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Horizontal Gene Transfer From Bacteria and Plants to the Arbuscular Mycorrhizal Fungus Rhizophagus irregularis.

ABSTRACT: Arbuscular mycorrhizal fungi (AMF) belong to Glomeromycotina, and are mutualistic symbionts of many land plants. Associated bacteria accompany AMF during their lifecycle to establish a robust tripartite association consisting of fungi, plants and bacteria. Physical association among this trinity provides possibilities for the exchange of genetic materials. However, very few horizontal gene transfer (HGT) from bacteria or plants to AMF has been reported yet. In this study, we complement existing algorithms by developing a new pipeline, Blast2hgt, to efficiently screen for putative horizontally derived genes from a whole genome. Genome analyses of the glomeromycete Rhizophagus irregularis identified 19 fungal genes that had been transferred between fungi and bacteria/plants, of which seven were obtained from bacteria. Another 18 R. irregularis genes were found to be recently acquired from either plants or bacteria. In the R. irregularis genome, gene duplication has contributed to the expansion of three foreign genes. Importantly, more than half of the R. irregularis foreign genes were expressed in various transcriptomic experiments, suggesting that these genes are functional in R. irregularis. Functional annotation and available evidence showed that these acquired genes may participate in diverse but fundamental biological processes such as regulation of gene expression, mitosis and signal transduction. Our study suggests that horizontal gene influx through endosymbiosis is a source of new functions for R. irregularis, and HGT might have played a role in the evolution and symbiotic adaptation of this arbuscular mycorrhizal fungus.

SUBMITTER: Li M

PROVIDER: S-EPMC5982333 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Phytohormone production by the arbuscular mycorrhizal fungus Rhizophagus irregularis.

Project description:Arbuscular mycorrhizal symbiosis is a mutualistic interaction between most land plants and fungi of the glomeromycotina subphylum. The initiation, development and regulation of this symbiosis involve numerous signalling events between and within the symbiotic partners. Among other signals, phytohormones are known to play important roles at various stages of the interaction. During presymbiotic steps, plant roots exude strigolactones which stimulate fungal spore germination and hyphal branching, and promote the initiation of symbiosis. At later stages, different plant hormone classes can act as positive or negative regulators of the interaction. Although the fungus is known to reciprocally emit regulatory signals, its potential contribution to the phytohormonal pool has received little attention, and has so far only been addressed by indirect assays. In this study, using mass spectrometry, we analyzed phytohormones released into the medium by germinated spores of the arbuscular mycorrhizal fungus Rhizophagus irregularis. We detected the presence of a cytokinin (isopentenyl adenosine) and an auxin (indole-acetic acid). In addition, we identified a gibberellin (gibberellin A4) in spore extracts. We also used gas chromatography to show that R. irregularis produces ethylene from methionine and the ?-keto ?-methylthio butyric acid pathway. These results highlight the possibility for AM fungi to use phytohormones to interact with their host plants, or to regulate their own development.

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Host- and stage-dependent secretome of the arbuscular mycorrhizal fungus Rhizophagus irregularis

Project description:Arbuscular mycorrhizal fungi arguably form the most successful and wide-spread endosymbiosis with plants. In general terms there is very little host-specificity in this interaction, indicating an extremely broad compatibility. However, host preferences as well as varying symbiotic efficiencies have been observed, the molecular basis of which is still largely unknown. Secreted proteins (SPs) may act as fungal effectors to control symbiotic efficiency in a host-dependent manner. Therefore, we studied whether AM fungi adjust their secretome in a host- and stage-dependent manner to contribute to their extremely wide host-range. We investigated the expression of SP encoding genes of R. irregularis DAOM197198 in three evolutionary distantly related plant species, Medicago truncatula (Medicago), Nicotiana benthamiana (Nicotiana) and Allium schoenoprasum (Chives). In addition we used laser microdissection in combination with RNAseq to study SP expression at different stages of the symbiotic interaction in Medicago. Our data indicate that the vast majority of 288 expressed SPs show equal expression levels in the interaction with all three host plants. In addition, a subset (~15%) of the SPs show significant differential expression depending on the host plant and/or environmental condition. This host-dependent expression appears to be controlled locally in the hyphal network in response to host metabolic cues. Overall, this study offers a comprehensive analysis of the R. irregularis secretome, which now offers a solid basis to direct functional studies on the role of fungal SPs in AM symbiosis.

2018-03-27 | GSE99655 | GEO

RiCRN1, a Crinkler Effector From the Arbuscular Mycorrhizal Fungus Rhizophagus irregularis, Functions in Arbuscule Development.

Project description:Arbuscular mycorrhizal (AM) symbiosis is one of the most prominent and beneficial plant-microbe interactions that facilitates mineral nutrition and confers tolerance to biotic and abiotic stresses. AM fungi colonize the root cortex and develop specialized structures called arbuscules where the nutrient exchange takes place. Arbuscule development is a highly controlled and coordinated process requiring the involvement of many plant proteins recruited at that interface. In contrast, much less is known about the fungal proteins involved in this process. Here, we have identified an AM fungal effector that participates in this developmental step of the symbiosis. RiCRN1 is a crinkler (CRN) effector that belongs to a subfamily of secreted CRN proteins from R. irregularis. CRNs have been so far only functionally characterized in pathogenic microbes and shown to participate in processes controlling plant cell death and immunity. RiCRN1 accumulates during symbiosis establishment parallel to MtPT4, the gene coding for an arbuscule-specific phosphate transporter. Expression in Nicotiana benthamiana leaves and in Medicago truncatula roots suggest that RiCRN1 is not involved in cell death processes. RiCRN1 dimerizes and localizes to nuclear bodies, suggesting that, similar to other CRNs, it functions in the plant nucleus. Downregulation of RiCRN1 using host-induced gene silencing led to an impairment of the symbiosis in M. truncatula and to a reduction of MtPT4, while ectopic expression of RiCRN1, surprisingly, led to a drastic reduction in arbuscule size that correlated with a decrease not only in MtPT4 but also in MtBCP1, a marker for initial stages of arbuscule development. Altogether, our results suggest that a tightly regulated expression in time and space of RiCRN1 is critical for symbiosis progression and for the proper initiation of arbuscule development.

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Project description:Arbuscular mycorrhizal fungi (AMF) are plant symbionts that have a pivotal role in maintaining soil fertility and nutrient cycling. However, these microsymbionts may be exposed to organic pollutants like pesticides or veterinary drugs known to occur in agricultural soils. Anthelminthics are veterinary drugs that reach soils through the application of contaminated manures in agricultural settings. Their presence might threaten the function of AMF, considered as sensitive indicators of the toxicity of agrochemicals to the soil microbiota. We determined the impact of the anthelminthic compounds albendazole and ivermectin on the establishment and functionality of the symbiosis between the model-legume Lotus japonicus and the AMF Rhizophagus irregularis. Our analyses revealed negative effects of albendazole on the development and functionality of arbuscules, the symbiotic organelle of AMF, at a concentration of 0.75 μg g-1. The impairment of the symbiotic function was verified by the reduced expression of genes SbtM1, PT4 and AMT2;2 involved in arbuscules formation, P and N uptake, and the lower phosphorus shoot content detected in the albendazole-treated plants. Our results provide first evidence for the toxicity of albendazole on the colonization capacity and function of R. irregularis at concentrations that may occur in agricultural soils systematically amended with drug-containing manures.

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GintAMT3 - a Low-Affinity Ammonium Transporter of the Arbuscular Mycorrhizal Rhizophagus irregularis.

Project description:Nutrient acquisition and transfer are essential steps in the arbuscular mycorrhizal (AM) symbiosis, which is formed by the majority of land plants. Mineral nutrients are taken up by AM fungi from the soil and transferred to the plant partner. Within the cortical plant root cells the fungal hyphae form tree-like structures (arbuscules) where the nutrients are released to the plant-fungal interface, i.e., to the periarbuscular space, before being taken up by the plant. In exchange, the AM fungi receive carbohydrates from the plant host. Besides the well-studied uptake of phosphorus (P), the uptake and transfer of nitrogen (N) plays a crucial role in this mutualistic interaction. In the AM fungus Rhizophagus irregularis (formerly called Glomus intraradices), two ammonium transporters (AMT) were previously described, namely GintAMT1 and GintAMT2. Here, we report the identification and characterization of a newly identified R. irregularis AMT, GintAMT3. Phylogenetic analyses revealed high sequence similarity to previously identified AM fungal AMTs and a clear separation from other fungal AMTs. Topological analysis indicated GintAMT3 to be a membrane bound pore forming protein, and GFP tagging showed it to be highly expressed in the intraradical mycelium of a fully established AM symbiosis. Expression of GintAMT3 in yeast successfully complemented the yeast AMT triple deletion mutant (MATa ura3 mep1? mep2?::LEU2 mep3?::KanMX2). GintAMT3 is characterized as a low affinity transport system with an apparent Km of 1.8 mM and a V max of 240 nmol(-1) min(-1) 10(8) cells(-1), which is regulated by substrate concentration and carbon supply.

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Reciprocal recombination genomic signatures in the symbiotic arbuscular mycorrhizal fungi Rhizophagus irregularis.

Project description:Arbuscular mycorrhizal fungi (AMF) are part of the most widespread fungal-plant symbiosis. They colonize at least 80% of plant species, promote plant growth and plant diversity. These fungi are multinucleated and contain either one or two haploid nuclear genotypes (monokaryon and dikaryon) identified by the alleles at a putative mating-type locus. This taxon has been considered as an ancient asexual scandal because of the lack of observable sexual structures. Despite identification of a putative mating-type locus and functional activation of genes related to mating when two isolates co-exist, it remains unknown if the AMF life cycle involves a sexual or parasexual stage. We used publicly available genome sequences to test if Rhizophagus irregularis dikaryon genomes display signatures of sexual reproduction in the form of reciprocal recombination patterns, or if they display exclusively signatures of parasexual reproduction involving gene conversion. We used short-read and long-read sequence data to identify nucleus-specific alleles within dikaryons and then compared them to orthologous gene sequences from related monokaryon isolates displaying the same putative MAT-types as the dikaryon. We observed that the two nucleus-specific alleles of the dikaryon A5 are more related to the homolog sequences of monokaryon isolates displaying the same putative MAT-type than between each other. We also observed that these nucleus-specific alleles displayed reciprocal recombination signatures. These results confirm that dikaryon and monokaryon isolates displaying the same putative MAT-type are related in their life-cycle. These results suggest that a genetic exchange mechanism, involving reciprocal recombination in dikaryon genomes, allows AMF to generate genetic diversity.

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