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ScienceDirect Plant carbon nourishment of arbuscular mycorrhizal fungi Ronelle Roth and Uta Paszkowski Reciprocal nutrient exchange between the majority of land plants and arbucular mycorrhizal (AM) fungi is the cornerstone of a stable symbiosis. To date, a dogma in the comprehension of AM fungal nourishment has been delivery of host organic carbon in the form of sugars. More recently a role for lipids as alternative carbon source or as a signalling molecule during AM symbiosis was proposed. Here we review the symbiotic requirement for carbohydrates and lipids across developmental stages of the AM symbiosis. We present a role for carbohydrate metabolism and signalling to maintain intraradical fungal growth, as opposed to lipid uptake at the arbuscule as an indispensible requirement for completion of the AM fungal life cycle.
nutrients. Concomitantly, fungal growth also extends into the soil where large extraradical mycelia (ERM) develop that are involved in the uptake of minerals and the generation of spores.
Edited by Tzyy-Jen Chiou and Toru Fujiwara
In the absence of a host, AM fungal spores contain sufficient resources to support modest hyphal growth, whereas plant derived organic carbon (C) is thought to fuel intense fungal proliferation and spore formation . Sugars as the key symbiotic C currency transferred from plant to fungus was suggested over 40 years ago . Indeed, intraradical hyphal (IH) uptake of C in the form of hexoses, particularly glucose, was later confirmed by in vivo NMR spectroscopy, radiorespirometry and stable isotope labelling [4–6]. Once acquired by IRM, hexoses can be converted into glycogen and lipids for long distance transport and storage in vesicles and spores inside and outside mycorrhizal roots, respectively. An emerging body of evidence more recently proposes fatty acids (FA) as an additional form of plant-delivered C [7,8,38]. Here, we review knowledge on fungal carbon requirements across the developmental stages of the symbiosis and propose that uptake of FA at the arbuscules is required for the completion of the fungal life-cycle.
A role for carbohydrates in sustaining fungal growth during AM symbiosis
Address Department of Plant Sciences, Downing Street, Cambridge CB2 3EA, United Kingdom Corresponding author: Paszkowski, Uta ([email protected]
Current Opinion in Plant Biology 2017, 39:50–56 This review comes from a themed issue on Cell signalling and gene regulation
1369-5266/Crown Copyright ã 2017 Published by Elsevier Ltd. All rights reserved.
Introduction The symbiotic success in arbuscular mycorrhizal (AM) symbioses for over 400 million years has involved host– fungal transactions, underpinned by a tightly regulated reciprocal nutrient exchange based on mutual rewards. For AM fungi, forming a successful symbiosis with plants is an obligate requirement to complete their life-cycle, manifested by the production of daughter spores . During the association, extensive hyphal growth occurs in the intercellular space of root epidermis and cortex tissue (intraradical mycelia, IRM), accompanied by the development of highly branched haustoria, the arbuscules, inside cortex cells. Arbuscules form by dichotomous hyphal branching while invaginating the cortex cell membrane. On a micrometer scale, an enormous symbiotic interface is created for the exchange of signals and Current Opinion in Plant Biology 2017, 39:50–56
AM fungi acquire sugar in the form of hexoses, predominantly glucose [6,9,10]. The first sugar transporter reported from a glomeromycotan fungus was the monosaccharide transporter from Geosiphon pyriformis, GpMST1, which engages in symbiosis with the cyanobacterium Nostoc punctiforme . The genome of Rhizophagus irregularis (formerly Glomus intraradices) contains related Monosaccharide Transporters (RiMSTs) with different spatial expression patterns and substrate specificity. While RiMST2 is highly expressed in planta, RiMST5 and RiMST6 transcripts accumulated preferentially in germinated spores (Figure 1, Table 1A, [12,13]). RiMST5 and RiMST6 are proton co-transporters with high specificity for glucose, indicating the possibility of glucose acquisition during spore germination . In contrast, RiMST2 has promiscuous substrate specificity for hexoses with preference for xylose and is present in extraradical mycelium (ERM), around IH and arbuscules during the interaction with potato and M. truncatula , indicating that sugar uptake in AM fungi might involve IH in addition to arbuscules, which is supported by earlier radiotracer-based observations (Figure 1, ). Furthermore, addition of xylose induced RiMST2 expression in www.sciencedirect.com
Plant carbon nourishment of arbuscular mycorrhizal fungi Roth and Paszkowski 51
Host Gene Expression Carbohydrates Lipids
Rhizodermis Exodermis Outer Cortex IH
RAM2 FatM STR1/STR2
Vasculature MST5/6 Glc
Sucrose Current Opinion in Plant Biology
Summary of fungal carbon nourishment during AM symbiosis. AM fungal colonization results in increased expression of source-to-sink metabolizing genes Sucrose Transporters (SUTs) and Sugars Will Eventually Be Exported Transporters (SWEETs) as well as genes encoding sucrose metabolizing enzymes Sucrose Synthase and Invertases. Fungal uptake of apoplastic hexoses are likely mediated by Monosaccharide Transporter2 (MST2) that is induced around intra-radical hyphae (IH) and arbuscules. Upregulation of MST5/6 in spores and extra-radical mycelia (ERM) suggest that AM fungi may also be able to take up glucose (Glc) from their surrounding. AM-conserved genes, RAM2 and FatM are induced in arbuscule-containing cells and are required for synthesis of the C16:0 fatty acid, b-monoacylglycerol (b-MAG). ABC transporters STR1/STR2 that localize to the peri-arbuscular membrane (PAM) might play a role in the transport of b-MAG into the symbiotic interface from where it is taken up by the fungus and utilized for arbuscule formation.
ERM, and may therefore also represent the trigger for RiMST2 expression in planta . Consistently, fungal xylose reductase genes, required for xylose catabolism, were induced during AM colonization. Functional analysis of RiMST2 by knocking down RiMST2 using hostinduced gene silencing (HIGS) led to severely compromised fungal colonisation and abnormal arbuscule morphology . This confirmed the importance of plant carbohydrates for the maintenance of IH and arbuscule
growth and moreover suggested cell wall monosaccharides as a source of organic C for AM fungi. During fungal colonisation of roots, an increased sourceto-sink flux occurs through redirection of sucrose from leaves to roots. Sucrose in- and efflux, monosaccharide uptake, or also sucrose cleaving Sucrose Synthase (SucS) and cell wall Invertases (cwInv) all regulate aspects of sugar partitioning. It is well established that distinct
Table 1A Fungal carbohydrate transporters induced during AM symbiosis Fungal carbohydrate transporters induced during AM symbiosis
IH and arbucules 
HIGS KD 
Spores and ERM 
AM symbiosis phenotype: quantitative Reduced colonization compared to WT n.d.
Mutant phenotype: arbuscule
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52 Cell signalling and gene regulation
members of gene families encoding these proteins are differentially regulated in response to mycorrhizal colonization, frequently being transcriptionally induced not only in but also next to arbuscule-containing cortex cells and furthermore adjacent to intraradical hyphae [14,15–18] (Figure 1, Table 1B, for recent review see Refs. [14,15–18]). A large body of literature documents their tight spatio-temporal control, and indicates a finely tuned activation of sink metabolism in plant cells surrounding hyphal structures. Interestingly, most of the characterized sugar transporters mediate uptake, possibly reflecting a certain degree of plant-fungal competition for sugars in colonized areas of the root. In contrast, members of the SWEET (Sugars Will Eventually be Exported Transporter) proteins are involved in monosaccharide or disaccharide export or import and can be targets of microbial effectors that redirect sugar fluxes towards the invader (reviewed in Ref. ). Promoters of genes encoding distinct members of potato SWEETs were recently shown to be active within and next to arbuscule-hosting cells (Figure 1, Table 1B, ). In mycorrhizal roots, SWEET activity may lead to the release of sugars into the interface between the plant and the fungal membrane (the peri-arbuscular space, PAS) and thereby fine-tune sugar fluxes and availability in colonized and adjacent non-colonized cortex cells. Although comprehensive functional analyses of the SWEET genes are required to confirm their function
during AM symbiosis their expression pattern is consistent with contributing to sustained fungal growth inside the host root.
Regulating AM symbiosis development by linking carbohydrate metabolism with signalling It is conceivable that the higher sink strength of mycorrhizal roots leads to sugar availability becoming a limiting factor for symbiosis development. However, the increased availability of hexoses due to overexpression of invertases in tobacco or M. truncatula did not yield increased fungal colonization levels, thereby arguing against a shortage of carbohydrates under normal growth conditions . However, reducing acid invertase activity or interfering with phloem loading caused a significant reduction in fungal colonization, demonstrating that below a critical threshold of available sugars fungal abundance was affected . Conversely, knockdown of the tomato sucrose transporter SUT2, but not SUT1 or SUT4, led to increased mycorrhizal colonization and abolished the positive growth response to AMS in tomato, intuitively pointing towards a fungal advantage in the competition for carbohydrates in the absence of functional SUT2 (Figure 1, Table 1B, ). However, although SUT2 is regulated by sucrose, predominantly in sink tissue, direct sucrose transport activity could not be confirmed but instead SUT2 shares features with yeast sugar sensors . Co-localization
Table 1B Plant genes involved in sugar partitioning and induced in AM symbiosis Plant gene name MtSucS1
LeLin6/ Invertases SlSWEETs
Gene expression Upregulated in vasculature, cortex cells surrounding IH and arbuscules  Induced  Upregulated in vasculature, cortex cells containing IH and arbuscules  Induced  Upregulated in vasculature, cortex cells containing IH and arbuscules  Upregulated in cortex cells containing IH and arbuscules; Protein localizes to PM and PAM  Upregulated in cortex cells containing IH and arbuscules  Induced 
Mutant phenotype: quantitative
Mutant phenotype: arbuscule
Anti-sense KD 
Reduced colonization compared to WT
Enzyme Activity Inhibited 
Reduced colonization compared to WT
Anti-sense KD  Anti-sense KD 
Anti-sense KD 
Increased colonization compared to WT
 Baier et al., Plant Physiology 2010, 152:1000–1014.  Harrison Plant Journal 1996, 9:491–503.
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Plant carbon nourishment of arbuscular mycorrhizal fungi Roth and Paszkowski 53
experiments suggested SUT2 might regulate tissue sucrose fluxes by a combination of sensing sucrose and modulating the activity of other high and low affinity sucrose transporters . In Funneliformis mosseae colonized tomato roots, SUT2 localized to both the plasma membrane (PM) and the peri-arbuscular membrane (PAM) and was shown to physically interact with components of brassinosteroid (BR) biosynthesis and signalling, namely a BRI1-Associated receptor Kinase (BAK1)-like receptor kinase, a membrane steroid-binding protein (MSBP) and the BR biosynthetic sterol reductase DIMINUTO/DWARF . Consistent with a role of BR signalling in AM symbiosis, mutation of either M. truncatula MSPB or tomato and rice DIMINUTO resulted in reduced AM fungal colonization [22,24,25]. A plausible scenario is therefore that SUT2 function directly or indirectly negatively regulates fungal expansion, a constraint which is removed by BR signalling . Induced expression of source-sink components, cwInv, SUTs and SWEETS during AM symbiosis also occurs in response to plant pathogens (reviewed in Ref. ). Thus profound modification of source-sink relationships may additionally provoke the activation of host defence signalling and thus regulation during AM symbiosis [26,27]. For some pathogens such as the obligate biotrophic fungus Erysiphe cichoracearum upregulation of hexoses in the host apoplast represents a valuable source of energy allowing for enhanced pathogen growth and reproduction . Sugar transporters of the SWEET family that function as facilitators of sugar efflux have similarly been targeted by pathogens to acquire sugars for their own growth . Interestingly the Arabidopsis homologue of the AM-induced M. truncatula Hexose 1 transporter (MtHex1), AtSTP13, is also induced during plant-pathogen interactions, and important in basal plant resistance . AtSTP13 interacts with both the pattern recognition receptor (PRR) flagellin-sensing 2 (FLS2) and its coreceptor BAK1 upon ligand binding (flg22), resulting in an increased hexose uptake from the apoplast . Upregulation of MtHex1 during AM colonization raises the intriguing possibility that similar sugar signalling mechanisms, operating through PRR complexes such as e.g. chitin-receptors [32,33], may be functionally relevant during AM symbiosis.
AM fungi are fatty acid heterotrophs As oleaginous organisms AM fungal hyphae accumulate most of their dry weight as lipids, stored in extraradical spores and intraradical vesicles from where they can be used as an energy source to sustain anabolism during spore germination (reviewed in Ref. ). Mass spectrometry based membrane lipid profiling of R. irregularis confirmed that lipids in ERM consist predominantly of triacylglycerol (TAG, >90%), containing 16:0 (palmitic acid) and 16:1v5 (palmitvaccenic acid) acyl groups . In fungi, cytosolic multi-domain fatty acid (FA) synthases www.sciencedirect.com
(Type I FAS) catalyse the de novo synthesis of FAs. Surprisingly, the genome of both R. irregularis and Gigaspora rosea lack genes encoding Type I FAS [7,35,36]. Nevertheless, the enzymatic machinery for the full FA desaturation and elongation pathway is present in R. irregularis and corresponding transcripts are upregulated in IRM ; hence substrate availability correlated with intraradical fungal structures and suggested that AM fungi acquire FA from their hosts. Indeed, a recent phylogenomics approach in M. truncatula identified 12 lipid biosynthesis genes that are only present in host plants of AM fungi, thereby possibly reflecting the specific evolutionary adaptation of the symbiotic system to FA requirements . Among these, the acyl-ACP thioesterase (FatM, Fat required for AM symbiosis) is specifically induced in arbuscule-containing cells . Importantly, mutation of FatM led to significantly reduced levels of AM fungal colonization and collapsed arbuscular fine branches [37,38]. FatM belongs to a gene family that includes three additional Fat genes, FatA, FatB and FatC in Medicago, which show partial overlap in their in vitro biochemical activities including their ability to hydrolyze C16:0-ACP . Consequently, all three Fat genes could to some extend restore arbuscule morphology when expressed in fatm mutants, however, none of them was upregulated during AM symbiosis. FatM function however, appeared to be the result of timing and heightened expression culminating in the increased release of C16:0 free fatty acids from plastids during AM symbiosis (Figure 1, ). This points to a fungal requirement of FatM for arbuscule development or for supplying lipids building the PAM . In addition to FatM, the earlier reported Reduced Arbuscular Mycorrhization 2 (RAM2) also belongs to the phylogenetically conserved AM-specific genes . RAM2 encodes a sn-2 glycerol-3-phosphate acyltransferases (sn2-GPAT), homologous to GPAT6 in A. thaliana that incorporates modified acyl groups into glycerol-3-phosphate (G3P) to generate cutin monomers and, via its phosphatase activity, also removes phosphate groups from lysophosphatidic acid (LPA) to generate sn-2 monoacylglycerol (b-MAG) (Yang et al 2012 Pl Ph, Yang et al 2010 PNAS). RAM2 was specifically induced in arbusculecontaining cells of M. truncatula and ram2 mutants displayed a strong morphological arbuscule phenotype resembling that of fatm mutants (Figure 1, ). Based on related lipid profiles of fatm and ram2, it was proposed that induced FatM expression during AM symbiosis results in an increase in 16:0 FA synthesis in plastids, which RAM2 inside the endoplasmic reticulum converts into 16:0 b–MAG . Cellular export of FAs is mediated by homodimerizing or heterodimerizing half-size ATP-binding cassette (ABC) Current Opinion in Plant Biology 2017, 39:50–56
54 Cell signalling and gene regulation
transporters of the ABCG clade . Specific to mycorrhizal plant species are two ABCG transporters STR1/STR2 that specifically reside and interact within the PAM . Interestingly, mutation of either gene yielded defective arbuscules that closely resemble that of fatm and ram2 mutants suggesting that STR1/STR2 could be required for FA transport across the PAM (Figure 1, [40,41]). However, lipid profiling showed reduced 16:0 b–MAG in fatm and ram2 relative to WT but not in str where 16:0 b–MAG levels were comparable to that of WT despite decreased FatM and RAM2 transcript levels . Although to date, the substrate(s) for STR1/STR2 remain unknown, the overlapping phenotypes of str1/str2, ram2 and fatm in M. truncatula together with lipid profiling speak in collective favour of a link between arbuscule development, lipid biosynthesis, and an involvement of STR1/STR2 in delivering FAs across PAM and into the symbiotic interface.
FA uptake at the arbuscule correlates with fungal completion of life cycle The correlation between arbuscule and spore formation  suggested that functional arbuscules are an essential requirement for completion of the fungal life cycle. Arbuscule development requires the DELLA type of GRAS transcription factors as M. truncatula della1/della2 mutants completely lack arbuscules . Interestingly, despite the absence of arbuscules della1/della2 mutants support significant IH growth within the root cortex, suggesting that IH growth in della1/della2 mutants was sustained by hyphal uptake of carbohydrates which may even be available at increased levels due to derepressed GA signalling . The signalling mechanisms underpinning arbuscule development are complex and beyond the scope of this article. Interestingly however, in contrast to DELLA, the GRAS protein RAM1 represents an AM-specific transcription factor that interacts with DELLA and additional GRAS proteins in a complex and is central for arbuscule development in M. truncatula, L. japonicus and petunia, once again reflecting functional conservation across phylogenetically distant mycorrhizal plant species (Figure 1, [43,44–46]). It is noteworthy that the different mutant phenotypes share the commonality that the fungus is able to continue intraradical spreading despite a lack of vesicle and spore production. These observations support a hypothesis whereby carbohydrate uptake promote intraradical fungal proliferation, however, for completion of the fungal life cycle alternative C sources such as FAs are required that are essential for arbuscule development. Importantly, RAM1 is strictly necessary for the activation of RAM2 and Str1/Str2 gene expression, and in M. truncatula overexpression of RAM1 in the absence of the fungus resulted in the upregulation of RAM2 and Str/ Str2 transcripts , thus pointing to RAM1 as the Current Opinion in Plant Biology 2017, 39:50–56
master regulator of arbuscule development, possibly by modulating lipid biosynthesis and allocation.
Concluding remarks Our understanding of AM fungal nourishment has progressed immensely since the first observations of sugar uptake by AM fungi. Although a large body of evidence supports altered carbohydrate flux during AM symbiosis, how AM fungi manipulate sugar flux during AM symbiosis remains an open question. Exciting new insights have emerged for the nourishing and possible signalling role of fatty acids for arbuscule development and for the completion of the AM fungal life cycle with production of spores and vesicles. Future labelling experiments should confirm transfer of FAs by STR/STR2 across the PAM and confirm the identity of lipids taken up by the fungus. Recent phylogenomic analyses have identified a plethora of novel candidates involved in lipid biosynthesis and metabolism. Uncovering their function and regulation during AM symbiosis will unleash new insights into organic C nurture of AM fungi and into ancient host-fungal transactions that drive AM symbiosis.
Acknowledgements Ronelle Roth is supported by the BBSRC grant BB/N008723/1 to Uta Paszkowski.
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