Two-step, long-distance nuclear migration guided by distinct actin networks prior to plant root hair formation

Abstract One of the most fundamental tasks for a cell to fulfill its function is to move the nucleus to its proper place through a process known as “nuclear migration.” In plant cells, the nucleus relocates spontaneously in response to developmental and environmental cues. Root hairs are tip-growing projections of root epidermal cells that are required for the acquisition of water and nutrients from the soil. Before its development, the nucleus travels approximately 50 µm across the cell body from the cell center toward the root hair initiation site to support continuous tip growth; however, the dynamics and molecular basis underlying this nuclear migration remain unclear. In this study, we show that long-distance nuclear migration to the root hair initiation site consists of two steps, each driven by distinct F-actin networks. Our cytological and genetic data indicate that the nucleus initially moves downward with the aid of F-actin, which consists of two classes of actin isoforms, ACTIN 7 (ACT7) and ACT2/ACT8, followed by the lateral movement to the root hair initiation site, which is guided by F-actin primarily incorporating ACT2/ACT8. Moreover, RHO-OF-PLANTS small GTPases play an important role in the formation of F-actin, which connects the nucleus to the root hair initiation site, thus facilitating the lateral nuclear movement. This study provides an example of distinct F-actin networks steering the nucleus in a stepwise manner to enable long-distance and precise nuclear migration within plant cells.