P-body formation is required for yeast proliferation in the phyllosphere

Processing bodies (P-bodies) are major cytosolic ribonucleoprotein granules involved in post-transcriptional regulation. Yeast has been an invaluable model for elucidating the functions of P-bodies under laboratory conditions. However, the physiological significance of P-bodies in natural environments remains unclear. Here, we demonstrate that P-body formation is required for yeast proliferation in the phyllosphere, the aerial parts of plants. Deletion of EDC3 , a gene critical for P-body formation, impaired proliferation of the methanol-utilizing yeast Candida boidinii on Arabidopsis thaliana leaves where the yeast assimilates methanol as the carbon source while adapting to changes in environmental conditions. In vitro experiments showed that P-bodies contribute to the spatiotemporal regulation of methanol-induced mRNAs (mimRNAs). These mimRNAs form cytosolic dot structures (termed mimRNA granules) that harbor multiple kinds of mimRNAs. In the edc3Δ strain, the formation of mimRNA granules was reduced along with a decrease in mimRNA abundance. Under oxidative stress, colocalization of P-bodies with mimRNA granules markedly increased and growth of the edc3Δ strain on methanol was suppressed, suggesting active sequestration of mimRNAs within P-bodies as a stress tolerance response. Time-lapse microscopy revealed dynamic interactions between P-bodies and mimRNAs granules with transient colocalization. Together, our findings indicate that P-bodies function as temporal storage sites where mimRNAs are protected from degradation in the phyllosphere.