Serendipita indica changes host sugar and defense status in Arabidopsis thaliana: cooperation or exploitation?

MAIN CONCLUSION: Manipulation of sugar metabolism upon S. indica root colonization triggers changes in sugar pools and defense responses in A. thaliana. ABSTRACT: Serendipita indica is an endophytic fungus that establishes mutualistic relationships with many different plants including important crops as well as the model plant A. thaliana. Successful root colonization typically results in growth promotion and enhanced tolerance against various biotic and abiotic stresses. The fungus delivers phosphorus to the host and receives in exchange carbohydrates. There are hints that S. indica prefers hexoses, glucose, and fructose, products of saccharose cleavage driven by invertases (INVs) and sucrose synthases (SUSs). Carbohydrate metabolism in this interaction, however, remains still widely unexplored. Therefore, in this work, the sugar pools as well as the expression of SUSs and cytosolic INVs in plants colonized by S. indica were analyzed. Using sus1/2/3/4 and cinv1/2 mutants the importance of these genes for the induction of growth promotion and proper root colonization was demonstrated. Furthermore, the expression of several defense-related marker genes in both multiple mutants in comparison to the wild-type plants was determined. Our results show that in colonized A. thaliana plants S. indica manipulates the sugar metabolism by altering the expression of host’s INV and SUS and modulates both the sugar pools and plant defense in its favor. We conclude that the interaction A. thaliana–S. indica is a balancing act between cooperation and exploitation, in which sugar metabolism plays a crucial role. Small changes in this mechanism can lead to severe disruption resulting in the lack of growth promotion or altered colonization rate. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00425-021-03587-3.