Symbiotic responses of Lotus japonicus to two isogenic lines of a mycorrhizal fungus differing in the presence/absence of an endobacterium.

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. Significance Statement: Using two isogenic lines of Gigaspora margarita, one containing and one lacking an endobacterium, for the first time we demonstrate that an endosymbiont hosted within the cytoplasm of an arbuscular mycorrhizal fungus has an impact on the regulatory networks of the plant host. OMICs analyses revealed that Lotus japonicus perceives the physiological differences between the two fungal isogenic lines; the absence of the bacterium leads to perturbation in mycorrhiza‐relevant pathways, which are associated with plant mitochondria and plastids. [ABSTRACT FROM AUTHOR]