Heterotrimeric G-proteins influence almost all aspects of plant growth, development, and responses to biotic and abiotic stresses in plants, likely via their interaction with specific effectors. However, the identity of such effectors and their mechanism of action are mostly unknown. While investigating the roles of different G-protein subunits in modulating the oil content in Camelina (Camelina sativa), an oil seed crop, we uncovered a role of Gb proteins in controlling anisotropic cell expansion. Knockdown of Gb genes causes reduced longitudinal and enhanced transverse expansion, resulting in altered cell, tissue, and organ shapes in transgenic plants during vegetative and reproductive development. These plants also exhibited substantial changes in their fatty acid and phospholipid profiles, which possibly leads to the increased oil content of the transgenic seeds. This increase is potentially caused by the direct interaction of Gb proteins with a specific patatin-like phospholipase, pPLAIIId. Camelina plants with suppressed Gb expression exhibit higher lipase activity, and show phenotypes similar to plants overexpressing pPLAIIId, suggesting that the Gb proteins are negative regulators of pPLAIIId. These results reveal interactions between the G-protein-mediated and lipid signaling/metabolic pathways, where specific phospholipases may act as effectors that control key developmental and environmental responses of plants.