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Many plants associate with arbuscular mycorrhizal fungi for nutrient acquisition, while legumes also associate with nitrogen-fixing rhizobial bacteria. Both associations rely on symbiosis signaling and here we show that cereals can perceive lipochitooligosaccharides (LCOs) for activation of symbiosis signaling, surprisingly including Nod factors produced by nitrogen-fixing bacteria. However, legumes show stringent perception of specifically decorated LCOs, that is absent in cereals. LCO perception in plants is activated by nutrient starvation, through transcriptional regulation of Nodulation Signaling Pathway (NSP)1 and NSP2. These transcription factors induce expression of an LCO receptor and act through the control of strigolactone biosynthesis and the karrikin-like receptor DWARF14-LIKE. We conclude that LCO production and perception is coordinately regulated by nutrient starvation to promote engagement with mycorrhizal fungi. Our work has implications for the use of both mycorrhizal and rhizobial associations for sustainable productivity in cereals.

Root systems regulate their branching patterns in response to environmental stimuli. Lateral root development in both monocotyledons and dicotyledons is enhanced in response to inoculation with arbuscular mycorrhizal (AM) fungi, which has been interpreted as a developmental response to specific, symbiosis-activating chitinaceous signals. Here, we report that generic instead of symbiosis-specific, chitin-derived molecules trigger lateral root formation. We demonstrate that this developmental response requires the well-known microbe-associated molecular pattern (MAMP) receptor, Chitin Elicitor Receptor Kinase 1 (CERK1), in rice, Medicago truncatula, and Lotus japonicus, as well as the non-host of AM fungi, Arabidopsis thaliana, lending further support for a broadly conserved signal transduction mechanism across angiosperms. Using rice mutants impaired in strigolactone biosynthesis and signaling, we show that strigolactone signaling is necessary to regulate this developmental response. Rice CERK1 operates together with either Chitin Elicitor Binding Protein (CEBiP) or Nod Factor Receptor 5 (NFR5) in immunity and symbiosis signaling, respectively; for the lateral root response, however, all three LysM receptors are required. Our work, therefore, reveals an overlooked but a conserved role of LysM receptors integrating MAMP perception with developmental responses in plants, an ability that might influence the interaction between roots and the rhizosphere biota.

Receptor-like kinases (RLKs) are key cell signaling components. The rice ARBUSCULAR RECEPTOR-LIKE KINASE 1 (OsARK1) regulates the arbuscular mycorrhizal (AM) association postarbuscule development and belongs to an undefined subfamily of RLKs. Our phylogenetic analysis revealed that ARK1 has an ancient paralogue in spermatophytes, ARK2 . Single ark2 and ark1/ark2 double mutants in rice showed a nonredundant AM symbiotic function for OsARK2 . Global transcriptomics identified a set of genes coregulated by the two RLKs, suggesting that OsARK1 and OsARK2 orchestrate symbiosis in a common pathway. ARK lineage proteins harbor a newly identified SPARK domain in their extracellular regions, which underwent parallel losses in ARK1 and ARK2 in monocots. This protein domain has ancient origins in streptophyte algae and defines additional overlooked groups of putative cell surface receptors.

Arbuscular mycorrhizal fungi (AMF) are ubiquitous in cultivated soils, forming symbiotic relationships with the roots of major crop species. Studies in controlled conditions have demonstrated the potential of AMF to enhance the growth of host plants. However, it is difficult to estimate the actual benefit in the field, not least because of the lack of suitable AMF-free controls. Here we implement a novel strategy using the selective incorporation of AMF-resistance into a genetic mapping population to evaluate maize response to AMF. We found AMF to account for about one-third of the grain production in a medium input field, as well as to affect the relative performance of different plant genotypes. Characterization of the genetic architecture of the host response indicated a trade-off between mycorrhizal dependence and benefit. We identified several QTL linked to host benefit, supporting the feasibility of breeding crops to maximize profit from symbiosis with AMF.

During establishment of arbuscular mycorrhizal symbioses, fungal hyphae invade root cells producing transient tree-like structures, the arbuscules, where exchange of photosynthates for soil minerals occurs. Arbuscule formation and collapse lead to rapid production and degradation of plant and fungal membranes, their spatiotemporal dynamics directly influencing nutrient exchange. We determined the ultra-structural details of both membrane surfaces and the interstitial apoplastic matrix by transmission electron microscopy tomography during growth and senescence of Rhizophagus irregularis arbuscules in rice. Invasive growth of arbuscular hyphae was associated with abundant fungal membrane tubules (memtubs) and plant peri-arbuscular membrane evaginations. Similarly, the phylogenetically distant arbuscular mycorrhizal fungus, Gigaspora rosea, and the fungal maize pathogen, Ustilago maydis, developed memtubs while invading host cells, revealing structural commonalities independent of the mutualistic or parasitic outcome of the interaction. Additionally, extracellular vesicles formed continuously in the peri-arbuscular interface from arbuscule biogenesis to senescence, suggesting an involvement in inter-organismic signal and nutrient exchange throughout the arbuscule lifespan. The symbiosis of mycorrhizal fungi and roots involves invasion of plant cells, followed by collapse of the intracellular fungal arbuscules. Ultra-structural details of this interaction show continuous formation of extracellular vesicles at the peri-arbuscular space.

Most plants associate with beneficial arbuscular mycorrhizal (AM) fungi that facilitate soil nutrient acquisition. Prior to contact, partner recognition triggers reciprocal genetic remodelling to enable colonisation. The plant Dwarf14-Like (D14L) receptor conditions pre-symbiotic perception of AM fungi, and also detects the smoke constituent karrikin. D14L-dependent signalling mechanisms, underpinning AM symbiosis are unknown. Here, we present the identification of a negative regulator from rice, which operates downstream of the D14L receptor, corresponding to the homologue of the Arabidopsis thaliana Suppressor of MAX2-1 (AtSMAX1) that functions in karrikin signalling. We demonstrate that rice SMAX1 is a suppressor of AM symbiosis, negatively regulating fungal colonisation and transcription of crucial signalling components and conserved symbiosis genes. Similarly, rice SMAX1 negatively controls strigolactone biosynthesis, demonstrating an unexpected crosstalk between the strigolactone and karrikin signalling pathways. We conclude that removal of SMAX1, resulting from D14L signalling activation, de-represses essential symbiotic programmes and increases strigolactone hormone production.

Most land plants engage in mutually beneficial interactions with arbuscular mycorrhizal (AM) fungi, the fungus providing phosphate and nitrogen in exchange for fixed carbon. During presymbiosis, both organisms communicate via oligosaccharides and butenolides. The requirement for a rice chitin receptor in symbiosis-induced lateral root development suggests that cell division programs operate in inner root tissues during both AM and nodule symbioses. Furthermore, the identification of transcription factors underpinning arbuscule development and degeneration reemphasized the plant's regulatory dominance in AM symbiosis. Finally, the finding that AM fungi, as lipid auxotrophs, depend on plant fatty acids (FAs) to complete their asexual life cycle revealed the basis for fungal biotrophy. Intriguingly, lipid metabolism is also central for asexual reproduction and interaction of the fungal sister clade, the Mucoromycotina, with endobacteria, indicative of an evolutionarily ancient role for lipids in fungal mutualism.

Arbuscular mycorrhizal symbiosis is an ancient interaction between plants and fungi of the phylum Glomeromycota. In exchange for photosynthetically fixed carbon, the fungus provides the plant host with greater access to soil nutrients via an extensive network of root-external hyphae. Here, to determine the impact of the symbiosis on the host ionome, the concentration of 19 elements was determined in the roots and leaves of a panel of 30 maize varieties, grown under phosphorus-limiting conditions, with or without inoculation with the fungus Funneliformis mosseae. Although the most recognized benefit of the symbiosis to the host plant is greater access to soil phosphorus, the concentration of a number of other elements responded significantly to inoculation across the panel as a whole. In addition, variety-specific effects indicated the importance of plant genotype to the response. Clusters of elements were identified that varied in a co-ordinated manner across genotypes, and that were maintained between non-inoculated and inoculated plants.

Phosphorous is important for life but often limiting for plants. The symbiotic pathway of phosphate uptake via arbuscular mycorrhizal fungi (AMF) is evolutionarily ancient and today occurs in natural and agricultural ecosystems alike. Plants capable of this symbiosis can obtain up to all of the phosphate from symbiotic fungi, and this offers potential means to develop crops less dependent on unsustainable P fertilizers. Here, we review the mechanisms and insights gleaned from the fine-tuned signal exchanges that orchestrate the intimate mutualistic symbiosis between plants and AMF. As the currency of trade, nutrients have signaling functions beyond being the nutritional goal of mutualism. We propose that such signaling roles and metabolic reprogramming may represent commitments for a mutualistic symbiosis that act across the stages of symbiosis development.

All plants need a nutrient called phosphorus to grow and thrive. Phosphorus is found in soil, but the supply is limited so plants often struggle to acquire enough of it. To overcome this problem, many plants form friendly relationships (or symbioses) with certain fungi in the soil known as arbuscular mycorrhizal fungi. The fungi colonize plant roots and supply phosphorus and other nutrients in return for sugars and various molecules. Although many crop plants – including barley and potatoes – are able to form these symbioses, farmers commonly apply fertilizers containing phosphate and other nutrients to their fields to increase the amount of food they produce. Breeding new crop varieties that are better at forming symbioses with the fungi could reduce the need for fertilizers. However, the methods currently available to study these relationships are laborious and time-consuming, typically requiring samples of plant roots to be examined in a laboratory. Wang, Schafer et al. used an approach called metabolomics to search for molecules in coyote tobacco plants that indicate the plants have formed symbioses with arbuscular mycorrhizal fungi. The experiments found that a group of molecules called blumenols accumulate in the roots and also in the shoots and leaves of plants with these symbioses, but not in the tobacco plants that were not able to associate with the fungi. Experiments in several other plant species including tomato, potato and barley produced similar findings, suggesting that the blumenols may be a useful and potentially universal indicator of symbioses between many different plants and fungi. Measuring the levels of blumenols in plant shoots and leaves is much quicker and easier than current methods of identifying fungal symbioses in plant root samples. Therefore, blumenols may be a useful tool for plant breeders who would like to screen large numbers of plants for these symbioses, and breed crops that negotiate better interactions with the beneficial fungi.

High concentrations of heavy metals (HM) in the soil have detrimental effects on ecosystems and are a risk to human health as they can enter the food chain via agricultural products or contaminated drinking water. Phytoremediation, a sustainable and inexpensive technology based on the removal of pollutants from the environment by plants, is becoming an increasingly important objective in plant research. However, as phytoremediation is a slow process, improvement of efficiency and thus increased stabilization or removal of HMs from soils is an important goal. Arbuscular mycorrhizal (AM) fungi provide an attractive system to advance plant-based environmental clean-up. During symbiotic interaction the hyphal network functionally extends the root system of their hosts. Thus, plants in symbiosis with AM fungi have the potential to take up HM from an enlarged soil volume. In this review, we summarize current knowledge about the contribution of the AM symbiosis to phytoremediation of heavy metals.

Early stages of a beneficial relationship Plants benefit from widespread symbiosis with arbuscular mycorrhizal fungi. This symbiosis between plant and fungus aids plants in capturing mineral and micronutrients from the soil. Gutjahr et al. have now identified a component of an intracellular receptor, the hydrolase DWARF 14 LIKE, required in rice roots for initiating the symbiosis. A similar receptor detects karrikins in smoke that signal opportunity for fireweed to grow after a forest fire. Science , this issue p. 1521

Contents Summary 1135 I. Introduction 1135 II. Recruitment of plant metabolites and hormones as signals in AM symbiosis 1136 III. Phytohormones are regulators of AM symbiosis and targets of plant breeding 1137 IV. Variation in host response to AM symbiosis 1137 V. Outlook 1137 Acknowledgements 1139 References 1139 SUMMARY: Cereals (rice, maize, wheat, sorghum and the millets) provide over 50% of the world's caloric intake, a value that rises to > 80% in developing countries. Since domestication, cereals have been under artificial selection, largely directed towards higher yield. Throughout this process, cereals have maintained their capacity to interact with arbuscular mycorrhizal (AM) fungi, beneficial symbionts that associate with the roots of most terrestrial plants. It has been hypothesized that the shift from the wild to cultivation, and above all the last c. 50 years of intensive breeding for high-input farming systems, has reduced the capacity of the major cereal crops to gain full benefit from AM interactions. Recent studies have shed further light on the molecular basis of establishment and functioning of AM symbiosis in cereals, providing insight into where the breeding process might have had an impact. Classic phytohormones, targets of artificial selection during the generation of Green Revolution semi-dwarf varieties, have emerged as important regulators of AM symbiosis. Although there is still much to be learnt about the mechanistic basis of variation in symbiotic outcome, these advances are providing an insight into the role of arbuscular mycorrhiza in agronomic systems.

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., Ronelle Roth is supported by the BBSRC grant BB/N008723/1 to Uta Paszkowski.

In recent years a number of legume genes involved in root nodule (RN) symbiosis have been identified in the model legumes, Lotus japonicus (Lotus) and Medicago truncatula. Among them, a distinct set of genes has been categorized as a common symbiosis pathway (CSP), because they are also essential for another mutual interaction, the arbuscular mycorrhiza (AM) symbiosis, which is evolutionarily older than the RN symbiosis and is widely distributed in the plant kingdom. Based on the concept that the legume RN symbiosis has evolved from the ancient AM symbiosis, one issue is whether the CSP is functionally conserved between non-nodulating plants, such as rice, and nodulating legumes. We identified three rice CSP gene orthologs, OsCASTOR, OsPOLLUX and OsCCaMK, and demonstrated the indispensable roles of OsPOLLUX and OsCCaMK in rice AM symbiosis. Interestingly, molecular transfection of either OsCASTOR or OsCCaMK could fully complement symbiosis defects in the corresponding Lotus mutant lines for both the AM and RN symbioses. Our results not only provide a conserved genetic basis for the AM symbiosis between rice and Lotus, but also indicate that the core of the CSP has been well conserved during the evolution of RN symbiosis. Through evolution, CASTOR and CCaMK have remained as the molecular basis for the maintenance of CSP functions in the two symbiosis systems.

Perception of arbuscular mycorrhizal fungi (AMF) triggers distinct plant signalling responses for parallel establishment of symbiosis and induction of lateral root formation. Rice receptor kinase CHITIN ELICITOR RECEPTOR KINASE 1 (CERK1) and α/β-fold hydrolase DWARF14-LIKE (D14L) are involved in pre-symbiotic fungal perception. After 6 wk post-inoculation with Rhizophagus irregularis, root developmental responses, fungal colonization and transcriptional responses were monitored in two independent cerk1 null mutants; a deletion mutant lacking D14L, and with D14L complemented as well as their respective wild-type cultivars (cv Nipponbare and Nihonmasari). Here we show that although essential for symbiosis, D14L is dispensable for AMF-induced root architectural modulation, which conversely relies on CERK1. Our results demonstrate uncoupling of symbiosis and the symbiotic root developmental signalling during pre-symbiosis with CERK1 required for AMF-induced root architectural changes., Leverhulme Early Career Fellowship. Grant Number: ECF‐2016‐392

The Arbuscular Mycorrhizal (AM) symbiosis is a ubiquitous relationship established in terrestrial ecosystems between the roots of most plants and fungi of the Glomeromycota. AM fungi occur amongst many other inhabitants of the soil, and successful development of AM symbioses relies on a pre-symbiotic signal exchange that allows mutual recognition and reprogramming for the anticipated physical interaction. The nature of some of the signals has been discovered in recent years, providing a first insight into the type of chemical language spoken between the two symbiotic partners. Importantly, these discoveries suggest that the dialogue is complex and that additional factors and corresponding receptors remain to be unveiled. Here, we explore the latest advances in this pre-symbiotic plant-fungal signal exchange and present the resulting current understanding of rhizosphere communication in AM symbioses.

Most terrestrial plants, including crops, engage in beneficial interactions with arbuscular mycorrhizal fungi. Vital to the association is mutual recognition involving the release of diffusible signals into the rhizosphere. Previously, we identified the maize no perception 1 (nope1) mutant to be defective in early signalling. Here, we report cloning of ZmNope1 on the basis of synteny with rice. NOPE1 encodes a functional homologue of the Candida albicans N-acetylglucosamine (GlcNAc) transporter NGT1, and represents the first plasma membrane GlcNAc transporter identified from plants. In C. albicans, exposure to GlcNAc activates cell signalling and virulence. Similarly, in Rhizophagus irregularis treatment with rice wild-type but not nope1 root exudates induced transcriptome changes associated with signalling function, suggesting a requirement of NOPE1 function for presymbiotic fungal reprogramming.

Summary Plant interactions with arbuscular mycorrhizal fungi have long attracted interest for their potential to promote more efficient use of mineral resources in agriculture. Their use, however, remains limited by a lack of understanding of the processes that determine the outcome of the symbiosis. In this study, the impact of host genotype on growth response to mycorrhizal inoculation was investigated in a panel of diverse maize lines. A panel of 30 maize lines was evaluated with and without inoculation with arbuscular mycorrhizal fungi. The line Oh43 was identified to show superior response and, along with five other reference lines, was characterized in greater detail in a split-compartment system, using 33P to quantify mycorrhizal phosphorus uptake. Changes in relative growth indicated variation in host capacity to profit from the symbiosis. Shoot phosphate content, abundance of root-internal and -external fungal structures, mycorrhizal phosphorus uptake, and accumulation of transcripts encoding plant PHT1 family phosphate transporters varied among lines. Superior response in Oh43 is correlated with extensive development of root-external hyphae, accumulation of specific Pht1 transcripts and high phosphorus uptake by mycorrhizal plants. The data indicate that host genetic factors influence fungal growth strategy with an impact on plant performance.

Central to the mutualistic arbuscular mycorrhizal symbiosis is the arbuscule, the site where symbiotic phosphate is delivered. Initial investigations in legumes have led to the exciting observation that symbiotic phosphate uptake not only enhances plant growth but also regulates arbuscule dynamics and is, furthermore, required for maintenance of the symbiosis. This review evaluates the possible role of the phosphate ion, not only as a nutrient but also as a signal that is necessary for reprogramming the host cortex cell for symbiosis.

Arbuscular mycorrhizal fungi colonize the roots of most monocotyledons and dicotyledons despite their different root architecture and cell patterning. Among the cereal hosts of arbuscular mycorrhizal fungi, Oryza sativa (rice) possesses a peculiar root system composed of three different types of roots: crown roots; large lateral roots; and fine lateral roots. Characteristic is the constitutive formation of aerenchyma in crown roots and large lateral roots and the absence of cortex from fine lateral roots. Here, we assessed the distribution of colonization by Glomus intraradices within this root system and determined its effect on root system architecture. Large lateral roots are preferentially colonized, and fine lateral roots are immune to arbuscular mycorrhizal colonization. Fungal preference for large lateral roots also occurred in sym mutants that block colonization of the root beyond rhizodermal penetration. Initiation of large lateral roots is significantly induced by G. intraradices colonization and does not require a functional common symbiosis signaling pathway from which some components are known to be needed for symbiosis-mediated lateral root induction in Medicago truncatula. Our results suggest variation of symbiotic properties among the different rice root-types and induction of the preferred tissue by arbuscular mycorrhizal fungi. Furthermore, signaling for arbuscular mycorrhizal-elicited alterations of the root system differs between rice and M. truncatula.

Phosphorus (P) is a major plant nutrient and developing crops with higher P-use efficiency is an important breeding goal. In this context we have conducted a comparative study of irrigated and rainfed rice varieties to assess genotypic differences in colonization with arbuscular mycorrhizal (AM) fungi and expression of different P transporter genes. Plants were grown in three different soil samples from a rice farm in the Philippines. The data show that AM symbiosis in all varieties was established after 4 weeks of growth under aerobic conditions and that, in soil derived from a rice paddy, natural AM populations recovered within 6 weeks. The analysis of AM marker genes (AM1, AM3, AM14) and P transporter genes for the direct Pi uptake (PT2, PT6) and AM-mediated pathway (PT11, PT13) were largely in agreement with the observed root AM colonization providing a useful tool for diversity studies. Interestingly, delayed AM colonization was observed in the aus-type rice varieties which might be due to their different root structure and might confer an advantage for weed competition in the field. The data further showed that P-starvation induced root growth and expression of the high-affinity P transporter PT6 was highest in the irrigated variety IR66 which also maintained grain yield under P-deficient field conditions.

Summary Maize mutants affected in the symbiotic interaction with the arbuscular mycorrhizal fungus Glomus mosseae have been found by a visual, macroscopic screen in a Mutator-tagged population of maize. Seven mutants have been identified, falling into three phenotypic classes. For each class one mutant has been characterized in more detail. The nope1 (noperception 1) mutant does not support appressoria formation of G. mosseae, suggesting the absence of a plant-encoded function necessary for early recognition prior to contact. The phenotype segregated as a monogenic recessive trait, indicating that a mutation in a single locus abolished compatibility of maize to G. mosseae. On a second mutant termed taci1 (taciturn 1), appressoria form at reduced frequency but their morphology is normal and leads to penetration of the rhizodermis. However, intraradically, the majority of hyphae are septate, resulting in terminated fungal spreading. This phenotype suggests that the mutation of taci1 has an effect on recognition and on cortex invasion. Segregation analysis indicates taci1 to carry a recessive mutation. In contrast, wild-type fungal morphology has been recorded in the Pram1 (Precocious arbuscular mycorrhiza 1) mutant, which displays enhanced and earlier fungal invasion. This trait segregates in a dominant fashion indicative of a gain-of-function mutation affecting the plant's control over restricting fungal colonization.

SPE IPM; International audience; Root systems consist of different root types (RTs) with distinct developmental and functional characteristics. RTs may be individually reprogrammed in response to their microenvironment to maximize adaptive plasticity. Molecular understanding of such specific remodeling—although crucial for crop improvement—is limited. Here, RT-specific transcriptomes of adult rice crown, large and fine lateral roots were assessed, revealing molecular evidence for functional diversity among individual RTs. Of the three rice RTs, crown roots displayed a significant enrichment of transcripts associated with phytohormones and secondary cell wall (SCW) metabolism, whereas lateral RTs showed a greater accumulation of transcripts related to mineral transport. In nature, arbuscular mycorrhizal (AM) symbiosis represents the default state of most root systems and is known to modify root system architecture. Rice RTs become heterogeneously colonized by AM fungi, with large laterals preferentially entering into the association. However, RT-specific transcriptional responses to AM symbiosis were quantitatively most pronounced for crown roots despite their modest physical engagement in the interaction. Furthermore, colonized crown roots adopted an expression profile more related to mycorrhizal large lateral than to noncolonized crown roots, suggesting a fundamental reprogramming of crown root character. Among these changes, a significant reduction in SCW transcripts was observed that was correlated with an alteration of SCW composition as determined by mass spectrometry. The combined change in SCW, hormone- and transport-related transcript profiles across the RTs indicates a previously overlooked switch of functional relationships among RTs during AM symbiosis, with a potential impact on root system architecture and functioning.

Plants share photosynthetically fixed carbon with arbuscular mycorrhizal (AM) fungi to maintain their growth and nutrition. AM fungi are oleogenic fungi that contain numerous lipid droplets in their syncytial mycelia during most of their life cycle. These lipid droplets are probably used for supporting growth of extraradical mycelia and propagation; however, when and where the lipid droplets are produced remains unclear. To address these issues, we investigated the correlation between intracellular colonization stages and the appearance of fungal lipid droplets in roots by a combination of vital staining of fungal structures, selective staining of lipids and live imaging. We discovered that a surge of lipid droplets coincided with the collapse of arbuscular branches, indicating that arbuscule collapse and the emergence of lipid droplets may be associated processes. This phenomenon was observed in the model AM fungus Rhizophagus irregularis and the ancestral member of AM fungi Paraglomus occultum. Because the collapsing arbuscules were metabolically inactive, the emerged lipid droplets are probably derived from preformed lipids but not de novo synthesized. Our observations highlight a novel mode of lipid release by AM fungi.

International audience; The mutualistic symbiosis involving Glomeromycota, a distinctive phylum of early diverging Fungi, is widely hypothesized to have promoted the evolution of land plants during the middle Paleozoic. These arbuscular mycorrhizal fungi (AMF) perform vital functions in the phosphorus cycle that are fundamental to sustainable crop plant productivity. The unusual biological features of AMF have long fascinated evolutionary biologists. The coenocytic hyphae host a community of hundreds of nuclei and reproduce clonally through large multinucleated spores. It has been suggested that the AMF maintain a stable assemblage of several different genomes during the life cycle, but this genomic organization has been questioned. Here we introduce the 153-Mb haploid genome of Rhizophagus irregularis and its repertoire of 28,232 genes. The observed low level of genome polymorphism (0.43 SNP per kb) is not consistent with the occurrence of multiple, highly diverged genomes. The expansion of mating-related genes suggests the existence of cryptic sex-related processes. A comparison of gene categories confirms that R. irregularis is close to the Mucoromycotina. The AMF obligate biotrophy is not explained by genome erosion or any related loss of metabolic complexity in central metabolism, but is marked by a lack of genes encoding plant cell wall-degrading enzymes and of genes involved in toxin and thiamine synthesis. A battery of mycorrhiza-induced secreted proteins is expressed in symbiotic tissues. The present comprehensive repertoire of R. irregularis genes provides a basis for future research on symbiosis-related mechanisms in Glomeromycota.

Pi acquisition of crops via arbuscular mycorrhizal (AM) symbiosis is becoming increasingly important due to limited high-grade rock Pi reserves and a demand for environmentally sustainable agriculture. Here, we show that 70% of the overall Pi acquired by rice (Oryza sativa) is delivered via the symbiotic route. To better understand this pathway, we combined genetic, molecular, and physiological approaches to determine the specific functions of two symbiosis-specific members of the PHOSPHATE TRANSPORTER1 (PHT1) gene family from rice, ORYsa;PHT1;11 (PT11) and ORYsa;PHT1;13 (PT13). The PT11 lineage of proteins from mono- and dicotyledons is most closely related to homologs from the ancient moss, indicating an early evolutionary origin. By contrast, PT13 arose in the Poaceae, suggesting that grasses acquired a particular strategy for the acquisition of symbiotic Pi. Surprisingly, mutations in either PT11 or PT13 affected the development of the symbiosis, demonstrating that both genes are important for AM symbiosis. For symbiotic Pi uptake, however, only PT11 is necessary and sufficient. Consequently, our results demonstrate that mycorrhizal rice depends on the AM symbiosis to satisfy its Pi demands, which is mediated by a single functional Pi transporter, PT11.

• The arbuscular mycorrhizal symbiosis is arguably the most ecologically important eukaryotic symbiosis, yet it is poorly understood at the molecular level. To provide novel insights into the molecular basis of symbiosis-associated traits, we report the first genome-wide analysis of the transcriptome from Glomus intraradices DAOM 197198. • We generated a set of 25,906 nonredundant virtual transcripts (NRVTs) transcribed in germinated spores, extraradical mycelium and symbiotic roots using Sanger and 454 sequencing. NRVTs were used to construct an oligoarray for investigating gene expression. • We identified transcripts coding for the meiotic recombination machinery, as well as meiosis-specific proteins, suggesting that the lack of a known sexual cycle in G. intraradices is not a result of major deletions of genes essential for sexual reproduction and meiosis. Induced expression of genes encoding membrane transporters and small secreted proteins in intraradical mycelium, together with the lack of expression of hydrolytic enzymes acting on plant cell wall polysaccharides, are all features of G. intraradices that are shared with ectomycorrhizal symbionts and obligate biotrophic pathogens. • Our results illuminate the genetic basis of symbiosis-related traits of the most ancient lineage of plant biotrophs, advancing future research on these agriculturally and ecologically important symbionts.

Exploitation of arbuscular mycorrhizal fungi may be an important approach for development of reduced-input agriculture. We discuss the use of linear models to analyze variation in mycorrhiza response among diverse plant varieties in order to assess the value of mycorrhizas. Our approach allows elimination of variation linked to differences in plant performance in the absence of mycorrhizas and the selection of plant lines that might harbor genetic variation of use to improve the mycorrhizal symbiosis in agriculture. We illustrate our approach by applying it to previously published and to novel data. We suggest that in dealing with a relative trait such as mycorrhiza effect, the choice of measure used to quantify the trait greatly affects interpretation. In the plant populations under consideration, we find evidence for a greater potential to increase mycorrhiza benefit than previously suggested.

Knowledge about signaling in arbuscular mycorrhizal (AM) symbioses is currently restricted to the common symbiosis (SYM) signaling pathway discovered in legumes. This pathway includes calcium as a second messenger and regulates both AM and rhizobial symbioses. Both monocotyledons and dicotyledons form symbiotic associations with AM fungi, and although they differ markedly in the organization of their root systems, the morphology of colonization is similar. To identify and dissect AM-specific signaling in rice (Oryza sativa), we developed molecular phenotyping tools based on gene expression patterns that monitor various steps of AM colonization. These tools were used to distinguish common SYM-dependent and -independent signaling by examining rice mutants of selected putative legume signaling orthologs predicted to be perturbed both upstream (CASTOR and POLLUX) and downstream (CCAMK and CYCLOPS) of the central, calcium-spiking signal. All four mutants displayed impaired AM interactions and altered AM-specific gene expression patterns, therefore demonstrating functional conservation of SYM signaling between distant plant species. In addition, differential gene expression patterns in the mutants provided evidence for AM-specific but SYM-independent signaling in rice and furthermore for unexpected deviations from the SYM pathway downstream of calcium spiking.

The majority of terrestrial plants live in association with symbiotic fungi that facilitate mineral nutrient uptake. The oldest and most prevalent of these associations are the arbuscular mycorrhizal (AM) symbioses that first evolved approximately 400 million years ago, coinciding with the appearance of the first land plants. Crop domestication, in comparison, is a relatively recent event, beginning approximately 10000 years ago. How has the dramatic change from wild to cultivated ecosystems impacted AM associations, and do these ancient symbioses potentially have a role in modern agriculture? Here, we review recent advances in AM research and the use of breeding approaches to generate new crop varieties that enhance the agronomic potential of AM associations.

Development of the mutualistic arbuscular mycorrhiza (AM) symbiosis between most land plants and fungi of the Glomeromycota is regulated by phytohormones. The role of jasmonate (JA) in AM colonization has been investigated in the dicotyledons Medicago truncatula, tomato and Nicotiana attenuata and contradicting results have been obtained with respect to a neutral, promotive or inhibitory effect of JA on AM colonization. Furthermore, it is currently unknown whether JA plays a role in AM colonization of monocotyledonous roots. Therefore we examined whether JA biosynthesis is required for AM colonization of the monocot rice. To this end we employed the rice mutant constitutive photomorphogenesis 2 (cpm2), which is deficient in JA biosynthesis. Through a time course experiment the amount and morphology of fungal colonization did not differ between wild-type and cpm2 roots. Furthermore, no significant difference in the expression of AM marker genes was detected between wild type and cpm2. However, treatment of wild-type roots with 50 μM JA lead to a decrease of AM colonization and this was correlated with induction of the defense gene PR4. These results indicate that JA is not required for AM colonization of rice but high levels of JA in the roots suppress AM development likely through the induction of defense.

Contents Summary 35 I. Introduction 35 II. Presymbiotic dialogue – recognition and anticipation 36 III. Early symbiotic phase – contact and penetration 39 IV. Mature symbiotic phase – haustoria and mineral nutrition 41 V. Concluding remarks 43 Acknowledgements 43 References 43 Summary Recent years have seen fascinating contributions to our understanding of the molecular dialogue between fungi and plants entering into arbuscular mycorrhizal (AM) symbioses. Attention has shifted from descriptions of physiological and cellular events to molecular genetics and modern chemical diagnostics. Genes, signal transduction pathways and the chemical structures of components relevant to the symbiosis have been defined. This review examines our current knowledge of signals and mechanisms involved in the establishment of AM symbioses.

Plants are solar-powered sugar factories that feed a multitude of other organisms. Many of these organisms associate directly with host plants to gain access to the plant's photosynthates. Such symbioses encompass a wide collection of styles ranging from mutualistic to commensal and parasitic. Among these, the mutualistic arbuscular mycorrhizal (AM) symbiosis is one of the evolutionarily oldest symbioses of plants, relying on the formation of an intimate relationship between fungi of the Glomeromycota and roots of the majority of vascular flowering plants. In this symbiosis, the fungus intracellularly colonizes living root cells, implying the existence of an extreme form of compatibility. Interestingly, molecular events that happen in the plant in response to mycorrhizal colonization also occur in other beneficial and, as recently shown, even antagonistic plant symbioses. Thus, basic 'compatibility modules' appear to be partially conserved between mutualism and parasitism.

Glomalean fungi induce and colonize symbiotic tissue called arbuscular mycorrhiza on the roots of most land plants. Other fungi also colonize plants but cause disease not symbiosis. Whole-transcriptome analysis using a custom-designed Affymetrix Gene-Chip and confirmation with real-time RT-PCR revealed 224 genes affected during arbuscular mycorrhizal symbiosis. We compared these transcription profiles with those from rice roots that were colonized by pathogens ( Magnaporthe grisea and Fusarium moniliforme ). Over 40% of genes showed differential regulation caused by both the symbiotic and at least one of the pathogenic interactions. A set of genes was similarly expressed in all three associations, revealing a conserved response to fungal colonization. The responses that were shared between pathogen and symbiont infection may play a role in compatibility. Likewise, the responses that are different may cause disease. Some of the genes that respond to mycorrhizal colonization may be involved in the uptake of phosphate. Indeed, phosphate addition mimicked the effect of mycorrhiza on 8% of the tested genes. We found that 34% of the mycorrhiza-associated rice genes were also associated with mycorrhiza in dicots, revealing a conserved pattern of response between the two angiosperm classes.

The establishment of arbuscular mycorrhizal (AM) symbioses, formed by most flowering plants in association with glomeromycotan fungi, and the root-nodule (RN) symbiosis, formed by legume plants and rhizobial bacteria, requires an ongoing molecular dialogue that underpins the reprogramming of root cells for compatibility. In both endosymbioses, there are distinct phases to the interaction, including a presymbiotic anticipation phase and, subsequently, an intraradical accommodation of the microsymbiont. Maintenance of the endosymbiosis then depends on reciprocal nutrient exchange with the microsymbiont-obtaining plant photosynthates in exchange for mineral nutrients: enhanced phosphate and nitrogen uptake from AM fungi and fixed nitrogen from rhizobia. Despite the taxonomically distinct groups of symbionts, commonalities are observed in the signaling components and the modulation of host cell responses in both AM and RN symbioses, reflecting common mechanisms for plant cell reprogramming during endosymbiosis.

Plett, Jonathan M. Martin, Francis1879-0356; Mutualistic mycorrhizal plant-fungal interactions have shaped the evolution of plant life on land. In these intimate associations, fungal hyphae grow invasively within plant tissues. Despite this invasion, these mycorrhizal fungi are not repulsed leading to a great deal of research focused on the signals exchanged between mutualistic fungi and their host plants in an effort to understand how these relationships are established. In this review, we focus on one type of signal used by mutualistic fungi during symbiosis: effector proteins. These small secreted proteins have recently been found to be used by a range of beneficial fungi to alter the physiological status of the plant host such that symbiosis is favoured. We discuss how the role of these novel proteins has altered our vision of how the 'mutualistic' lifestyle evolved in fungi: rather than being perceived as beneficial by their plant hosts, these microbes currently viewed as 'beneficial' may actually be overcoming the defences of their plant hosts in a mechanism originally thought to be unique to pathogenic microbes.