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

Abstract

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.

Unearthing the plant–microbe quid pro quo in root associations with beneficial fungi

“…Although the molecular bases for these nutrient transfers on the fungal side are not yet clear, the involvement of the fungal sulphate transporter SiSulT (Narayan et al ., 2021), the iron transporter PiFTR (Verma et al ., 2021) and the phosphate transporter PiPT (Kumar et al ., 2011) is strongly suspected. Reciprocal C transfer from the plant to the fungus has not been proven, but it is known that the fungus alters C metabolism in A. thaliana , which could mediate the uptake of monosaccharides from the plant by the fungus (Opitz et al ., 2021).…”

Environmental Stress Determines The Colonization and Impact of An Endophytic Fungus On Invasive Knotweed

“…through the production of defense compounds or secondary metabolites inhibiting microbial growth (Zipfel & Oldroyd, 2017), or by diverting more carbohydrates to fungal symbionts (Carbonnel & Gutjahr, 2014;Martin et al, 2017). This has also been shown for the closely related S. indica which interferes with the immune system of host plants (Jacobs et al, 2011) and in uences sugar concentrations in their roots (Opitz et al, 2021). The functional and adaptive explanation for this is usually that plant bene ts from interactions with fungi are environmentdependent, and therefore plants stimulate or restrict fungal access depending on these bene ts.…”

Environmental stress determines the colonization and impact of an endophytic fungus on invasive knotweed

“…through the production of defense compounds or secondary metabolites inhibiting microbial growth (Zipfel & Oldroyd, 2017), or by diverting more carbohydrates to fungal symbionts (Carbonnel & Gutjahr, 2014;Martin et al, 2017). This has also been shown for the closely related S. indica which interferes with the immune system of host plants (Jacobs et al, 2011) and influences sugar concentrations in their roots (Opitz et al, 2021).…”

“…The copyright holder for this preprint this version posted September 16, 2021. ; https://doi.org/10.1101/2021.09.10.459653 doi: bioRxiv preprint 13 (Jacobs et al, 2011) and influences sugar concentrations in their roots (Opitz et al, 2021).…”