A phase-separated protein hub modulates resistance to Fusarium head blight in wheat

Abstract

Fusarium head blight (FHB) is a devastating wheat disease. Fhb1, the most widely applied genetic locus for FHB resistance, is conferred by TaHRC of an unknown mode of action. Here, we show that TaHRC alleles distinctly drive liquid-liquid phase separation (LLPS) within a proteinaceous complex, determining FHB susceptibility or resistance. TaHRC-S (susceptible) exhibits stronger LLPS ability than TaHRC-R (resistant), and this distinction is further intensified by fungal mycotoxin deoxynivalenol, leading to opposing FHB symptoms. TaHRC recruits a protein class with intrinsic LLPS potentials, referred to as an "HRC-containing hub." TaHRC-S drives condensation of hub components, while TaHRC-R comparatively suppresses hub condensate formation. The function of TaSR45a splicing factor, a hub member, depends on TaHRC-driven condensate state, which in turn differentially directs alternative splicing, switching between susceptibility and resistance to wheat FHB. These findings reveal a mechanism for FHB spread within a spike and shed light on the roles of complex condensates in controlling plant disease.

Keywords: Fhb1; Fusarium head blight; alternative splicing; condensates; phase separation; resistance; susceptibility; wheat.