A Major Role of Class III HD-ZIPs in Promoting Sugar Beet Cyst Nematode Syncytium Formation in Arabidopsis

Cyst nematodes use a stylet to secrete plant CLE-like peptide effector mimics into selected root cells of host plants to hijack CLE signaling pathways for feeding site (syncytium) formation. Here, we identified ATHB8, a HD-ZIP III family transcription factor, as a downstream component of the CLE signaling pathway in syncytium formation. ATHB8 is expressed in the early stages of syncytium initiation, and then transitions to neighboring cells of the syncytium as it expands; an expression pattern coincident with auxin response at the infection site. Conversely, MIR165a, which expresses in endodermal cells and moves into the vasculature to suppress HD-ZIP III TFs, is down-regulated near the infection site. Knocking down HD-ZIP III TFs by inducible over-expression of MIR165a in Arabidopsis dramatically reduced female development of the sugar beet cyst nematode (Heterodera schachtii). HD-ZIP III TFs are known to function downstream of auxin to promote cellular quiescence and define stem cell organizer cells in vascular patterning. Taken together, our results suggest that HD-ZIP III TFs may function as a connecting point for CLE and auxin signaling pathways in promoting syncytium formation, possibly by inducing root cells into a quiescent status and priming them for initial syncytial cell establishment and/or subsequent cellular incorporation.