RabE1a- and SEC10b-mediated exocytosis and AP2β-mediated endocytosis are involved in the intracellular transport of tobamoviruses.

To establish systemic infection, plant viruses must replicate, and conduct intra- and intercellular movement and long-distance movement, all of which require the participation of host factors. Tobamoviruses move in the form of movement protein (MP)-viral RNA complex and utilize endocytosis for intracellular movement. However, how tobamoviral MPs hijack host factors to reach the plasma membrane (PM) and then plasmodesmata (PD) is still largely unknown. Tomato brown rugose fruit virus (ToBRFV) is an emerging tobamovirus that mainly infects tomatoes and peppers. Here, we show that tomato RabE1a, a small Rab GTPase, interacts with ToBRFV MP and participates in the movement of ToBRFV. Knocking out RabE1a in tomatoes could inhibit infection by ToBRFV. RabE1a positively regulates MP transport to the PM, and this transport process is regulated by its nucleotide-binding state. Furthermore, RabE1a interacts with the exocyst subunit SEC10b to jointly regulate MP transport to the PM and intracellular movement of ToBRFV. The adaptor protein AP2β interacts with MP and transports MP from the PM to the PD for intercellular movement of ToBRFV. We further find that knocking out RabE1a could also inhibit the infection of other tobamoviruses. In summary, MP exocytosis is coregulated by RabE1a and the exocyst subunit SEC10b for transport to the PM, where it then uses AP2β-regulated endocytosis to PD. These results provide a comprehensive overview of tobamoviral MP intracellular transport and are insightful for breeding tomato plants resistant to ToBRFV and related tobamoviruses.