Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China; CIMMYT-JAAS Joint Center for Wheat Diseases, The Research Center of Wheat Scab, Zhongshan Biological Breeding Laboratory, Key Laboratory of Germplasm Innovation in Downstream of Huaihe River (Nanjing), Ministry of Agriculture and Rural Affairs, Jiangsu Academy of Agricultural Sciences, Nanjing 210014, China.
Waite Research Institute, School of Agriculture, Food and Wine, The University of Adelaide, Urrbrae, SA 5064, Australia.
Cell Host Microbe. 2024 May 8;32(5):710-726.e10. doi: 10.1016/j.chom.2024.04.002. Epub 2024 Apr 23.
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.
镰刀菌穗腐病(FHB)是一种严重危害小麦的疾病。Fhb1 是应用最广泛的抗 FHB 遗传位点,其作用方式尚不清楚。本研究表明,TaHRC 等位基因在蛋白复合物内明显驱动液-液相分离(LLPS),决定了 FHB 的敏感性或抗性。TaHRC-S(敏感)比 TaHRC-R(抗性)具有更强的 LLPS 能力,真菌霉菌毒素脱氧雪腐镰刀菌烯醇进一步加剧了这种差异,导致相反的 FHB 症状。TaHRC 招募了一类具有内在 LLPS 潜力的蛋白质,称为“含有 HRC 的枢纽”。TaHRC-S 驱动枢纽成分的凝聚,而 TaHRC-R 则相对抑制枢纽凝聚体的形成。枢纽成员 TaSR45a 剪接因子的功能取决于 TaHRC 驱动的凝聚状态,这反过来又通过不同的剪接方式,在敏感性和抗性之间切换,从而控制小麦 FHB。这些发现揭示了 FHB 在穗部传播的机制,并阐明了复杂凝聚物在控制植物疾病中的作用。