SIS1 by HIGS results in a reduced mycorrhization rate and stunted arbuscules in M. truncatula^[62]. The LysM effector RiSLM is one of the highest expressed effectors from R. irregularis and is able to sequester fungal cell wall-derived COs to protect hyphae from plant chitinases so as to evade chitin-triggered immunity^[63,64]. Silencing RiSLM by HIGS shows that RiSLM is positively required for AM fungal colonization and arbuscule development^[63]. Although RiSLM also binds LCOs, the LCO-triggered symbiotic transcriptional response was not inhibited by excessive RiSLM^[63]. It is therefore conceivable that AM fungi might use a suite of effectors to block plant immunity and develop a successful association.

AM and root nodule symbiosis and actinobacteria symbiosis share the common symbiotic signaling pathway (CSSP) and, even if few signal molecules and cognate receptors are reported, several interesting questions remain. How do plant cells discriminate the signals from different microbes to trigger divergent downstream networks of transcriptomic and metabolic responses? How are the host spectrum and distribution of the divergent AM fungi determined? What are the roles of secreted proteins/effectors in determining host specificity?

2 Regulation of AM symbiosis

2.1 Nutrients as regulators of AM symbiosis

Nitrogen, phosphorus and potassium (K) are the major macronutrients limiting plant growth despite the fact that they are the most abundant elements in soils, as a result of their availability being low due to strong adsorption on mineral surfaces. Plants have adapted to assimilate mineral nutrients from their surroundings directly or through beneficial microbes such as Frankia, Rhizobium and mycorrhizal fungi, especially when the hydromineral resources are scarce^[65–67]. The characteristic effect of AM symbiosis is to increase nutrient uptake, especially N, P and K uptake. Plants take up inorganic phosphate (Pi) from soils via direct Pi uptake (DPU) and mycorrhizal Pi uptake (MPU) pathways, but MPU suppresses DPU and may contribute up to 100% of the total Pi uptake by host plants^[68,69]. The plant phosphate transporter 1 (Pht1) family has a pivotal role in phosphate uptake, translocation and remobilization^[70,71]. Numerous studies over the past two decades have found mycorrhiza-inducible and mycorrhiza-specific Pi transporters in different plant species and these transporters are clustered into two clades of the Pht1 family according to their protein sequences^[72–78], while the transcriptional regulation mechanism of the mycorrhiza-specific Pi transporters has been recently reported. AP2 transcription factors CBX1 in Lotus japonicus and WRI5a in Medicago truncatula regulate the transcription of the mycorrhiza-specific Pi transporter gene PT4 in the CTTC/AW-dependent manner and transient expression of CBX1 may also activate the mycorrhiza-specific Pi transporter genes from different host species, suggesting a conserved mechanism in dicotyledon species^[79,80]. Moreover, the genes involved in de novo biosynthesis and transport of fatty acids in response to AM fungi were upregulated by CBX1 and WRI5a, indicating that the gene module related to carbon and Pi exchange in AM symbiosis is regulated by CBX1/WRI5a. As the periarbuscular membrane localized Pi transporters are Pi:H symporters, H⁺-ATPase was supposed to generate the proton gradient to counteract the proton influx in cytoplasm via Pi transporters^[71]. The co-regulated H⁺-ATPase is essential for AM symbiosis^[81,82] and overexpression of H⁺-ATPase simultaneously enhanced phosphate and nitrogen uptake^[83], supporting the linked P and N uptake in AM symbiosis. Increasing evidence indicates that AM fungi take up and transfer organic (amino acids and peptides) and inorganic N (nitrate, NO₃^– and ammonium, NH₄⁺) to their hosts, and about one-third of the root protein N may be provided by AM fungi^[84]. Several mycorrhiza-inducible N transporters have been reported in plants (reviewed by Wipf et al.^[85]), while their function and regulation mechanisms in AM symbiosis are not yet characterized. Genome-wide gene expression profiles in different mycorrhizal species have been described, including mycorrhiza-induced K transporter genes^[86–88]. In tomato, the mycorrhiza-specific K transporter SlHAK10 is involved in mycorrhizal K uptake, as Slhak10 mutants showed decreased mycorrhizal K uptake and overexpression of SlHAK10 enhanced mycorrhization only under low K conditions^[89].

In addition, P and N status are major regulators of AM symbiotic associations rather than other major nutrients such as K, S, Mg, Ca and Fe^[90]. Pi deficiency promotes AM symbiosis and Pi sufficiency suppresses AM symbiosis^[91]. Addition of N also decreases mycorrhization^[92]. The suppression of AM symbiosis by high Pi may lead to starvation of other nutrients due to reduction of functional fungal structures. However, N starvation forces the plant to bypass the high Pi suppression on AM formation in plants, suggesting a complicated regulation by N and P status^[90]. Mature arbuscules and periarbuscular membrane are responsible for nutrient exchange during AM symbiosis. The degenerated arbuscule phenotype in the phosphate transporter Mtpt4 mutant was suppressed by deprivation of N simultaneously, which is dependent on the ammonium transporter gene AMT2.3, but with unchanged shoot N transport^[93]. It is therefore reasonable to speculate that the transporters may also act as P and N sensors in AM symbiosis and interaction between P and N signaling may exist. In the AM nonhost A. thaliana, inositol pyrophosphate InsP8 ligand binds the Pi sensor SPX domain-containing protein 1 (SPX1) to regulate the Pi-dependent response^[94], and the nitrate transceptor NRT1.1 (CHL1/NPF6.3) functions as a dual-affinity transporter and nitrate sensor in nitrate signaling^[95–97]. Further investigations are therefore required to obtain insights into the P and N sensing and crosstalk between P and N signaling in mycorrhizal symbiosis. In addition, the impact of K on AM symbiosis has been little studied. When long-term K deprivation was induced in M. truncatula, K availability did not affect AM colonization, but mycorrhizal plants showed increased root biomass and shoot K⁺ contents compared with nonmycorrhizal plants under K-limited conditions, and the genome-wide transcriptional profile indicates that AM fungi might modulate the plant responses to K starvation^[98]. In addition, cross-talks between macronutrients and micronutrients have been recognized^[99]. The complicated tripartite interactions among the nutrients Pi, Zn and Fe in mycorrhizal and non-mycorrhizal plants have been discussed in detail^[100].

2.2 Systemic regulation of AM symbiosis

CLAVATA3/Endosperm surrounding region-related (CLE) peptides comprise 12–13 amino acid glycosylated peptides and work in a similar manner to phytohormones regulating developmental processes and stress responses locally and systemically^[101]. Several CLEs are responsive to the macronutrients N, P and S or AM fungi in M. truncatula and L. japonicus^[87,102]. CLE peptides are involved in local and systemic control of the extent of symbionts^[103]. Root nodule formation is controlled by a systemic feedback loop called autoregulation of nodulation (AON), involving nodule-induced CLE peptides and CLV1-like leucine-rich repeat (LRR) RLKs LjHAR1/MtSUNN/GmNARK in the shoots, leading to a shoot-derived suppression of nodule numbers in the roots^[104,105]. Similarly, defects in LjHAR1/MtSUNN/GmNARK led to increased AM fungal colonization, implicating a role for these LRR-RLKs in autoregulation of mycorrhizal symbiosis (AOM)^[106–108]. MtCLE53 was induced by both Glomus versiforme and R. irregularis in M. truncatula roots and MtCLE33 was induced in response to high Pi^[109]. Overexpression of either MtCLE53 or MtCLE33 resulted in reduced fungal entry and colonization, while knockdown of MtCLE53 by RNA interference showed enhanced mycorrhization. Overexpression of MtCLE53 or MtCLE33 also led to downregulation of SL biosynthesis genes and upregulation of the cognate receptor gene MtSUNN^[109]. This evidence provides a new avenue toward the AOM in roots by CLEs-SUNN through strigolactones, integrating P status and mycorrhization. Interestingly, a RiCLE from R. irregularis was identified that can promote mycorrhizal colonization^[110]. A large set of AM-induced and AM-suppressed RLKs was identified in silico^[87]. Only a few LysM-RLKs and LRR-RLKs have been well studied, while the functions of other RLKs such as L-type lectin RLKs, malectin RLKs, pollen RLKs and wall-associated kinases in AM symbiosis remain unknown, and the cognate ligands of these potential receptors are also unknown.

3 AM symbiosis and root microbiota in natural soils

Plants grow in a microbe-rich environment and different plant species harbor diverse microbiome in their roots and the rhizosphere. Plants recruit functional conserved core microbial consortia from soil^[111]. A beneficial association with AM fungi can affect the root fungal community. Based on the relative microbiota profiling (RMP) of bacterial 16S rRNA genes and fungal internal transcribed spacers (ITSs), it has been shown that wildtype L. japonicus plants host a wide spectrum of Glomeromycota, while defective mutants in AM symbiosis disturbed the assemblage of microbes especially in the endosphere, characterized by depletion of Glomeromycota and concomitant enrichment of Ascomycota including fungi from Helotiales and Nectriaceae^[112,113]. AM fungi may inhibit root colonization by other endophytic fungi through direct interactions such as antagonism via the release of antimicrobial substances or competition for resources, and by indirect effects associated with plant mycorrhization and/or primed plant immunity^[113]. It has been hypothesized that non-symbiotic microorganisms can highjack components of AM signaling pathways to effectively colonize plant tissues, but experimental evidence is insufficient to provide a clear conclusion^[114–117]. Few fungal taxa were consistently depleted in all tested symbiotic mutant plants other than Glomeromycota taxa, suggesting that this might be true for some but not all microbes^[113]. Further investigations on isolation of the fungi which require CSSP genes for colonization will help to answer this question. Recently, based on a quantitative microbiota profiling (QMP) method to absolutely quantify the bacterial 16S rRNA gene in bulk soil and rhizocompartments, a novel feature of rhizosphere bacterial microbiota assembly compared to the RMP method was proposed^[118]. It will be important to revisit the impact of AM fungi on the root community based on quantitative microbiota profiling.

Plant species and environmental factors contribute significantly to the assemblage of the microbial community. Indeed, L. japonicus and A. thaliana possess distinguishable fungal communities, even though the soil was taken from the same site^[113,119]. Phosphorus status and active compounds in root exudates (strigolactones and cutin monomers) do have effects on other biotic interactions^{[20,120–122]}. Other beneficial endophytes were reported to be functional under P deficiency conditions. In non-mycorrhizal Brassicaceae species, beneficial fungi (ascomycetes Collectotrichum tofieldiae and Helotiales F229) can alleviate phosphate starvation in A. thaliana and Arabis alpina, respectively; the basidiomycete Serendipita indica (syn. Piriformospora indica) was isolated and reintroduced, and this significantly increased plant growth and P uptake in A. thaliana and maize^{[119,123–125]}. On the other hand, mycorrhiza helper bacteria were isolated from various plant-mycorrhizal fungal symbioses or the rhizosphere with significant effects on mycorrhiza formation or positive impacts on the function of mycorrhizal symbiosis^[126]. Some AM fungi from Gigasporaceae harbor endobacteria which are not essential for AM fungal survival but can enhance fungal fitness^[127]. Further studies on the endobacteria in AM fungi and beneficial microbes in nonmycorrhizal species are needed to understand and exploit beneficial associations in and beyond legume species in natural soils.

References

[1] Smith S E, Smith F A. Fresh perspectives on the roles of arbuscular mycorrhizal fungi in plant nutrition and growth. Mycologia, 2012, 104(1): 1–13

[2] Wang W, Shi J, Xie Q, Jiang Y, Yu N, Wang E. Nutrient exchange and regulation in arbuscular mycorrhizal symbiosis. Molecular Plant, 2017, 10(9): 1147–1158

[3] Jiang Y, Wang W, Xie Q, Liu N, Liu L, Wang D, Zhang X, Yang C, Chen X, Tang D, Wang E. Plants transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi. Science, 2017, 356(6343): 1172–1175

[4] Luginbuehl L H, Menard G N, Kurup S, Van Erp H, Radhakrishnan G V, Breakspear A, Oldroyd G E D, Eastmond P J. Fatty acids in arbuscular mycorrhizal fungi are synthesized by the host plant. Science, 2017, 356(6343): 1175–1178

[5] Keymer A, Pimprikar P, Wewer V, Huber C, Brands M, Bucerius S L, Delaux P M, Klingl V, Röpenack-Lahaye E V, Wang T L, Eisenreich W, Dörmann P, Parniske M, Gutjahr C. Lipid transfer from plants to arbuscular mycorrhiza fungi. eLife, 2017, 6: e29107

[6] Gutjahr C, Parniske M. Cell and developmental biology of arbuscular mycorrhiza symbiosis. Annual Review of Cell and Developmental Biology, 2013, 29(1): 593–617

[7] Waters M T, Gutjahr C, Bennett T, Nelson D C. Strigolactone signaling and evolution. Annual Review of Plant Biology, 2017, 68(1): 291–322

[8] Akiyama K, Matsuzaki K, Hayashi H. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature, 2005, 435(7043): 824–827

[9] Besserer A, Puech-Pagès V, Kiefer P, Gomez-Roldan V, Jauneau A, Roy S, Portais J C, Roux C, Bécard G, Séjalon-Delmas N. Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biology, 2006, 4(7): e226

[10] Kobae Y, Kameoka H, Sugimura Y, Saito K, Ohtomo R, Fujiwara T, Kyozuka J. Strigolactone biosynthesis genes of rice arerequired for the punctual entry of arbuscular mycorrhizal fungi into the roots. Plant & Cell Physiology, 2018, 59(3): 544–553

[11] Liu W, Kohlen W, Lillo A, Op den Camp R, Ivanov S, Hartog M, Limpens E, Jamil M, Smaczniak C, Kaufmann K, Yang W C, Hooiveld G J E J, Charnikhova T, Bouwmeester H J, Bisseling T, Geurts R. Strigolactone biosynthesis in Medicago truncatula and rice requires the symbiotic GRAS-type transcription factors NSP1 and NSP2. Plant Cell, 2011, 23(10): 3853–3865

[12] Genre A, Chabaud M, Balzergue C, Puech-Pagès V, Novero M, Rey T, Fournier J, Rochange S, Bécard G, Bonfante P, Barker D G. Short-chain chitin oligomers from arbuscular mycorrhizal fungi trigger nuclear Ca²⁺ spiking in Medicago truncatula roots and their production is enhanced by strigolactone. New Phytologist, 2013, 198(1): 190–202

[13] Giovannetti M, Mari A, Novero M, Bonfante P. Early Lotus japonicus root transcriptomic responses to symbiotic and pathogenic fungal exudates. Frontiers of Plant Science, 2015, 6: 480

[14] Abdel-Lateif K, Bogusz D, Hocher V. The role of flavonoids in the establishment of plant roots endosymbioses with arbuscular mycorrhiza fungi, rhizobia and Frankia bacteria. Plant Signaling & Behavior, 2012, 7(6): 636–641

[15] Aguilar J M M, Ashby A M, Richards A J M, Loake G J, Watson M D, Shaw C H. Chemotaxis of Rhizobium leguminosarum towards flavonoid inducers of the symbiotic nodulation genes. Journal of General and Applied Microbiology, 1988, 134(10): 2741–2746

[16] Dharmatilake A J, Bauer W D. Chemotaxis of Rhizobium meliloti towards nodulation gene-inducing compounds from alfalfa roots. Applied and Environmental Microbiology, 1992, 58(4): 1153–1158

[17] Bécard G, Douds D D, Pfeffer P E. Extensive in vitro hyphal growth of vesicular-arbuscular mycorrhizal gungi in the presence of CO₂ and flavonols. Applied and Environmental Microbiology, 1992, 58(3): 821–825

[18] Nagahashi G, Douds D D Jr. The effects of hydroxy fatty acids on the hyphal branching of germinated spores of AM fungi. Fungal Biology, 2011, 115(4–5): 351–358

[19] Fich E A, Segerson N A, Rose J K C. The plant polyester cutin: biosynthesis, structure, and biological roles. Annual Review of Plant Biology, 2016, 67(1): 207–233

[20] Wang E, Schornack S, Marsh J F, Gobbato E, Schwessinger B, Eastmond P, Schultze M, Kamoun S, Oldroyd G E D. A common signaling process that promotes mycorrhizal and oomycete colonization of plants. Current Biology, 2012, 22(23): 2242–2246

[21] Wang J Y, Haider I, Jamil M, Fiorilli V, Saito Y, Mi J, Baz L, Kountche B A, Jia K P, Guo X, Balakrishna A, Ntui V O, Reinke B, Volpe V, Gojobori T, Blilou I, Lanfranco L, Bonfante P, Al-Babili S. The apocarotenoid metabolite zaxinone regulates growth and strigolactone biosynthesis in rice. Nature Communications, 2019, 10(1): 810

[22] Nelson D C, Flematti G R, Ghisalberti E L, Dixon K W, Smith S M. Regulation of seed germination and seedling growth by chemical signals from burning vegetation. Annual Review of Plant Biology, 2012, 63(1): 107–130

[23] Morffy N, Faure L, Nelson D C. Smoke and hormone mirrors: action and evolution of karrikin and strigolactone signaling. Trends in Genetics, 2016, 32(3): 176–188

[24] Gutjahr C, Gobbato E, Choi J, Riemann M, Johnston M G, Summers W, Carbonnel S, Mansfield C, Yang S Y, Nadal M, Acosta I, Takano M, Jiao W B, Schneeberger K, Kelly K A, Paszkowski U. Rice perception of symbiotic arbuscular mycorrhizal fungi requires the karrikin receptor complex. Science, 2015, 350(6267): 1521–1524

[25] Villaécija-Aguilar J A, Hamon-Josse M, Carbonnel S, Kretschmar A, Schmidt C, Dawid C, Bennett T, Gutjahr C. SMAX1/SMXL2 regulate root and root hair development downstream of KAI2-mediated signalling in Arabidopsis. PLOS Genetics, 2019, 15(8): e1008327

[26] McGuiness P N, Reid J B, Foo E. The role of gibberellins and brassinosteroids in nodulation and arbuscular mycorrhizal associations. Frontiers of Plant Science, 2019, 10: 269

[27] Jiang C, Gao X, Liao L, Harberd N P, Fu X. Phosphate starvation root architecture and anthocyanin accumulation responses are modulated by the gibberellin-DELLA signaling pathway in Arabidopsis. Plant Physiology, 2007, 145(4): 1460–1470

[28] Floss D S, Levy J G, Lévesque-Tremblay V, Pumplin N, Harrison M J. DELLA proteins regulate arbuscule formation in arbuscular mycorrhizal symbiosis. Proceedings of the National Academy of Sciences of the United States of America, 2013, 110(51): E5025–E5034

[29] Yu N, Luo D, Zhang X, Liu J, Wang W, Jin Y, Dong W, Liu J, Liu H, Yang W, Zeng L, Li Q, He Z, Oldroyd G E D, Wang E. A DELLA protein complex controls the arbuscular mycorrhizal symbiosis in plants. Cell Research, 2014, 24(1): 130–133

[30] Jin Y, Liu H, Luo D, Yu N, Dong W, Wang C, Zhang X, Dai H, Yang J, Wang E. DELLA proteins are common components of symbiotic rhizobial and mycorrhizal signalling pathways. Nature Communications, 2016, 7(1): 12433

[31] Pimprikar P, Carbonnel S, Paries M, Katzer K, Klingl V, Bohmer M J, Karl L, Floss D S, Harrison M J, Parniske M, Gutjahr C. A CCaMK-CYCLOPS-DELLA complex activates transcription of RAM1 to regulate arbuscule branching. Current Biology, 2016, 26(8): 987–998

[32] Floss D S, Gomez S K, Park H J, MacLean A M, Müller L M, Bhattarai K K, Lévesque-Tremblay V, Maldonado-Mendoza I E, Harrison M J. A transcriptional program for arbuscule degeneration during AM symbiosis is regulated by MYB1. Current Biology, 2017, 27(8): 1206–1212

[33] Heck C, Kuhn H, Heidt S, Walter S, Rieger N, Requena N. Symbiotic fungi control plant root cortex development through the novel GRAS transcription factor MIG1. Current Biology, 2016, 26(20): 2770–2778

[34] Floss D S, Lévesque-Tremblay V, Park H J, Harrison M J. DELLA proteins regulate expression of a subset of AM symbiosis-induced genes in Medicago truncatula. Plant Signaling & Behavior, 2016, 11(4): e1162369

[35] Xue L, Cui H, Buer B, Vijayakumar V, Delaux P M, Junkermann S, Bucher M. Network of GRAS transcription factors involved in the control of arbuscule development in Lotus japonicus. Plant Physiology, 2015, 167(3): 854–871

[36] Hirsch S, Kim J, Muñoz A, Heckmann A B, Downie J A, Oldroyd G E D. GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula. Plant Cell, 2009, 21(2): 545–557

[37] Gobbato E, Marsh J F, Vernié T, Wang E, Maillet F, Kim J, Miller J B, Sun J, Bano S A, Ratet P, Mysore K S, Dénarié J, Schultze M, Oldroyd G E D. A GRAS-type transcription factor with a specific function in mycorrhizal signaling. Current Biology, 2012, 22(23): 2236–2241

[38] Liaqat F, Eltem R. Chitooligosaccharides and their biological activities: a comprehensive review. Carbohydrate Polymers, 2018, 184: 243–259

[39] Cao Y, Halane M K, Gassmann W, Stacey G. The role of plant innate immunity in the legume-rhizobium symbiosis. Annual Review of Plant Biology, 2017, 68(1): 535–561

[40] Maillet F, Poinsot V, André O, Puech-Pagès V, Haouy A, Gueunier M, Cromer L, Giraudet D, Formey D, Niebel A, Martinez E A, Driguez H, Bécard G, Dénarié J. Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature, 2011, 469(7328): 58–63

[41] Feng F, Sun J, Radhakrishnan G V, Lee T, Bozsóki Z, Fort S, Gavrin A, Gysel K, Thygesen M B, Andersen K R, Radutoiu S, Stougaard J, Oldroyd G E D. A combination of chitooligosaccharide and lipochitooligosaccharide recognition promotes arbuscular mycorrhizal associations in Medicago truncatula. Nature Communications, 2019, 10(1): 5047

[42] Dénarié J, Debellé F, Promé J C. Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annual Review of Biochemistry, 1996, 65(1): 503–535

[43] Zipfel C, Oldroyd G E D. Plant signalling in symbiosis and immunity. Nature, 2017, 543(7645): 328–336

[44] Madsen E B, Madsen L H, Radutoiu S, Olbryt M, Rakwalska M, Szczyglowski K, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J. A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature, 2003, 425(6958): 637–640

[45] Radutoiu S, Madsen L H, Madsen E B, Felle H H, Umehara Y, Grønlund M, Sato S, Nakamura Y, Tabata S, Sandal N, Stougaard J. Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature, 2003, 425(6958): 585–592

[46] Cao Y, Liang Y, Tanaka K, Nguyen C T, Jedrzejczak R P, Joachimiak A, Stacey G. The kinase LYK5 is a major chitin receptor in Arabidopsis and forms a chitin-induced complex with related kinase CERK1. eLife, 2014, 3: e03766

[47] Hayafune M, Berisio R, Marchetti R, Silipo A, Kayama M, Desaki Y, Arima S, Squeglia F, Ruggiero A, Tokuyasu K, Molinaro A, Kaku H, Shibuya N. Chitin-induced activation of immune signaling by the rice receptor CEBiP relies on a unique sandwich-type dimerization. Proceedings of the National Academy of Sciences of the United States of America, 2014, 111(3): E404–E413

[48] Zhang X, Dong W, Sun J, Feng F, Deng Y, He Z, Oldroyd G E D, Wang E. The receptor kinase CERK1 has dual functions in symbiosis and immunity signalling. Plant Journal, 2015, 81(2): 258–267

[49] Miyata K, Kozaki T, Kouzai Y, Ozawa K, Ishii K, Asamizu E, Okabe Y, Umehara Y, Miyamoto A, Kobae Y, Akiyama K, Kaku H, Nishizawa Y, Shibuya N, Nakagawa T. The bifunctional plant receptor, OsCERK1, regulates both chitin-triggered immunity and arbuscular mycorrhizal symbiosis in rice. Plant & Cell Physiology, 2014, 55(11): 1864–1872

[50] Sun J, Miller J B, Granqvist E, Wiley-Kalil A, Gobbato E, Maillet F, Cottaz S, Samain E, Venkateshwaran M, Fort S, Morris R J, Ané J M, Dénarié J, Oldroyd G E D. Activation of symbiosis signaling by arbuscular mycorrhizal fungi in legumes and rice. Plant Cell, 2015, 27(3): 823–838

[51] He J, Zhang C, Dai H, Liu H, Zhang X, Yang J, Chen X, Zhu Y, Wang D, Qi X, Li W, Wang Z, An G, Yu N, He Z, Wang Y F, Xiao Y, Zhang P, Wang E. A LysM receptor heteromer mediates perception of arbuscular mycorrhizal symbiotic signal in rice. Molecular Plant, 2019, 12(12): 1561–1576

[52] Huang R, Li Z, Mao C, Zhang H, Sun Z, Li H, Huang C, Feng Y, Shen X, Bucher M, Zhang Z, Lin Y, Cao Y, Duanmu D. Natural variation at OsCERK1 regulates arbuscular mycorrhizal symbiosis in rice. New Phytologist, 2020, 225(4): 1762–1776

[53] Girardin A, Wang T M, Ding Y, Keller J, Buendia L, Gaston M, Ribeyre C, Gasciolli V, Auriac M C, Vernie T, Bendahmane A, Ried M K, Parniske M, Morel P, Vandenbussche M, Schorderet M, Reinhardt D, Delaux P M, Bono J J, Lefebvre B.LCO receptors involved in arbuscular mycorrhiza are functional for rhizobia perception in legumes. Current Biology, 2019, 29(24): 4249–4259. e5

[54] Kobae Y, Kawachi M, Saito K, Kikuchi Y, Ezawa T, Maeshima M, Hata S, Fujiwara T. Up-regulation of genes involved in N-acetylglucosamine uptake and metabolism suggests a recycling mode of chitin in intraradical mycelium of arbuscular mycorrhizal fungi. Mycorrhiza, 2015, 25(5): 411–417

[55] Nadal M, Sawers R, Naseem S, Bassin B, Kulicke C, Sharman A, An G, An K, Ahern K R, Romag A, Brutnell T P, Gutjahr C, Geldner N, Roux C, Martinoia E, Konopka J B, Paszkowski U. An N-acetylglucosamine transporter required for arbuscular mycorrhizal symbioses in rice and maize. Nature Plants, 2017, 3(6): 17073

[56] Kamel L, Tang N, Malbreil M, San Clemente H, Le Marquer M, Roux C, Frei Dit Frey N. The comparison of expressed candidate secreted proteins from two arbuscular mycorrhizal fungi unravels common and specific molecular tools to invade different host plants. Frontiers of Plant Science, 2017, 8: 124

[57] Le Marquer M, San Clemente H, Roux C, Savelli B, Frei Dit Frey N. Identification of new signalling peptides through a genome-wide survey of 250 fungal secretomes. BMC Genomics, 2019, 20(1): 64

[58] Sędzielewska Toro K, Brachmann A. The effector candidate repertoire of the arbuscular mycorrhizal fungus Rhizophagus clarus. BMC Genomics, 2016, 17(1): 101

[59] Zeng T, Holmer R, Hontelez J, Te Lintel-Hekkert B, Marufu L, de Zeeuw T, Wu F, Schijlen E, Bisseling T, Limpens E. Host- and stage-dependent secretome of the arbuscular mycorrhizal fungus Rhizophagus irregularis. Plant Journal, 2018, 94(3): 411–425

[60] Kloppholz S, Kuhn H, Requena N. A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy. Current Biology, 2011, 21(14): 1204–1209

[61] Voß S, Betz R, Heidt S, Corradi N, Requena N. RiCRN1, a crinkler effector from the arbuscular mycorrhizal fungus Rhizophagus irregularis, functions in arbuscule development. Frontiers in Microbiology, 2018, 9: 2068

[62] Tsuzuki S, Handa Y, Takeda N, Kawaguchi M. Strigolactone-induced putative secreted protein 1 is required for the establishment of symbiosis by the arbuscular mycorrhizal fungus Rhizophagus irregularis. Molecular Plant-Microbe Interactions, 2016, 29(4): 277–286

[63] Zeng T, Rodriguez-Moreno L, Mansurkhodzaev A, Wang P, van den Berg W, Gasciolli V, Cottaz S, Fort S, Thomma B P H J, Bono J J, Bisseling T, Limpens E. A lysin motif effector subverts chitin-triggered immunity to facilitate arbuscular mycorrhizal symbiosis. New Phytologist, 2020, 225(1): 448–460

[64] Schmitz A M, Pawlowska T E, Harrison M J. A short LysM protein with high molecular diversity from an arbuscular mycorrhizal fungus, Rhizophagus irregularis. Mycoscience, 2019, 60(1): 63–70

[65] Smith S E, Smith F A. Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annual Review of Plant Biology, 2011, 62(1): 227–250

[66] Santi C, Bogusz D, Franche C. Biological nitrogen fixation in non-legume plants. Annals of Botany, 2013, 111(5): 743–767

[67] Ferguson B J, Mens C, Hastwell A H, Zhang M, Su H, Jones C H, Chu X, Gresshoff P M. Legume nodulation: the host controls the party. Plant, Cell & Environment, 2019, 42(1): 41–51

[68] Smith S E, Smith F A, Jakobsen I. Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiology, 2003, 133(1): 16–20

[69] Smith S E, Smith F A, Jakobsen I. Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. New Phytologist, 2004, 162(2): 511–524

[70] Nussaume L, Kanno S, Javot H, Marin E, Pochon N, Ayadi A, Nakanishi T M, Thibaud M C. Phosphate import in plants: focus on the PHT1 transporters. Frontiers of Plant Science, 2011, 2: 83

[71] Bucher M. Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytologist, 2007, 173(1): 11–26

[72] Loth-Pereda V, Orsini E, Courty P E, Lota F, Kohler A, Diss L, Blaudez D, Chalot M, Nehls U, Bucher M, Martin F. Structure and expression profile of the phosphate Pht1 transporter gene family in mycorrhizal Populus trichocarpa. Plant Physiology, 2011, 156(4): 2141–2154

[73] Walder F, Brulé D, Koegel S, Wiemken A, Boller T, Courty P E. Plant phosphorus acquisition in a common mycorrhizal network: regulation of phosphate transporter genes of the Pht1 family in sorghum and flax. New Phytologist, 2015, 205(4): 1632–1645

[74] Rausch C, Bucher M. Molecular mechanisms of phosphate transport in plants. Planta, 2002, 216(1): 23–37

[75] Karandashov V, Bucher M. Symbiotic phosphate transport in arbuscular mycorrhizas. Trends in Plant Science, 2005, 10(1): 22–29

[76] Javot H, Penmetsa R V, Terzaghi N, Cook D R, Harrison M J. A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proceedings of the National Academy of Sciences of the United States of America, 2007, 104(5): 1720–1725

[77] Yang S Y, Grønlund M, Jakobsen I, Grotemeyer M S, Rentsch D, Miyao A, Hirochika H, Kumar C S, Sundaresan V, Salamin N, Catausan S, Mattes N, Heuer S, Paszkowski U. Nonredundant regulation of rice arbuscular mycorrhizal symbiosis by two members of the phosphate transporter1 gene family. Plant Cell, 2012, 24(10): 4236–4251

[78] Willmann M, Gerlach N, Buer B, Polatajko A, Nagy R, Koebke E, Jansa J, Flisch R, Bucher M. Mycorrhizal phosphate uptake pathway in maize: vital for growth and cob development on nutrient poor agricultural and greenhouse soils. Frontiers of Plant Science, 2013, 4: 533

[79] Xue L, Klinnawee L, Zhou Y, Saridis G, Vijayakumar V, Brands M, Dörmann P, Gigolashvili T, Turck F, Bucher M. AP2 transcription factor CBX1 with a specific function in symbiotic exchange of nutrients in mycorrhizal Lotus japonicus. Proceedings of the National Academy of Sciences of the United States of America, 2018, 115(39): E9239–E9246

[80] Jiang Y, Xie Q, Wang W, Yang J, Zhang X, Yu N, Zhou Y, Wang E. Medicago AP2-domain transcription factor WRI5a is a master regulator of lipid biosynthesis and transfer during mycorrhizal symbiosis. Molecular Plant, 2018, 11(11): 1344–1359

[81] Krajinski F, Courty P E, Sieh D, Franken P, Zhang H, Bucher M, Gerlach N, Kryvoruchko I, Zoeller D, Udvardi M, Hause B. The H⁺-ATPase HA1 of Medicago truncatula is essential for phosphate transport and plant growth during arbuscular mycorrhizal symbiosis. Plant Cell, 2014, 26(4): 1808–1817

[82] Wang E, Yu N, Bano S A, Liu C, Miller A J, Cousins D, Zhang X, Ratet P, Tadege M, Mysore K S, Downie J A, Murray J D, Oldroyd G E D, Schultze M. A H⁺-ATPase that energizes nutrient uptake during mycorrhizal symbioses in rice and Medicago truncatula. Plant Cell, 2014, 26(4): 1818–1830

[83] Liu J, Chen J, Xie K, Tian Y, Yan A, Liu J, Huang Y, Wang S, Zhu Y, Chen A, Xu G. A mycorrhiza-specific H⁺-ATPase is essential for arbuscule development and symbiotic phosphate and nitrogen uptake. Plant, Cell & Environment, 2020, 43(4): 1069–1083

[84] Govindarajulu M, Pfeffer P E, Jin H, Abubaker J, Douds D D, Allen J W, Bücking H, Lammers P J, Shachar-Hill Y. Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature, 2005, 435(7043): 819–823

[85] Wipf D, Krajinski F, van Tuinen D, Recorbet G, Courty P E. Trading on the arbuscular mycorrhiza market: from arbuscules to common mycorrhizal networks. New Phytologist, 2019, 223(3): 1127–1142

[86] Guether M, Balestrini R, Hannah M, He J, Udvardi M K, Bonfante P. Genome-wide reprogramming of regulatory networks, transport, cell wall and membrane biogenesis during arbuscular mycorrhizal symbiosis in Lotus japonicus. New Phytologist, 2009, 182(1): 200–212

[87] Handa Y, Nishide H, Takeda N, Suzuki Y, Kawaguchi M, Saito K. RNA-seq transcriptional profiling of an arbuscular mycorrhiza provides insights into regulated and coordinated gene expression in Lotus japonicus and Rhizophagus irregularis. Plant & Cell Physiology, 2015, 56(8): 1490–1511

[88] Sugimura Y, Saito K. Comparative transcriptome analysis between Solanum lycopersicum L. and Lotus japonicus L. during arbuscular mycorrhizal development. Soil Science and Plant Nutrition, 2017, 63(2): 127–136

[89] Liu J, Liu J, Liu J, Cui M, Huang Y, Tian Y, Chen A, Xu G. The potassium transporter SlHAK10 is involved in mycorrhizal potassium uptake. Plant Physiology, 2019, 180(1): 465–479

[90] Nouri E, Breuillin-Sessoms F, Feller U, Reinhardt D. Phosphorus and nitrogen regulate arbuscular mycorrhizal symbiosis in Petunia hybrida. PLoS One, 2014, 9(6): e90841

[91] Breuillin F, Schramm J, Hajirezaei M, Ahkami A, Favre P, Druege U, Hause B, Bucher M, Kretzschmar T, Bossolini E, Kuhlemeier C, Martinoia E, Franken P, Scholz U, Reinhardt D. Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning. Plant Journal, 2010, 64(6): 1002–1017

[92] Blanke V, Renker C, Wagner M, Füllner K, Held M, Kuhn A J, Buscot F. Nitrogen supply affects arbuscular mycorrhizal colonization of Artemisia vulgaris in a phosphate-polluted field site. New Phytologist, 2005, 166(3): 981–992

[93] Breuillin-Sessoms F, Floss D S, Gomez S K, Pumplin N, Ding Y, Levesque-Tremblay V, Noar R D, Daniels D A, Bravo A, Eaglesham J B, Benedito V A, Udvardi M K, Harrison M J. Suppression of arbuscule degeneration in Medicago truncatula phosphate transporter4 mutants is dependent on the ammonium transporter 2 family protein AMT2;3. Plant Cell, 2015, 27(4): 1352–1366

[94] Dong J, Ma G, Sui L, Wei M, Satheesh V, Zhang R, Ge S, Li J, Zhang T E, Wittwer C, Jessen H J, Zhang H, An G Y, Chao D Y, Liu D, Lei M. Inositol pyrophosphate InsP8 acts as an intracellular phosphate signal in Arabidopsis. Molecular Plant, 2019, 12(11): 1463–1473

[95] Ho C H, Lin S H, Hu H C, Tsay Y F. CHL1 functions as a nitrate sensor in plants. Cell, 2009, 138(6): 1184–1194

[96] Liu K H, Huang C Y, Tsay Y F. CHL1 is a dual-affinity nitrate transporter of Arabidopsis involved in multiple phases of nitrate uptake. Plant Cell, 1999, 11(5): 865–874

[97] Tsay Y F, Schroeder J I, Feldmann K A, Crawford N M. The herbicide sensitivity gene CHL1 of Arabidopsis encodes a nitrate-inducible nitrate transporter. Cell, 1993, 72(5): 705–713

[98] Garcia K, Chasman D, Roy S, Ané J M. Physiological responses and gene co-expression network of mycorrhizal roots under K⁺ deprivation. Plant Physiology, 2017, 173(3): 1811–1823

[99] Briat J F, Rouached H, Tissot N, Gaymard F, Dubos C. Integration of P, S, Fe, and Zn nutrition signals in Arabidopsis thaliana: potential involvement of PHOSPHATE STARVATION RESPONSE 1 (PHR1). Frontiers of Plant Science, 2015, 6: 290

[100] Xie X, Hu W, Fan X, Chen H, Tang M. Interactions between phosphorus, zinc, and iron homeostasis in nonmycorrhizal and mycorrhizal plants. Frontiers of Plant Science, 2019, 10: 1172

[101] Hirakawa Y, Sawa S. Diverse function of plant peptide hormones in local signaling and development. Current Opinion in Plant Biology, 2019, 51: 81–87

[102] de Bang T C, Lundquist P K, Dai X, Boschiero C, Zhuang Z, Pant P, Torres-Jerez I, Roy S, Nogales J, Veerappan V, Dickstein R, Udvardi M K, Zhao P X, Scheible W R. Genome-wide identification of Medicago peptides involved in macronutrient responses and nodulation. Plant Physiology, 2017, 175(4): 1669–1689

[103] Mortier V, Den Herder G, Whitford R, Van de Velde W, Rombauts S, D’Haeseleer K, Holsters M, Goormachtig S. CLE peptides control Medicago truncatula nodulation locally and systemically. Plant Physiology, 2010, 153(1): 222–237

[104] Tsikou D, Yan Z, Holt D B, Abel N B, Reid D E, Madsen L H, Bhasin H, Sexauer M, Stougaard J, Markmann K. Systemic control of legume susceptibility to rhizobial infection by a mobile microRNA. Science, 2018, 362(6411): 233–236

[105] Sasaki T, Suzaki T, Soyano T, Kojima M, Sakakibara H, Kawaguchi M. Shoot-derived cytokinins systemically regulate root nodulation. Nature Communications, 2014, 5(1): 4983

[106] Morandi D, Sagan M, Prado-Vivant E, Duc G. Influence of genes determining supernodulation on root colonization by the mycorrhizal fungus Glomus mosseae in Pisum sativum and Medicago truncatula mutants. Mycorrhiza, 2000, 10(1): 37–42

[107] Solaiman M Z, Senoo K, Kawaguchi M, Imaizumi-Anraku H, Akao S, Tanaka A, Obata H. Characterization of mycorrhizas fglomus sp. on roots of hypernodulating mutants of Lotus japonicus. Journal of Plant Research, 2000, 113(4): 443–448

[108] Sakamoto K, Nohara Y. Soybean (Glycine max [L.] Merr.) shoots systemically control arbuscule formation in mycorrhizal symbiosis. Soil Science and Plant Nutrition, 2009, 55(2): 252–257

[109] Müller L M, Flokova K, Schnabel E, Sun X, Fei Z, Frugoli J, Bouwmeester H J, Harrison M J. A CLE-SUNN module regulates strigolactone content and fungal colonization in arbuscular mycorrhiza. Nature Plants, 2019, 5(9): 933–939

[110] Le Marquer M, Bécard G, Frei Dit Frey N. Arbuscular mycorrhizal fungi possess a CLAVATA3/embryo surrounding region-related gene that positively regulates symbiosis. New Phytologist, 2019, 222(2): 1030–1042

[111] Vorholt J A, Vogel C, Carlström C I, Müller D B. Establishing causality: opportunities of synthetic communities for plant microbiome research. Cell Host & Microbe, 2017, 22(2): 142–155

[112] Thiergart T, Zgadzaj R, Bozsóki Z, Garrido-Oter R, Radutoiu S, Schulze-Lefert P. Lotus japonicus symbiosis genes impact microbial interactions between symbionts and multikingdom commensal communities. mBio, 2019, 10(5): e01833-19

[113] Xue L, Almario J, Fabiańska I, Saridis G, Bucher M. Dysfunction in the arbuscular mycorrhizal symbiosis has consistent but small effects on the establishment of the fungal microbiota in Lotus japonicus. New Phytologist, 2019, 224(1): 409–420

[114] Wang E, Schornack S, Marsh J F, Gobbato E, Schwessinger B, Eastmond P, Schultze M, Kamoun S, Oldroyd G E D. A common signaling process that promotes mycorrhizal and oomycete colonization of plants. Current Biology, 2012, 22(23): 2242–2246

[115] Banhara A, Ding Y, Kühner R, Zuccaro A, Parniske M. Colonization of root cells and plant growth promotion by Piriformospora indica occurs independently of plant common symbiosis genes. Frontiers of Plant Science, 2015, 6: 667

[116] Huisman R, Bouwmeester K, Brattinga M, Govers F, Bisseling T, Limpens E. Haustorium formation in Medicago truncatula roots infected by Phytophthora palmivora does not involve the common endosymbiotic program shared by arbuscular mycorrhizal fungi and rhizobia. Molecular Plant-Microbe Interactions, 2015, 28(12): 1271–1280

[117] Rey T, Chatterjee A, Buttay M, Toulotte J, Schornack S. Medicago truncatula symbiosis mutants affected in the interaction with a biotrophic root pathogen. New Phytologist, 2015, 206(2): 497–500

[118] Wang X L, Wang M X, Xie X G, Guo S Y, Zhou Y, Zhang X B, Yu N, Wang E T. An amplification-selection model for quantified rhizosphere microbiota assembly. Science Bulletin, 2020, 65(12): 983–986

[119] Fabiańska I, Gerlach N, Almario J, Bucher M. Plant-mediated effects of soil phosphorus on the root-associated fungal microbiota in Arabidopsis thaliana. New Phytologist, 2019, 221(4): 2123–2137

[120] López-Ráez J A, Shirasu K, Foo E. Strigolactones in plant interactions with beneficial and detrimental organisms: the Yin and Yang. Trends in Plant Science, 2017, 22(6): 527–537

[121] Fabiańska I, Sosa-Lopez E, Bucher M. The role of nutrient balance in shaping plant root-fungal interactions: facts and speculation. Current Opinion in Microbiology, 2019, 49: 90–96

[122] Castrillo G, Teixeira P J P L, Paredes S H, Law T F, de Lorenzo L, Feltcher M E, Finkel O M, Breakfield N W, Mieczkowski P, Jones C D, Paz-Ares J, Dangl J L. Root microbiota drive direct integration of phosphate stress and immunity. Nature, 2017, 543(7646): 513–518

[123] Almario J, Jeena G, Wunder J, Langen G, Zuccaro A, Coupland G, Bucher M. Root-associated fungal microbiota of nonmycorrhizal Arabis alpina and its contribution to plant phosphorus nutrition. Proceedings of the National Academy of Sciences of the United States of America, 2017, 114(44): E9403–E9412

[124] Hiruma K, Gerlach N, Sacristán S, Nakano R T, Hacquard S, Kracher B, Neumann U, Ramírez D, Bucher M, O’Connell R J, Schulze-Lefert P. Root endophyte Colletotrichum tofieldiae confers plant fitness benefits that are phosphate status dependent. Cell, 2016, 165(2): 464–474

[125] Bakshi M, Vahabi K, Bhattacharya S, Sherameti I, Varma A, Yeh K W, Baldwin I, Johri A K, Oelmüller R. WRKY6 restricts Piriformospora indica-stimulated and phosphate-induced root development in Arabidopsis. BMC Plant Biology, 2015, 15(1): 305

[126] Frey-Klett P, Garbaye J, Tarkka M. The mycorrhiza helper bacteria revisited. New Phytologist, 2007, 176(1): 22–36

[127] Salvioli A, Ghignone S, Novero M, Navazio L, Venice F, Bagnaresi P, Bonfante P. Symbiosis with an endobacterium increases the fitness of a mycorrhizal fungus, raising its bioenergetic potential. ISME Journal, 2016, 10(1): 130–144

Acknowledgements

We thank Ke Yu (Henan University, China) and Qiujin Xie (CAS Center for Excellence in Molecular Plant Sciences, China) for comments on the manuscript. This work was supported by the National Natural Science Foundation of China (31730103, 31825003 and 31970268). We apologize that it was not possible to cite all the work of our colleagues.

Compliance with ethics guidelines

Xue Li and Ertao Wang declare that they have no conflicts of interest or financial conflicts to disclose.

This article does not contain any studies with human or animal subjects performed by any of the authors.

RIGHTS & PERMISSIONS

The Author(s) 2020. Published by Higher Education Press. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0)