ZmGDIa-hel counters the RBSDV-induced reduction of active gibberellins to alleviate maize rough dwarf virus disease

Maize rough dwarf disease (MRDD) threatens maize production globally. The P7-1 effector of the rice black-streaked dwarf virus (RBSDV) targets maize Rab GDP dissociation inhibitor alpha (ZmGDIa) to cause MRDD. However, P7-1 has difficulty recruiting a ZmGDIa variant with an alternative helitron-derived exon 10 (ZmGDIa-hel), resulting in recessive resistance. Here, we demonstrate that P7-1 can recruit another maize protein, gibberellin 2-oxidase 13 (ZmGA20x7.3), which also exhibits tighter binding affinity for ZmGDIa than ZmGDIa-hel. The oligomerization of ZmGA20x7.3 is vital for its function in converting bioactive gibberellins into inactive forms. Moreover, the enzymatic activity of ZmGA20x7.3 oligomers increases when forming hetero-oligomers with P7-1/ZmGDIa, but decreases when ZmGDIa-hel replaces ZmGDIa. Viral infection significantly promotes ZmGA20x7.3 expression and oligomerization in ZmGDIa-containing susceptible maize, resulting in reduced bioactive GA1/GA4 levels. This causes an auxin/cytokinin imbalance and ultimately manifests as MRDD syndrome. Conversely, in resistant maize, ZmGDIa-hel counters these virus-induced changes, thereby mitigating MRDD severity.

Suining Deng, Siqi Jiang, Baoshen Liu, Tao Zhong, Qingcai Liu, Jianju Liu, Yuanliang Liu, Can Yin, Chen Sun, Mingliang Xu