Arbuscular Mycorrhiza Symbiosis Research Articles

The application of a treated sugar beet waste residue to soil modifies the responses of mycorrhizal and non mycorrhizal lettuce plants to drought stress

Positive effects of sugar beet (SB) application on soil properties and performance of several woody shrub legumes have been described under heavy metal stress and in diverse degraded environments, especially when combined with arbuscular mycorrhiza (AM). However, information on the combined effect of SB amendments and AM symbiosis in horticultural crop plants under drought stress is scarce. Thus, the main objective of this work was to determine if the combination of treated SB waste and AM fungi results in improved drought tolerance of an horticultural food crop such as lettuce and whether or not the effects observed are linked to enhanced antioxidant activities and regulation of two stress-related genes. Lettuce plants inoculated or not with Glomus intraradices and grown on soil amended or not with a treated SB waste were cultivated under well-watered conditions or subjected to drought stress. Plant growth, expression of two drought responsive genes encoding for Δ1-pyrroline-5-carboxylate synthetase and 9-cis-epoxycarotenoid dioxygenase, oxidative damage to lipids and the activity of four antioxidant enzymes were measured. Results showed that the application of treated SB waste resulted negative for the development of AM and nonAM plants (both under well-watered and under drought stress conditions). This effect can not be ascribed to the impairment of specific plant antioxidant defenses. In contrast, a lack of induction of a gene from the ABA biosynthetic pathway was observed in SB-treated plants, which could have contributed to the low performance of these plants. The positive effects of combined application of treated SB waste as amendment and AM fungi have not been shown for a horticultural food crop such as Lactuca sativa. Thus, before starting a program aimed at the utilization of different amendments based on transformed wastes, basic studies on functional and physiological compatibility between the plant and the amendment are necessary.

Arsenic toxicity in crop plants: physiological effects and tolerance mechanisms

Heavy metals are toxic substances released into the environment, contributing to a variety of toxic effects on living organisms in food chain by accumulation and biomagnifications. Certain pollutants such as arsenic (As) remain in the environment for an extensive period. They eventually accumulate to levels that could harm physiochemical properties of soils and lead to loss of soil fertility and crop yield. Arsenic, when not detoxified, may trigger a sequence of reactions leading to growth inhibition, disruption of photosynthetic and respiratory systems, and stimulation of secondary metabolism. Plants respond to As toxicity by a variety of mechanisms including hyperaccumulation, antioxidant defense system, and phytochelation. Arbuscular mycorrhizae symbiosis occurs in almost all habitats and climates, including disturbed soils. There is growing evidence that arbuscular mycorrhizae fungi may alleviate metal/metalloid toxicity to host plant. Here, we review (1) arsenic speciation in the environment and how As is taken up by the roots and metabolised within plants, and (2) the role of arbuscular mycorrhizae in alleviating arsenic toxicity in crop plants.

Ethylene‐dependent/ethylene‐independent ABA regulation of tomato plants colonized by arbuscular mycorrhiza fungi

We investigated the relationship between ABA and ethylene regulating the formation of the arbuscular mycorrhiza (AM) symbiosis in tomato (Solanum lycopersicum) plants and tried to define the specific roles played by each of these phytohormones in the mycorrhization process. We analysed the impact of ABA biosynthesis inhibition on mycorrhization by Glomus intraradices in transgenic tomato plants with an altered ethylene pathway. We also studied the effects on mycorrhization in sitiens plants treated with the aminoethoxyvinyl glycine hydrochloride (AVG) ethylene biosynthesis inhibitor and supplemented with ABA. In addition, the expression of plant and fungal genes involved in the mycorrhization process was studied. ABA biosynthesis inhibition qualitatively altered the parameters of mycorrhization in accordance with the plant's ethylene perception and ethylene biosynthesis abilities. Inhibition of ABA biosynthesis in wild-type plants negatively affected all the mycorrhization parameters studied, while tomato mutants impaired in ethylene synthesis only showed a reduced arbuscular abundance in mycorrhizal roots. Inhibition of ethylene synthesis in ABA-deficient sitiens plants increased the intensity of mycorrhiza development, while ABA application rescued arbuscule abundance in the root's mycorrhizal zones. The results of our study show an antagonistic interaction between ABA and ethylene, and different roles of each of the two hormones during AM formation. This suggests that a dual ethylene-dependent/ethylene-independent mechanism is involved in ABA regulation of AM formation.

Arbuscular mycorrhizal fungi in roots of non-photosynthetic plants, <i>Sciaphila japonica</i> and <i>Sciaphila tosaensis</i> (Triuridaceae)

The mycorrhizal fungi in the roots of achlorophyllous Sciaphila japonica and S. tosaensis (Triuridaceae) were identified by molecular methods. The habitats of S. japonica were in a tree plantation of Japanese cypress, Chamaecyparis obtusa, and bamboo forests, and those of S. tosaensis were in a camellia forest and a bamboo forest. In the root cortical cells of both plants, aseptate hyphal coils were observed, which suggested the Paris-type arbuscular mycorrhiza (AM). A phylogenetic analysis based on a partial sequence of an AM fungal nuclear small subunit ribosomal RNA gene showed that the fungal DNA sequences of S. japonica were separated into three closely related clades. Those of S. tosaensis were separated into two clades, which were also closely related to each other. The AM fungi of S. japonica and S. tosaensis were completely separated in the phylogenetic tree even among those found in the same habitat, which suggests the high specificities in the plant-fungal partnerships. All the detected AM fungi in these plants belonged to Glomus-group A. Even though the habitats are in quite common environments, both plant species are known as endangered species in Japan. Such a definite specificity in AM symbioses seems to restrict the distribution of the myco-heterotrophic plants.

Common and not so common symbiotic entry

Great advances have been made in our understanding of the host plant's common symbiosis functions, which in legumes mediate intracellular accommodation of both nitrogen-fixing bacteria and arbuscular mycorrhiza (AM) fungi. However, it has become apparent that additional plant genes are required specifically for bacterial entry inside the host root. In this opinion article, we consider Lotus japonicus nap1 and pir1 symbiotic mutants within the context of other deleterious mutations that impair an intracellular accommodation of bacteria but have no impact on the colonization of roots by AM fungi. We highlight a clear delineation of early signaling events during bacterial versus AM symbioses while suggesting a more intricate origin of the plant's ability for intracellular accommodation of bacteria.

Function of GRAS Proteins in Root Nodule Symbiosis is Retained in Homologs of a Non-Legume, Rice

Root nodule (RN) symbiosis in legumes shares genes involved in the early signaling pathway with more ancient arbuscular mycorrhiza (AM) symbiosis, which is widespread in higher plants. The non-legume homologs of such genes have been well documented to be not only essential for the AM symbiosis in non-legume mycorrhizal plants but also functional in the RN symbiosis in legume plants. In contrast, it has not been investigated in detail whether RN symbiosis-specific genes, which are not essential for AM symbiosis, are functionally conserved in non-legumes. Two GRAS-domain transcription factors, NSP1 and NSP2, have been shown to be required for RN symbiosis, but not for AM symbiosis. In this study, we demonstrated that their homologs, OsNSP1 and OsNSP2, from rice are able to fully rescue the RN symbiosis-defective phenotypes of the mutants of corresponding genes in the model legume, Lotus japonicus. Our results indicate that some of the genes essential for RN symbiosis conserve their functions in homologs from non-legumes, which do not nodulate.

Regulation of the nitrogen transfer pathway in the arbuscular mycorrhizal symbiosis: gene characterization and the coordination of expression with nitrogen flux.

The arbuscular mycorrhiza (AM) brings together the roots of over 80% of land plant species and fungi of the phylum Glomeromycota and greatly benefits plants through improved uptake of mineral nutrients. AM fungi can take up both nitrate and ammonium from the soil and transfer nitrogen (N) to host roots in nutritionally substantial quantities. The current model of N handling in the AM symbiosis includes the synthesis of arginine in the extraradical mycelium and the transfer of arginine to the intraradical mycelium, where it is broken down to release N for transfer to the host plant. To understand the mechanisms and regulation of N transfer from the fungus to the plant, 11 fungal genes putatively involved in the pathway were identified from Glomus intraradices, and for six of them the full-length coding sequence was functionally characterized by yeast complementation. Two glutamine synthetase isoforms were found to have different substrate affinities and expression patterns, suggesting different roles in N assimilation. The spatial and temporal expression of plant and fungal N metabolism genes were followed after nitrate was added to the extraradical mycelium under N-limited growth conditions using hairy root cultures. In parallel experiments with (15)N, the levels and labeling of free amino acids were measured to follow transport and metabolism. The gene expression pattern and profiling of metabolites involved in the N pathway support the idea that the rapid uptake, translocation, and transfer of N by the fungus successively trigger metabolic gene expression responses in the extraradical mycelium, intraradical mycelium, and host plant.

A dominant function of CCaMK in intracellular accommodation of bacterial and fungal endosymbionts.

In legumes, Ca2+/calmodulin-dependent protein kinase (CCaMK) is a component of the common symbiosis genes that are required for both root nodule (RN) and arbuscular mycorrhiza (AM) symbioses and is thought to be a decoder of Ca2+ spiking, one of the earliest cellular responses to microbial signals. A gain-of-function mutation of CCaMK has been shown to induce spontaneous nodulation without rhizobia, but the significance of CCaMK activation in bacterial and/or fungal infection processes is not fully understood. Here we show that a gain-of-function CCaMKT265D suppresses loss-of-function mutations of common symbiosis genes required for the generation of Ca2+ spiking, not only for nodule organogenesis but also for successful infection of rhizobia and AM fungi, demonstrating that the common symbiosis genes upstream of Ca2+ spiking are required solely to activate CCaMK. In RN symbiosis, however, CCaMKT265D induced nodule organogenesis, but not rhizobial infection, on Nod factor receptor (NFRs) mutants. We propose a model of symbiotic signaling in host legume plants, in which CCaMK plays a key role in the coordinated induction of infection thread formation and nodule organogenesis.

Knockdown of the symbiotic sucrose synthase MtSucS1 affects arbuscule maturation and maintenance in mycorrhizal roots of Medicago truncatula.

The relevance of the symbiosis-induced Medicago truncatula sucrose synthase gene MtSucS1 for an efficient arbuscular mycorrhiza (AM) was studied using two independent antisense lines that displayed up to 10-fold reduced SucS1 levels in roots. Mycorrhizal MtSucS1-reduced lines exhibited an overall stunted aboveground growth under inorganic phosphorus limitation. Apart from a reduced plant height, shoot weight, and leaf development, a delayed flowering, resulting in a lower seed yield, was observed. In addition, the root-to-shoot and root weight ratios increased significantly. Gene expression studies demonstrated a major reversion of AM-associated transcription, exhibiting a significant repression of well-known plant AM marker and mycosymbiont genes, together indicating a diminished AM fungus colonization of MtSucS1-antisense lines. Concomitantly, gas chromatography-mass spectrometry-based metabolite profiling revealed that mycorrhizal MtSucS1-reduced lines were affected in important nodes of the carbon, nitrogen, and phosphorus metabolism, accentuating a physiological significance of MtSucS1 for AM. In fact, antisensing MtSucS1 provoked an impaired fungal colonization within the less abundant infected regions, evident from strongly reduced frequencies of internal hyphae, vesicles, and arbuscules. Moreover, arbuscules were early senescing, accompanied with a reduced development of mature arbuscules. This defective mycorrhiza status correlated with reduced phosphorus and nitrogen levels and was proportional to the extent of MtSucS1 knockdown. Together, our results point to an important role for MtSucS1 in the establishment and maintenance of arbuscules in the AM symbiosis.

O papel da comunidade de fungos micorrízicos arbusculares (FMA) autóctones no desenvolvimento de espécies vegetais nativas em área de dunas de restinga revegetadas no litoral do Estado da Paraíba

A simbiose entre fungos micorrizicos arbusculares (FMA) com raizes de plantas vasculares constitui uma das mais importantes formas de mitigar o impacto das areas pertubadas. O trabalho objetivou caracterizar a comunidade de FMA presente no solo de area de duna revegetada e avaliar sua influencia sobre o desenvolvimento de especies nativas. Foi realizada coleta de solo durante o periodo chuvoso em area revegetada, avaliando-se: producao de proteinas do solo relacionadas a glomalina (PSRG), densidade e diversidade de glomerosporos. A influencia da comunidade nativa de FMA foi determinada para duas especies vegetais nativas: Tabebuia roseo-alba (Ridl.) Sandw. (peroba) e Tocoyena selloana Schum. (jenipapo-bravo). Para cada especie foram testados dois tratamentos - solo nativo (SN) e solo nativo desinfestado (SND) - em delineamento inteiramente casualizado com 10 repeticoes. Ao final foram avaliados: altura, diâmetro do caule, numero de folhas, area foliar, biomassa seca e conteudo de nutrientes nas partes aerea e radicular, densidade de glomerosporos, colonizacao micorrizica hifalica, arbuscular, vesicular e total e producao de proteinas do solo relacionadas a glomalina (PSRG). O solo da area de duna revegetada apresentou 1 glomerosporo g-1 de solo e 1,20 ± 0,04 mg PSRG g-1 solo, sendo identificadas seis especies de FMA. Maior desenvolvimento vegetal e fungico ocorreram no SN. A colonizacao micorrizica na peroba foi de 80% e no jenipapo-bravo 60%. Os FMA estao presentes em areas revegetadas apos extracao de minerios, e contribuem para o crescimento das especies nativas testadas em condicoes de casa de vegetacao, sugerindo assim, que o desempenho dessas plantas e influenciado pela simbiose micorrizica arbuscular.

Molecular genetic mechanisms used by legumes to control early stages of mutually beneficial (mutualistic) symbiosis

Recent data on the plant control of early stages of mutually beneficial (mutualistic) symbioses of legumes, the mechanisms of perception and transmission of the microsymbiont's molecular signals in the macrosymbiont's cells, and induction of the genetic programs of the development of symbiotic compartments and organs of the plant are summarized. It is demonstrated that the genetic system of the plant controlling the development of nitrogen-fixing symbiosis of legumes (symbiotic root nodules), which emerged 70-80 Ma ago, has undoubtedly evolved on the basis of the genetic system controlling the development of the symbiosis with arbuscular mycorrhizal fungi (which emerged 40-500 Ma ago. Interactions between genes and between gene products, as well as exchange of molecular signals, form the basis of mutually beneficial (mutualistic) plant-bacterium interactions. Even in the case of a highly specific nitrogen-fixing symbiosis of legumes (symbiotic nodules), the receptors perceiving the signal from root-nodule bacteria may function in different ways. The development of arbuscular mycorrhiza and nitrogen-fixing symbiosis in legumes is a multistep process involving hundreds of genes of both the macro- and microsymbionts. For the symbioses to develop successfully, these genes should act in a coordinated way in the newly formed superorganismal system. Further studies are necessary to shed light onto the complexity of the plant genetic control of the development of mutualistic symbioses in legumes and provide information required for improving their functions in adaptive plant-breeding systems.

Plant‐microbe symbioses: new insights into common roots

Arbuscular mycorrhiza (AM), a type of plant-fungal endosymbiosis, and nodulation, a bacterial-plant endosymbiosis, are the most ubiquitous symbioses on earth. Recent findings have established part of a shared genetic basis underlying these interactions. Here, we approach root endosymbioses through the lens of the homology and modularity concepts aiming at further clarifying the proximate and ultimate causes for the establishment of these biological systems. We review the genetics that underlie interspecific signaling and its concomitant shift in genetic programs for either partner. Also, through the comparative analysis of genetic modules shared by AM and nodulation symbioses, we identify fundamental nodes in these networks, suggesting the elemental steps that may have permitted symbiotic adaptation. Here, we show that this approach, allied to recent technical advances in the study of genetic systems architecture, can provide clear testable hypotheses for the advancement of our understanding on the evolution and development of symbiotic systems.

Apoplastic plant subtilases support arbuscular mycorrhiza development in Lotus japonicus

In the arbuscular mycorrhiza (AM) symbiosis, plant roots accommodate Glomeromycota fungi within an intracellular compartment, the arbuscule. At this symbiotic interface, fungal hyphae are surrounded by a plant membrane, which creates an apoplastic compartment, the periarbuscular space (PAS) between fungal and plant cell. Despite the importance of the PAS for symbiotic signal and metabolite exchange, only few of its components have been identified. Here we show that two apoplastic plant proteases of the subtilase family are required for AM development. SbtM1 is the founder member of a family of arbuscular mycorrhiza-induced subtilase genes that occur in at least two clusters in the genome of the legume Lotus japonicus. A detailed expression analysis by RT-PCR revealed that SbtM1, SbtM3, SbtM4 and the more distantly related SbtS are all rapidly induced during development of arbuscular mycorrhiza, but only SbtS and SbtM4 are also up-regulated during root nodule symbiosis. Promoter-reporter fusions indicated specific activation in cells that are adjacent to intra-radical fungal hyphae or in cells that harbour them. Venus fluorescent protein was observed in the apoplast and the PAS when expressed from a fusion construct with the SbtM1 signal peptide or the full-length subtilase. Suppression of SbtM1 or SbtM3 by RNAi caused a decrease in intra-radical hyphae and arbuscule colonization, but had no effect on nodule formation. Our data indicate a role for these subtilases during the fungal infection process in particular arbuscule development.

The effect of arbuscular mycorrhizal root colonization on growth and nutrient uptake of two different cowpea (Vigna unguiculata [L.] Walp.) genotypes exposed to drought stress

In the present investigation, the effect of arbuscular mycorrhiza (AM) fungal root colonization on nutrient uptake, growth and soil water depletion of cowpea plants exposed to a drought stress period was studied in a greenhouse experiment. Arbuscular mycorrhizal and nonAM plants of an old, local variety from Brazil ‘Carioca’, and of the breeding improved cultivar ‘Epace-10’ were exposed to 24 days of drought, with or without a subsequent period of water resupply. Control plants remained well watered throughout the growth period. The AM symbiosis greatly enhanced nutrient uptake of drought stressed plants. However, water uptake, growth and net photosynthesis were unaffected by AM root colonization during drought stress. Recovery after water resupply was much faster when plants were inoculated with AM, probably due to an improved plant nutritional status. The cultivar Epace-10 was much more dependent on the AM symbiosis for growth and nutrient uptake compared with Carioca in all irrigation treatments. Only when roots were AM colonized, Epace-10 plants were able to recover from drought stress after water resupply. Our study suggests that the AM symbiosis constitutes an important strategy by which leguminous plants overcome periods of drought. Under conditions of low soil water and P availability, the presence of AM fungal propagules in the field soil appears to be a prerequisite for successful cultivation of cowpea, particularly with respect to the breeding improved cultivar Epace-10.

Divergence of Evolutionary Ways Among Common sym Genes: CASTOR and CCaMK Show Functional Conservation Between Two Symbiosis Systems and Constitute the Root of a Common Signaling Pathway

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.

Arbuscular mycorrhiza: the mother of plant root endosymbioses

Arbuscular mycorrhiza (AM), a symbiosis between plants and members of an ancient phylum of fungi, the Glomeromycota, improves the supply of water and nutrients, such as phosphate and nitrogen, to the host plant. In return, up to 20% of plant-fixed carbon is transferred to the fungus. Nutrient transport occurs through symbiotic structures inside plant root cells known as arbuscules. AM development is accompanied by an exchange of signalling molecules between the symbionts. A novel class of plant hormones known as strigolactones are exuded by the plant roots. On the one hand, strigolactones stimulate fungal metabolism and branching. On the other hand, they also trigger seed germination of parasitic plants. Fungi release signalling molecules, in the form of 'Myc factors' that trigger symbiotic root responses. Plant genes required for AM development have been characterized. During evolution, the genetic programme for AM has been recruited for other plant root symbioses: functional adaptation of a plant receptor kinase that is essential for AM symbiosis paved the way for nitrogen-fixing bacteria to form intracellular symbioses with plant cells.

Prepenetration apparatus assembly precedes and predicts the colonization patterns of arbuscular mycorrhizal fungi within the root cortex of both Medicago truncatula and Daucus carota.

Arbuscular mycorrhizas (AM) are widespread, ancient endosymbiotic associations that contribute significantly to soil nutrient uptake in plants. We have previously shown that initial fungal penetration of the host root is mediated via a specialized cytoplasmic assembly called the prepenetration apparatus (PPA), which directs AM hyphae through the epidermis (Genre et al., 2005). In vivo confocal microscopy studies performed on Medicago truncatula and Daucus carota, host plants with different patterns of AM colonization, now reveal that subsequent intracellular growth across the root outer cortex is also PPA dependent. On the other hand, inner root cortical colonization leading to arbuscule development involves more varied and complex PPA-related mechanisms. In particular, a striking alignment of polarized PPAs can be observed in adjacent inner cortical cells of D. carota, correlating with the intracellular root colonization strategy of this plant. Ultrastructural analysis of these PPA-containing cells reveals intense membrane trafficking coupled with nuclear enlargement and remodeling, typical features of arbusculated cells. Taken together, these findings imply that prepenetration responses are both conserved and modulated throughout the AM symbiosis as a function of the different stages of fungal accommodation and the host-specific pattern of root colonization. We propose a model for intracellular AM fungal accommodation integrating peri-arbuscular interface formation and the regulation of functional arbuscule development.

The Jasmonic Acid Signalling Pathway Restricts the Development of the Arbuscular Mycorrhizal Association in Tomato

The role of the jasmonate signalling pathway in modulating the establishment of the arbuscular mycorrhiza (AM) symbiosis between tomato plants and Glomus intraradices fungus was studied. The consequences of AM formation due to the blockage of the jasmonate signalling pathway were studied in experiments with plant mutants impaired in JA perception. The tomato jai-1 mutant (jas- monic acid insensitive 1) failed to regulate colonization and was more susceptible to fungal infection, showing acceler- ated colonization. The frequency and the intensity of fungal colonization were greatly increased in the jai-1 insensitive mutant plants. In parallel, the systemic effects on mycorrh- ization due to the activation of the jasmonate signalling pathway by foliar application of MeJA were evaluated and histochemical and molecular parameters of mycorrhizal intensity and efficiency were measured. Histochemical deter- mination of fungal infectivity and fungal alkaline phosphatase activity reveal that the systemic application of MeJA was effective in reducing mycorrhization and mainly affected fungal phosphate metabolism and arbuscule formation, ana- lyzed by the expression of GiALP and the AM-specific gene LePT4, respectively. The results of the present study clearly show that JA participates in the susceptibility of tomato to infection by arbuscular mycorrhizal fungi, and it seems that arbuscular colonization in tomato is tightly controlled by the jasmonate signalling pathway.

SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankia bacteria

Root endosymbioses vitally contribute to plant nutrition and fitness worldwide. Nitrogen-fixing root nodulation, confined to four plant orders, encompasses two distinct types of associations, the interaction of legumes (Fabales) with rhizobia bacteria and actinorhizal symbioses, where the bacterial symbionts are actinomycetes of the genus Frankia. Although several genetic components of the host-symbiont interaction have been identified in legumes, the genetic basis of actinorhiza formation is unknown. Here, we show that the receptor-like kinase gene SymRK, which is required for nodulation in legumes, is also necessary for actinorhiza formation in the tree Casuarina glauca. This indicates that both types of nodulation symbiosis share genetic components. Like several other legume genes involved in the interaction with rhizobia, SymRK is also required for the interaction with arbuscular mycorrhiza (AM) fungi. We show that SymRK is involved in AM formation in C. glauca as well and can restore both nodulation and AM symbioses in a Lotus japonicus symrk mutant. Taken together, our results demonstrate that SymRK functions as a vital component of the genetic basis for both plant-fungal and plant-bacterial endosymbioses and is conserved between legumes and actinorhiza-forming Fagales.

Functional adaptation of a plant receptor-kinase paved the way for the evolution of intracellular root symbioses with bacteria.

Nitrogen-fixing root nodule symbioses (RNS) occur in two major forms—Actinorhiza and legume-rhizobium symbiosis—which differ in bacterial partner, intracellular infection pattern, and morphogenesis. The phylogenetic restriction of nodulation to eurosid angiosperms indicates a common and recent evolutionary invention, but the molecular steps involved are still obscure. In legumes, at least seven genes—including the symbiosis receptor-kinase gene SYMRK—are essential for the interaction with rhizobia bacteria and for the Arbuscular Mycorrhiza (AM) symbiosis with phosphate-acquiring fungi, which is widespread in occurrence and believed to date back to the earliest land plants. We show that SYMRK is also required for Actinorhiza symbiosis of the cucurbit Datisca glomerata with actinobacteria of the genus Frankia, revealing a common genetic basis for both forms of RNS. We found that SYMRK exists in at least three different structural versions, of which the shorter forms from rice and tomato are sufficient for AM, but not for functional endosymbiosis with bacteria in the legume Lotus japonicus. Our data support the idea that SYMRK sequence evolution was involved in the recruitment of a pre-existing signalling network from AM, paving the way for the evolution of intracellular root symbioses with nitrogen-fixing bacteria.