As members of the plant microbiota, arbuscular mycorrhizal fungi (AMF, Glomeromycotina) symbiotically colonize plant roots. AMF also possess their own microbiota, hosting some uncultivable endobacteria. Ongoing research has revealed the genetics underlying plant responses to colonization by AMF, but the fungal side of the relationship remains in the dark. Here, we sequenced the genome of Gigaspora margarita, a member of the Gigasporaceae in an early diverging group of the Glomeromycotina. In contrast to other AMF, G. margarita may host distinct endobacterial populations and possesses the largest fungal genome so far annotated (773.104 Mbp), with more than 64% transposable elements. Other unique traits of the G. margarita genome include the expansion of genes for inorganic phosphate metabolism, the presence of genes for production of secondary metabolites and a considerable number of potential horizontal gene transfer events. The sequencing of G. margarita genome reveals the importance of its immune system, shedding light on the evolutionary pathways that allowed early diverging fungi to interact with both plants and bacteria.
Several studies have investigated soil microbial biodiversity, but understanding of the mechanisms underlying plant responses to soil microbiota remains in its infancy. Here, we focused on tomato (Solanum lycopersicum), testing the hypothesis that plants grown on native soils display different responses to soil microbiotas. Using transcriptomics, proteomics, and biochemistry, we describe the responses of two tomato genotypes (susceptible or resistant to Fusarium oxysporum f. sp. lycopersici) grown on an artificial growth substrate and two native soils (conducive and suppressive to Fusarium). Native soils affected tomato responses by modulating pathways involved in responses to oxidative stress, phenol biosynthesis, lignin deposition, and innate immunity, particularly in the suppressive soil. In tomato plants grown on steam-disinfected soils, total phenols and lignin decreased significantly. The inoculation of a mycorrhizal fungus partly rescued this response locally and systemically. Plants inoculated with the fungal pathogen showed reduced disease symptoms in the resistant genotype in both soils, but the susceptible genotype was partially protected from the pathogen only when grown on the suppressive soil. The 'state of alert' detected in tomatoes reveals novel mechanisms operating in plants in native soils and the soil microbiota appears to be one of the drivers of these plant responses.
Climate changes include the intensification of drought in many parts of the world, increasing its frequency, severity and duration. However, under natural conditions, environmental stresses do not occur alone, and, in addition, more stressed plants may become more susceptible to attacks by pests and pathogens. Studies on the impact of the arbuscular mycorrhizal (AM) symbiosis on tomato response to water deficit showed that several drought-responsive genes are differentially regulated in AM-colonized tomato plants (roots and leaves) during water deficit. To date, global changes in mycorrhizal tomato root transcripts under water stress conditions have not been yet investigated. Here, changes in root transcriptome in the presence of an AM fungus, with or without water stress (WS) application, have been evaluated in a commercial tomato cultivar already investigated for the water stress response during AM symbiosis. Since root-knot nematodes (RKNs, Meloidogyne incognita ) are obligate endoparasites and cause severe yield losses in tomato, the impact of the AM fungal colonization on RKN infection at 7 days post-inoculation was also evaluated. Results offer new information about the response to AM symbiosis, highlighting a functional redundancy for several tomato gene families, as well as on the tomato and fungal genes involved in WS response during symbiosis, underlying the role of the AM fungus. Changes in the expression of tomato genes related to nematode infection during AM symbiosis highlight a role of AM colonization in triggering defense responses against RKN in tomato. Overall, new datasets on the tomato response to an abiotic and biotic stress during AM symbiosis have been obtained, providing useful data for further researches.
Summary As other arbuscular mycorrhizal fungi, Gigaspora margarita contains unculturable endobacteria in its cytoplasm. A cured fungal line has been obtained and showed it was capable of establishing a successful mycorrhizal colonization. However, previous OMICs and physiological analyses have demonstrated that the cured fungus is impaired in some functions during the pre‐symbiotic phase, leading to a lower respiration activity, lower ATP, and antioxidant production. Here, by combining deep dual‐mRNA sequencing and proteomics applied to Lotus japonicus roots colonized by the fungal line with bacteria (B+) and by the cured line (B−), we tested the hypothesis that L. japonicus (i) activates its symbiotic pathways irrespective of the presence or absence of the endobacterium, but (ii) perceives the two fungal lines as different physiological entities. Morphological observations confirmed the absence of clear endobacteria‐dependent changes in the mycorrhizal phenotype of L. japonicus, while transcript and proteomic datasets revealed activation of the most important symbiotic pathways. They included the iconic nutrient transport and some less‐investigated pathways, such as phenylpropanoid biosynthesis. However, significant differences between the mycorrhizal B+/B− plants emerged in the respiratory pathways and lipid biosynthesis. In both cases, the roots colonized by the cured line revealed a reduced capacity to activate genes involved in antioxidant metabolism, as well as the early biosynthetic steps of the symbiotic lipids, which are directed towards the fungus. Similar to its pre‐symbiotic phase, the intraradical fungus revealed transcripts related to mitochondrial activity, which were downregulated in the cured line, as well as perturbation in lipid biosynthesis.
Traditionally, the most popular sentences used to describe the arbuscular mycorrhizal symbiosis sound like: "AM fungi form one of the most widespread root symbioses, associating with 80% of land plants. In this symbiosis, the fungus provides the plant host with mineral nutrients, especially phosphate, receiving in turn carbohydrates. " In the last years, the mycorrhiza research field has witnessed a big step forward in the knowledge of the physiology and the mechanisms governing this important symbiosis, that helped plants colonizing the lands more than 400 MYA. The huge expansion of the-omics studies produced the first results on the fungal side, with genomes and transcriptomes of AM fungi being published. In parallel, the need for more sustainable agricultural practices has boosted the research in the field of the plant symbioses, with the final aim of improving plant productivity employing symbiotic microbes as bioinoculants. Beside all the other (positive) effects that mycorrhizal fungi exert on plants, the nutrient exchange is considered as the keystone, and the core mechanism governing this symbiosis. This review will focus on the molecular determinants underneath this exchange, both on the fungal and the plant side. Coming back to the sentence that claims this symbiosis as based on phosphate provided to the plant in return to carbohydrate, we will find that some concepts of this view still stand, while some others have been partly revolutionized.
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