Cell walls (CWs) are protein-rich polysaccharide matrices essential for plant growth and environmental acclimation. The CW constitutes the first physical barrier as well as a primary source of nutrients for microbes interacting with plants, such as the vascular pathogen Fusarium oxysporum (Fo). Fo colonizes roots, advancing through the plant primary CWs towards the vasculature, where it grows causing devastation in many crops. The pathogenicity of Fo and other vascular microbes relies on their capacity to reach and colonize the xylem. However, little is known about the root-microbe interaction before the pathogen reaches the vasculature and the role of the plant CW during this process. Using the pathosystem Arabidopsis-Fo5176, we show dynamic transcriptional changes in both fungus and root during their interaction. One of the earliest plant responses to Fo5176 was the downregulation of primary CW synthesis genes. We observed enhanced resistance to Fo5176 in Arabidopsis mutants impaired in primary CW cellulose synthesis. We confirmed that Arabidopsis roots deposit lignin in response to Fo5176 infection, but we show that lignin-deficient mutants were as susceptible as wildtype plants to Fo5176. Genetic impairment of jasmonic acid biosynthesis and signaling did not alter Arabidopsis response to Fo5176, whereas impairment of ethylene signaling did increase vasculature colonization by Fo5176. Abolishing ethylene signaling attenuated the observed resistance while maintaining the dwarfism observed in primary CW cellulose-deficient mutants. Our study provides significant insights on the dynamic root-vascular pathogen interaction at the transcriptome level and the vital role of primary CW cellulose during defense response to these pathogens. These findings represent an essential resource for the generation of plant resistance to Fo that can be transferred to other vascular pathosystems.

中文翻译：

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时间分辨双转录组学揭示了一种原代细胞壁纤维素依赖性防御血管病原体的机制

细胞壁 (CW) 是植物生长和环境适应所必需的富含蛋白质的多糖基质。CW 构成了第一道物理屏障，也是微生物与植物相互作用的主要营养来源，例如血管病原体尖孢镰刀菌 (Fo)。Fo 定殖根部，通过植物初级 CW 向脉管系统前进，它在那里生长，对许多作物造成破坏。Fo 和其他血管微生物的致病性取决于它们到达和定殖木质部的能力。然而，在病原体到达脉管系统之前根与微生物的相互作用以及植物 CW 在此过程中的作用知之甚少。使用病理系统拟南芥-Fo5176，我们展示了真菌和根在它们相互作用过程中的动态转录变化。最早的植物对 Fo5176 的反应之一是初级 CW 合成基因的下调。我们观察到初级 CW 纤维素合成受损的拟南芥突变体对 Fo5176 的抗性增强。我们证实，拟南芥根部在响应 Fo5176 感染时会沉积木质素，但我们表明木质素缺陷突变体与野生型植物一样对 Fo5176 敏感。茉莉酸生物合成和信号传导的遗传损伤并没有改变拟南芥对 Fo5176 的反应，而乙烯信号传导的损伤确实增加了 Fo5176 的脉管系统定植。消除乙烯信号减弱了观察到的抗性，同时保持了在初级 CW 纤维素缺陷突变体中观察到的侏儒症。我们的研究为转录组水平的动态根-血管病原体相互作用以及初级 CW 纤维素在对这些病原体的防御反应中的重要作用提供了重要的见解。这些发现代表了植物对 Fo 产生抗性的重要资源，这种抗性可以转移到其他血管病理系统。