Chromosome doubling increases <i>PECTIN METHYLESTERASE 2</i> expression, biomass, and osmotic stress tolerance in kiwifruit

Chromosome doubling-induced polyploidization is a popular tool for crop breeding. Polyploidy crops commonly have multiple advantages, including increased biomass and stress tolerance. However, little is known about the genes responsible for these advantages. We found kiwifruit (Actinidia chinensis cv. Hongyang) PECTIN METHYLESTERASE 2 (AcPME2) is substantially upregulated in artificially created tetraploid plants that show increased biomass and enhanced tolerance to osmotic stress. Overexpression (OE) of AcPME2 led to increased biomass and enhanced stress tolerance in Arabidopsis (Arabidopsis thaliana), tomato (Solanum lycopersicum), and kiwifruit. Upon short-term osmotic stress treatment, AcPME2-OE plants showed higher levels of demethylesterified pectins and more Ca2+ accumulation in the cell wall than Col-0 plants, which led to increased cell wall stiffness. The stress-induced plasmolysis assays indicated that AcPME2 dynamically mediated the cell wall stiffness in response to osmotic stress, which is dependent on Ca2+ accumulation. Transcriptomic analysis discovered that dozens of stress-responsive genes were significantly upregulated in the AcPME2-OE plants under osmotic stress. Besides, AcPME2-mediated cell wall reinforcement prevented cell wall collapse and deformation under osmotic stress. Our results revealed a single gene contributes to two advantages of polyploidization (increased biomass and osmotic stress tolerance) and that AcPME2 dynamically regulates cell wall stiffness in response to osmotic stress.