Auxin Controls Root Gravitropic Response by Affecting Starch Granule Accumulation and Cell Wall Modification in Tomato

The gravitropic growth of roots is crucial for plants to adapt to terrestrial environments and acquire nutrients from the soil. Tomatoes are a vital economic crop that requires abundant water and nutrients for growth and development. However, there are few reports on the regulatory mechanisms of tomato root gravitropism, particularly auxin-mediated root gravitropic growth. Here, we revealed the signaling pathway of auxin regulating tomato root gravity response through exogenous auxin and auxin inhibitor treatment combined with transcriptome profiling. Our data underscore the necessity of auxin biosynthesis, transport, and optimal levels for the gravitropic growth of tomato roots. Treatment with exogenous auxin or auxin biosynthesis inhibitors diminished gravitropic response in tomato roots. Conversely, treatment with an auxin transport inhibitor led to a robust agravitropic response. Furthermore, we observed that auxin controls root gravitropic growth by establishing concentration gradients and influences root perception of gravity signals by positively regulating starch granule accumulation. Treatment with the exogenous auxin NAA heightened starch synthesis, while exogenous application of the auxin biosynthesis inhibitor yucasin dampened starch synthesis in tomato roots. Our study observed a slow gravitropic response in cultivated cherry tomato (Aisheng) roots. Time series analysis showed that tomato roots bend toward gravity at a slower rate. Transcriptome analysis revealed that many (2770) differentially expressed genes (DEGs) were identified in roots following 36 h of gravity stimulation. In contrast, only 58 DEGs were detected after 3 h of gravity stimulation, further supporting the slow gravitropic response phenotype of tomato roots. GO and KEGG analysis highlighted auxin response, starch and sugar metabolism, and cell wall modification as the major regulatory pathways involved in the gravitropic response and growth of tomato roots. Our results indicate that auxin mediates root sensing of gravity signals through feedback regulation of starch accumulation and controls root gravitropic bending by regulating the expression of cell wall modification-related genes.