ZmARF1 positively regulates low phosphorus stress tolerance via modulating lateral root development in maize

Phosphorus (P) deficiency is one of the most critical factors for plant growth and productivity, including its inhibition of lateral root initiation. Auxin response factors (ARFs) play crucial roles in root development via auxin signaling mediated by genetic pathways. In this study, we found that the transcription factor ZmARF1 was associated with low inorganic phosphate (Pi) stress-related traits in maize. This superior root morphology and greater phosphate stress tolerance could be ascribed to the overexpression of ZmARF1. The knock out mutant zmarf1 had shorter primary roots, fewer root tip number, and lower root volume and surface area. Transcriptomic data indicate that ZmLBD1, a direct downstream target gene, is involved in lateral root development, which enhances phosphate starvation tolerance. A transcriptional activation assay revealed that ZmARF1 specifically binds to the GC-box motif in the promoter of ZmLBD1 and activates its expression. Moreover, ZmARF1 positively regulates the expression of ZmPHR1, ZmPHT1;2, and ZmPHO2, which are key transporters of Pi in maize. We propose that ZmARF1 promotes the transcription of ZmLBD1 to modulate lateral root development and Pi-starvation induced (PSI) genes to regulate phosphate mobilization and homeostasis under phosphorus starvation. In addition, ZmERF2 specifically binds to the ABRE motif of the promoter of ZmARF1 and represses its expression. Collectively, the findings of this study revealed that ZmARF1 is a pivotal factor that modulates root development and confers low-Pi stress tolerance through the transcriptional regulation of the biological function of ZmLBD1 and the expression of key Pi transport proteins. Phosphorus (P) is a critical macronutrient for plant growth and development. Root system architecture (RSA) affects the ability of plants to obtain water and mineral nutrients from soil. Several auxin response factors (ARFs) are involved in auxin signaling and lateral root (LR) formation in P-deficient plants, but the molecular mechanisms underlying P deficiency-induced changes in the RSA of maize is not well understood. We found that ZmARF1 positively regulates root development and confers tolerance to low inorganic phosphate (Pi) stress in maize. ZmARF1 regulates root development by interacting with the promoter of ZmLBD1 and positively regulating its expression. Furthermore, we empirically revealed that ZmARF1 enhanced Pi mobilization under low Pi stress by positively regulating the expression of ZmPHR1, ZmPHT1;2, and ZmPHO2, which are key Pi transporters in the Pi transport machinery of maize. Overall, enhanced root development and expression of key Pi transporter proteins have been suggested as key nexuses mediating the biological function of ZmARF1 in conferring low-Pi stress tolerance in maize.