Potato purple top phytoplasma infection induces autophagy-associated lipid dynamics that support pathogen proliferation

Authors: INABA, JUNICHI - Orise Fellow; Kim, Bo Min; ZHAO, YAN - Retired ARS Employee; Huang, Qi; Wei, Wei

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/20/2026
Publication Date: 8/25/2026
Citation: Inaba, J., Kim, B., Zhao, Y., Huang, Q., Wei, W. 2026. Potato purple top phytoplasma infection induces autophagy-associated lipid dynamics that support pathogen proliferation. Plant Physiology. 202:1-15. https://doi.org/10.1093/plphys/kiag628.
DOI: https://doi.org/10.1093/plphys/kiag628

Interpretive Summary: Phytoplasmas are small, plant-pathogenic bacteria that reduce crop yields and rely on their hosts for essential nutrients, though their nutrient acquisition strategies remain poorly understood. Using phytoplasma infected tomato plants, ARS scientists in Beltsville, Maryland, found that infection alters how the plant manages fats (lipids), which are essential for cell membranes and energy storage. The pathogen activates autophagy, a cellular recycling process, and is associated with the movement of fat storage structures (lipid droplets) toward the bacteria. The decrease in membrane lipids alongside increased storage lipids suggests enhanced membrane turnover and lipid sequestration. When autophagy is inhibited, lipid redistribution is disrupted and bacterial proliferation is reduced, indicating that the pathogen benefits from this host process. In addition, a phytoplasma enzyme capable of breaking down fats is identified, which may further support nutrient acquisition. These findings suggest that phytoplasmas exploit the plant’s recycling system to access nutrients. This work provides new insight into how plant pathogens survive and may help researchers develop new strategies to control phytoplasma-related crop diseases, benefiting both scientists and agriculture.

Technical Abstract: Phytoplasmas are unculturable, phloem-restricted bacterial pathogens responsible for devastating diseases in crops and ornamentals worldwide. Their mechanism for nutrient acquisition from host plants remains largely unknown. This study demonstrated that infection with potato purple top phytoplasma induced extensive remodeling of lipid metabolism in tomato plants, closely linked to autophagy activation. Western blot and confocal analyses revealed increased ATG8 lipidation and autophagosome formation at endoplasmic reticulum stress sites, alongside the redistribution of lipid droplets toward phytoplasma cells. Lipidomic profiling showed a decline in chloroplast galactolipids and phospholipids with a concomitant rise in triacylglycerol, indicating accelerated membrane turnover and neutral lipid sequestration. Transmission electron microscopy further revealed frequent spatial proximity between lipid droplets and phytoplasmas. Inhibition of autophagy with 3-methyladenine blocked lipid droplet breakdown, disrupted endoplasmic reticulum organization, and reduced phytoplasma titers, suggesting that host autophagy contributes to phytoplasma proliferation. In addition, genome analysis identified a conserved phytoplasma-encoded alpha/beta hydrolase (potato purple top-lipase), predicted to be related to monoacylglycerol lipases. In vivo assays in yeast and Nicotiana benthamiana confirmed that potato purple top-lipase reduced neutral lipids, mainly triacylglycerol, and that catalytic triad mutations abolished activity. Because potato purple top-lipase lacks a predicted secretory signal peptide, it likely functions intracellularly within phytoplasma cells and may participate in the metabolism of lipid intermediates. These findings support a model in which phytoplasma infection is associated with host autophagy-associated lipid droplet mobilization and a phytoplasma lipase that may contribute to host-derived lipid resources, providing insight into potential nutrient acquisition strategies of phloem-restricted pathogens.