Xylella fastidiosa (Xf) is a global bacterial threat for a diversity of plants, including olive trees. However, current understanding of host responses upon Xf-infection is limited to allow early disease prediction, diagnosis, and sustainable strategies for breeding on plant tolerance. Recently, we identified a major complex trait for early de novo programming, named CoV-MAC-TED, by comparing early transcriptome data during plant cell survival with SARS-CoV-2-infected human cells. This trait linked ROS/RNS balancing during first hours of stress perception with increased aerobic fermentation connected to alpha-tubulin-based cell restructuration and control of cell cycle progression. Furthermore, our group had advanced concepts and strategies for breeding on plant holobionts. Here, we studied tolerance against Xf-infection by applying a CoV-MAC-TED-related gene set to (1) progress proof-of-principles, (2) highlight the importance of individual host responses for knowledge gain, (3) benefit sustainable production of Xf-threatened olive, (4) stimulate new thinking on principle roles of secondary metabolite synthesis and microbiota for system equilibration and, (5) advance functional marker development for resilience prediction including tolerance to Xf-infections. We performed hypothesis-driven complex analyses in an open access transcriptome of primary target xylem tissues of naturally Xf-infected olive trees of the Xf-tolerant cv. Leccino and the Xf-susceptible cv. Ogliarola. The results indicated that cyanide-mediated equilibration of oxygen-dependent respiration and carbon-stress alleviation by the help of increased glycolysis-driven aerobic fermentation paths and phenolic metabolism associate to tolerance against Xf. Furthermore, enhanced alternative oxidase (AOX) transcript levels through transcription Gleichschaltung linked to quinic acid synthesis appeared as promising trait for functional marker development. Moreover, the results support the idea that fungal endophytes strengthen Xf-susceptible genotypes, which lack efficient AOX functionality. Overall, this proof-of-principles approach supports the idea that efficient regulation of the multi-functional AOX gene family can assist selection on multiple-resilience, which integrates Xf-tolerance, and stimulates future validation across diverse systems.

中文翻译：

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成年橄榄树的转录组分析表明乙醛释放和氰化物介导的呼吸特征对于木杆菌的耐受性至关重要，并建议 AOX 基因家族作为多重恢复力的标记

苛养木杆菌 (Xf) 是对包括橄榄树在内的多种植物的全球性细菌威胁。然而，目前对 Xf 感染宿主反应的了解仅限于早期疾病预测、诊断和植物耐受性育种的可持续策略。最近，我们通过比较植物细胞与感染 SARS-CoV-2 的人类细胞存活期间的早期转录组数据，确定了早期从头编程的一个主要复杂特征，称为 CoV-MAC-TED。这一特征将应激感知的最初几个小时内的 ROS/RNS 平衡与增加的有氧发酵联系起来，而有氧发酵又与基于 α-微管蛋白的细胞重组和细胞周期进程的控制相关。此外，我们课题组在植物全生物育种方面拥有先进的理念和策略。在这里，我们通过应用 CoV-MAC-TED 相关基因集来研究对 Xf 感染的耐受性，以 (1) 进展原理验证，(2) 强调个体宿主反应对知识获取的重要性，(3) 益处受 Xf 威胁的橄榄的可持续生产，(4) 激发对次生代谢物合成和微生物群对系统平衡的主要作用的新思考，(5) 推进用于复原力预测的功能标记开发，包括对 Xf 感染的耐受性。我们在 Xf 耐受品种的天然 Xf 感染橄榄树的主要目标木质部组织的开放获取转录组中进行了假设驱动的复杂分析。Leccino 和 Xf 敏感 cv。奥利亚罗拉。结果表明，氰化物介导的氧依赖性呼吸平衡和通过增加糖酵解驱动的有氧发酵路径和酚类代谢来缓解碳胁迫与对 Xf 的耐受性相关。此外，通过与奎尼酸合成相关的转录 Gleichschaltung 来增强替代氧化酶 (AOX) 转录水平，这似乎是功能标记开发的有希望的特征。此外，结果支持这样的观点，即内生真菌增强了 Xf 敏感基因型，而该基因型缺乏有效的 AOX 功能。总体而言，这种原理验证方法支持这样的观点：多功能 AOX 基因家族的有效调控可以帮助选择多重弹性，整合 Xf 耐受性，并刺激未来跨不同系统的验证。