Arabidopsis Restricts Sugar Loss to a Colonizing Trichoderma harzianum Strain by Downregulating SWEET11 and -12 and Upregulation of SUC1 and SWEET2 in the Roots

Phosphate (Pi) availability has a strong influence on the symbiotic interaction between Arabidopsis and a recently described root-colonizing beneficial Trichoderma harzianum strain. When transferred to media with insoluble Ca₃(PO₄)₂ as a sole Pi source, Arabidopsis seedlings died after 10 days. Trichoderma grew on the medium containing Ca₃(PO₄)₂ and the fungus did colonize in roots, stems, and shoots of the host. The efficiency of the photosynthetic electron transport of the colonized seedlings grown on Ca₃(PO₄)₂ medium was reduced and the seedlings died earlier, indicating that the fungus exerts an additional stress to the plant. Interestingly, the fungus initially alleviated the Pi starvation response and did not activate defense responses against the hyphal propagation. However, in colonized roots, the sucrose transporter genes SWEET11 and -12 were strongly down-regulated, restricting the unloading of sucrose from the phloem parenchyma cells to the apoplast. Simultaneously, up-regulation of SUC1 promoted sucrose uptake from the apoplast into the parenchyma cells and of SWEET2 sequestration of sucrose in the vacuole of the root cells. We propose that the fungus tries to escape from the Ca₃(PO₄)₂ medium and colonizes the entire host. To prevent excessive sugar consumption by the propagating hyphae, the host restricts sugar availability in its apoplastic root space by downregulating sugar transporter genes for phloem unloading, and by upregulating transporter genes which maintain the sugar in the root cells.