Living off the fat of the plant: Powdery mildew fungi thrive on host thylakoid lipids

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“Eat healthy fats!” is a familiar mantra to promote a balanced diet. It highlights the human need for polyunsaturated fatty acids such as omega-3. Biochemically, omega-3 describes a double bond within a fatty acid chain 3 atoms away from the terminal methyl group. A common example of an omega-3 fatty acid is α-linolenic acid, a carboxylic acid with an 18-carbon chain and 3 cis double bonds (18:3). Essential fats such as α-linolenic acid are vital for human metabolism, and we typically obtain these lipids from plant-based foods like nuts, seeds, and oils.

Interestingly, in this respect, humans have something in common with powdery mildew fungi. These notorious plant parasites are named after the eponymous symptoms they cause on the surface of above-ground plant parts. As obligate biotrophs, powdery mildew fungi rely on living host cells for nutrients, which they extract using specialized feeding structures called haustoria. These structures form 1 day after infection and resemble tiny, inflated laboratory gloves within host epidermal cells. By 3 to 7 days post infection, the fungi produce spores on the plant surface that create the characteristic powdery appearance (Kuhn et al. 2016). The spores are filled with plant-derived lipid bodies that provide energy reservoirs for future infections (Jiang et al. 2017).

In new work, Hang Xue, Johan Jaenisch, and colleagues (Xue et al. 2025) unmasked how powdery mildew fungi manipulate host plant metabolism to extract thylakoid lipids for their own benefit. Using the Arabidopsis thaliana-Golovinomyces orontii pathosystem, the authors investigated the accumulation of lipids in infected rosette leaves. They observed a 3.5-fold increase in triacylglycerols (TAGs) in infected wild-type A. thaliana plants 12 days post inoculation, with a notable enrichment of unsaturated fatty acids, including 18:2 and 18:3. The authors then searched for 16:3 fatty acids, which are specific to the chloroplast. TAGs containing these fatty acids were indeed enriched in infected leaves, suggesting chloroplasts as the primary lipid source for powdery mildew fungi.

TAGs are storage lipids composed of 3 fatty acids attached to a central glycerol backbone. In eukaryotes, the final and rate-limiting step of TAG synthesis is catalyzed by diacylglycerol transferases (DGAT) in the endoplasmic reticulum (Xu et al. 2020). The authors tested whether loss-of-function of the canonical A. thaliana DGATs, DGAT1 and DGAT2, hinders powdery mildew spore production. Strikingly, after infection with G. orontii, dgat2 mutants showed no significant difference in spore accumulation, while dgat1 mutants showed enhanced powdery mildew spore development compared with Col-0 wild-type plants (see Figure).

Unlike DGAT1 and DGAT2, A. thaliana DGAT3 has an N-terminal chloroplast transport signal. The authors confirmed chloroplast localization using fluorophore-labeled DGAT3 in Nicotiana benthamiana and found that DGAT3 knockdown or knockout reduced powdery mildew spore production by 20% to 50%. Notably, DGAT3 prefers 18:2 and 18:3 substrates (Hernández et al. 2012), which were considerably reduced in chloroplast TAGs of infected dgat3 mutants compared with infected wild-type leaves.

Plants deprived of DGAT3 did not show constitutive activation of plant defense. Thus, the authors concluded that reduced spore production on dgat3 mutants is due to decreased TAG production in chloroplasts. By contrast, DGAT1 reduces spore production by limiting substrates for chloroplast TAG synthesis (see Figure) and/or by contributing to the presence of endoplasmic reticulum-derived lipid droplets, containing defense compounds.

In this work, the authors uncovered the role of DGAT3 in obligate biotrophy and lipid metabolism. Among other findings, their results open the interesting perspective of leveraging powdery mildew infection to study plant lipid metabolism. This approach may also support engineering plant TAG profiles enriched in fatty acids essential for a balanced human diet.

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