An Uncanonical CCCH-Tandem Zinc-Finger Protein Represses Secondary Wall Synthesis and Controls Mechanical Strength in Rice.

Secondary walls, which represent the bulk of biomass, have a large impact on plant growth and adaptation to environments. Secondary wall synthesis is switched and regulated by a sophisticated signaling transduction network. However, there is limited understanding of these regulatory pathways. Here, we report that ILA1-interacting protein 4 (IIP4) can repress secondary wall synthesis. IIP4 is a phosphorylation substrate of an Raf-like MAPKKK, but its function is unknown. By generating iip4 mutants and relevant transgenic plants, we found that lesions in IIP4 enhance secondary wall formation. Gene expression and transactivation activity assays revealed that IIP4 negatively regulates the expression of MYB61 and CESAs but does not bind their promoters. IIP4 interacts with NAC29/NAC31, the upstream regulators of secondary wall synthesis, and suppresses the downstream regulatory pathways in plants. Mutagenesis analyses showed that phosphomimic IIP4 proteins translocate from the nucleus to the cytoplasm, which releases interacting NACs and attenuates its repression function. Moreover, we revealed that IIPs are evolutionarily conserved and share unreported CCCH motifs, referred to as uncanonical CCCH-tandem zinc-finger proteins. Collectively, our study provides mechanistic insights into the control of secondary wall synthesis and presents an opportunity for improving relevant agronomic traits in crops.