Emerging Arabidopsis roots exhibit hypersensitive gravitropism associated with distinctive auxin synthesis and polar transport within the elongation zone

Gravitropism is crucial for plants to secure light, water, and minerals essential for developing seedlings. Despite its importance, the gravitropism of young roots remains largely unexplored. Herein, we reported that the emerging Arabidopsis roots exhibit hypersensitive gravitropism compared to mature roots, growing relatively slowly but bending exceptionally rapidly. This rapid gravibending is characterized by substantial growth inhibition and a distinctive auxin accumulation on the lower side of the elongation zone. Intriguingly, surgical experiments suggest that these auxins predominantly originate from the elongation zone rather than from the shoot or root cap. However, their asymmetrical distribution is heavily modulated by the root cap. Confocal analysis of GFP-tagged TAA1 further confirms that gravitational stimulus induces active auxin biosynthesis in the elongation zone of nascent roots but not in mature roots. Furthermore, mutations in the PIN proteins, especially PIN2, severely impair the rapid gravitropic responses in emerging roots. Interestingly, PIN2 in nascent roots is not confined to the epidermis and cortex but extends to the endodermis, contrasting with its distribution in mature roots. Gravitational stimulation leads to a marked asymmetrical distribution of PIN2 between the upper and lower sides of the roots, which is strongly inhibited by surgical removal of the root cap. These observations indicate that gravitational stimulation triggers active auxin synthesis and PIN protein-mediated lateral transport within the elongation zone of emerging roots, resulting in swift gravitropic responses. These results offer an intriguing enhancement and expansion to the mechanism of root gravitropism.