Department of Plant Pathology and Weed Research, ARO, Volcani Institute, Rishon LeZion, Israel.
Microbiol Spectr. 2022 Aug 31;10(4):e0028022. doi: 10.1128/spectrum.00280-22. Epub 2022 Jul 27.
The plant hormone cytokinin (CK) is an important developmental regulator. Previous work has demonstrated that CKs mediate plant immunity and disease resistance. Some phytopathogens have been reported to secrete CKs and may manipulate CK signaling to improve pathogenesis. In recent work, we demonstrated that CK directly inhibits the development and virulence of fungal phytopathogens by attenuating the cell cycle and reducing cytoskeleton organization. Here, focusing on Botrytis cinerea, we report that CK possesses a dual role in fungal biology, with role prioritization being based on sugar availability. In a sugar-rich environment, CK strongly inhibited B. cinerea growth and deregulated cytoskeleton organization. This effect diminished as sugar availability decreased. In its second role, we show using biochemical assays and transgenic redox-sensitive fungal lines that CK can promote glycolysis and energy consumption in B. cinerea, both and . Glycolysis and increased oxidation mediated by CK were stronger in low sugar availability, indicating that sugar availability could indeed be one possible element determining the role of CK in the fungus. Transcriptomic data further support our findings, demonstrating significant upregulation to glycolysis, oxidative phosphorylation, and sucrose metabolism upon CK treatment. Thus, the effect of CK in fungal biology likely depends on energy status. In addition to the plant producing CK during its interaction with the pathogen for defense priming and pathogen inhibition, the pathogen may take advantage of this increased CK to boost its metabolism and energy production, in preparation for the necrotrophic phase of the infection. The hormone cytokinin (CK) is a plant developmental regulator. Previous research has highlighted the involvement of CK in plant defense. Here, we report that CK has a dual role in plant-fungus interactions, inhibiting fungal growth while positively regulating B. cinerea energy utilization, causing an increase in glucose utilization and energy consumption. The effect of CK on B. cinerea was dependent on sugar availability, with CK primarily causing increases in glycolysis when sugar availability was low, and growth inhibition in a high-sugar environment. We propose that CK acts as a signal to the fungus that plant tissue is present, causing it to activate energy metabolism pathways to take advantage of the available food source, while at the same time, CK is employed by the plant to inhibit the attacking pathogen.
植物激素细胞分裂素（CK）是一种重要的发育调节剂。先前的研究表明，CK 介导植物免疫和抗病性。一些植物病原菌已被报道分泌 CK，并可能操纵 CK 信号以改善发病机制。在最近的工作中，我们证明 CK 通过减弱细胞周期和减少细胞骨架组织直接抑制真菌植物病原菌的发育和毒力。在这里，我们专注于灰葡萄孢，报告 CK 在真菌生物学中具有双重作用，作用的优先级基于糖的可用性。在富含糖的环境中，CK 强烈抑制灰葡萄孢的生长并使细胞骨架组织失调。随着糖可用性的降低，这种效果减弱。在其第二个作用中，我们使用生化测定和转基因氧化还原敏感真菌系表明 CK 可以促进灰葡萄孢中的糖酵解和能量消耗，既 又 。在低糖可用性下，CK 介导的糖酵解和氧化增强，表明糖可用性确实可以是决定 CK 在真菌中作用的一个可能因素。转录组数据进一步支持我们的发现，表明 CK 处理后显著上调糖酵解、氧化磷酸化和蔗糖代谢。因此，CK 在真菌生物学中的作用可能取决于能量状态。除了植物在与病原体相互作用时产生 CK 以进行防御启动和病原体抑制外，病原体还可能利用这种增加的 CK 来促进其新陈代谢和能量产生，为感染的坏死阶段做准备。激素细胞分裂素（CK）是一种植物发育调节剂。先前的研究强调了 CK 在植物防御中的作用。在这里，我们报告 CK 在植物-真菌相互作用中具有双重作用，抑制真菌生长，同时正向调节灰葡萄孢的能量利用，导致葡萄糖利用和能量消耗增加。CK 对灰葡萄孢的影响取决于糖的可用性，当糖可用性低时，CK 主要导致糖酵解增加，而在高糖环境中则抑制生长。我们提出 CK 作为一种信号传递给真菌，表明植物组织存在，使其激活能量代谢途径，利用可用的食物来源，同时 CK 被植物用来抑制攻击的病原体。
