Rice Dwarf Virus P2 Protein Hijacks Auxin Signaling by Directly Targeting the Rice OsIAA10 Protein, Enhancing Viral Infection and Disease Development

The phytohormone auxin plays critical roles in regulating myriads of plant growth and developmental processes. Microbe infection can disturb auxin signaling resulting in defects in these processes, but the underlying mechanisms are poorly understood. Auxin signaling begins with perception of auxin by a transient co-receptor complex consisting of an F-box transport inhibitor response 1/auxin signaling F-box (TIR1/AFB) protein and an auxin/indole-3-acetic acid (Aux/IAA) protein. Auxin binding to the co-receptor triggers ubiquitination and 26S proteasome degradation of the Aux/IAA proteins, leading to subsequent events, including expression of auxin-responsive genes. Here we report that Rice dwarf virus (RDV), a devastating pathogen of rice, causes disease symptoms including dwarfing, increased tiller number and short crown roots in infected rice as a result of reduced sensitivity to auxin signaling. The RDV capsid protein P2 binds OsIAA10, blocking the interaction between OsIAA10 and OsTIR1 and inhibiting 26S proteasome-mediated OsIAA10 degradation. Transgenic rice plants overexpressing wild-type or a dominant-negative (degradation-resistant) mutant of OsIAA10 phenocopy RDV symptoms are more susceptible to RDV infection; however, knockdown of OsIAA10 enhances the resistance of rice to RDV infection. Our findings reveal a previously unknown mechanism of viral protein reprogramming of a key step in auxin signaling initiation that enhances viral infection and pathogenesis.

植物激素生长素（auxin）在调控众多植物生长发育过程中发挥关键作用。微生物侵染可干扰生长素信号转导，进而导致上述过程出现缺陷，但其背后的分子机制尚不清楚。生长素信号转导始于瞬时共受体复合物对生长素的感知，该复合物由F盒运输抑制剂响应1/生长素信号F盒（TIR1/AFB）蛋白与生长素/吲哚-3-乙酸（Aux/IAA）蛋白组成。生长素与该共受体结合会触发Aux/IAA蛋白的泛素化及26S蛋白酶体降解，进而引发后续事件，包括生长素响应基因的表达。本研究发现，水稻毁灭性病原水稻矮缩病毒（RDV）可通过降低水稻对生长素信号的敏感性，引发感病植株出现矮化、分蘖数增加及冠根缩短等病害症状。RDV衣壳蛋白P2可结合OsIAA10，阻断OsIAA10与OsTIR1的相互作用，并抑制26S蛋白酶体介导的OsIAA10降解。过表达野生型或显性负效（抗降解）OsIAA10突变体的转基因水稻植株，不仅会重现RDV感染后的病症，且更易感染RDV；而敲低OsIAA10则可增强水稻对RDV的抗性。本研究揭示了一种此前未知的病毒蛋白重编程生长素信号起始关键步骤的机制，该机制可促进病毒侵染与致病过程。