Soybean Auxin Transporter PIN3 Regulates Nitrate Acquisition to Improve Nitrogen Use and Seed Traits

Enhancing nitrogen-use efficiency is essential for boosting crop yields and advancing sustainable agriculture, particularly in the absence of synthetic fertilizers. Despite the inherent nitrogen-fixation capacity of the staple legume crop soybean (Glycine max) by symbiotic rhizobia, improving nitrogen use has been challenging. Here, a role for the auxin-efflux transporters PIN3a and PIN3b in soybean nitrate acquisition is uncovered. PIN3a/b localizes to the plasma membrane, and high environmental nitrate induces PIN3a degradation and its accumulation at cell junctions. Disrupting PIN3 homologs results in auxin over-accumulation, impairs pavement-cell polarity, and enhances signaling via the transcription factors ARF and STF3/4. These transcription factors separately bind to and activate the NPF2.13 promoter, thereby strengthening nitrate uptake. pin3ab and pin3abd mutants have enhanced nitrate acquisition and resistant to high nitrate on pavement-cell growth. The elevated nitrogen accumulation translates to higher oil contents in pin3ab mutant seeds in an elite cultivar background across multiple years and field locations. The findings shed light on the regulation of nitrate uptake in crop-plant development and demonstrate the unexpected potential of manipulating auxin transporters to enhance soybean nitrogen-use efficiency and agronomic performance.