La2O3 Nanoparticles Can Cause Cracking of Tomato Fruit through Genetic Reconstruction

La2O3 nanoparticles (NPs) have shown great potential in agriculture, but cracking of plant sensitive tissue could occur during application, resulting in a poor appearance, facilitating entry for insects and fungi, and increasing economic losses. Herein, exocarp cracking mechanisms of tomato (Solanum lycopersicum L.) fruit in response to La2O3 NPs were investigated. Tomato plants were exposed to La2O3 NPs (0–40 mg/L, 90 days) by a split-root system under greenhouse condition. La2O3 NPs with high concentrations (25 and 40 mg/L) increased the obvious cracking of the fruit exocarp by 20.0 and 22.7%, respectively. After exposure to 25 mg/L La2O3 NPs, decreased thickness of the cuticle and cell wall and lower wax crystallization patterns of tomato fruit exocarp were observed. Biomechanical properties (e.g., firmness and stiffness) of fruit exocarp were decreased by 34.7 and 25.9%, respectively. RNA-sequencing revealed that the thinner cuticle was caused by the downregulation of cuticle biosynthesis related genes; pectin remodeling, including the reduction in homogalacturonan (e.g., LOC101264880) and rhamnose (e.g., LOC101248505), was responsible for the thinner cell wall. Additionally, genes related to water and abscisic acid homeostasis were significantly upregulated, causing the increases of water and soluble solid content of fruit and elevated fruit inner pressure. Therefore, the thinner fruit cuticle and cell wall combined with the higher inner pressure caused fruit cracking. This study improves our understanding of nanomaterials on important agricultural crops, including the structural reconstruction of fruit exocarp contributing to NPs-induced cracking at the molecular level.