The increased susceptibility of ripe fruit to fungal pathogens poses a substantial threat to crop production and marketability. Here, we coupled transcriptomic analyses with mutant studies to uncover critical processes associated with defenses and susceptibility in tomato (Solanum lycopersicum) fruit. Using unripe and ripe fruit inoculated with three fungal pathogens, we identified common pathogen responses reliant on chitinases, WRKY transcription factors, and reactive oxygen species detoxification. We established that the magnitude and diversity of defense responses do not significantly impact the interaction outcome, as susceptible ripe fruit mounted a strong defense response to pathogen infection. Then, to distinguish features of ripening that may be responsible for susceptibility, we utilized non-ripening tomato mutants that displayed different susceptibility patterns to fungal infection. Based on transcriptional and hormone profiling, susceptible tomato genotypes had losses in the maintenance of cellular redox homeostasis, while jasmonic acid accumulation and signaling coincided with defense activation in resistant fruit. We identified and validated a susceptibility factor, pectate lyase (PL). CRISPR-based knockouts of PL, but not polygalacturonase (PG2a), reduced susceptibility of ripe fruit by >50%. This study suggests that targeting specific genes that drive susceptibility is a viable strategy to improve the resistance of tomato fruit against fungal disease.

中文翻译：

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番茄果实对真菌病的敏感性可以通过抑制敏感性因子与成熟分开

成熟水果对真菌病原体的敏感性增加，对作物的生产和销售构成了重大威胁。在这里，我们将转录组学分析与突变研究相结合，以揭示与番茄（Solanum lycopersicum）果实的防御和敏感性相关的关键过程。使用接种了三种真菌病原体的未成熟果实，我们确定了依赖于几丁质酶，WRKY转录因子和活性氧解毒的常见病原体反应。我们确定防御反应的强度和多样性不会显着影响相互作用的结果，因为易感成熟果实对病原体感染具有较强的防御反应。然后，为了区分可能导致敏感性的成熟特征，我们利用非成熟的番茄突变体对真菌感染表现出不同的敏感性模式。基于转录和激素谱，易感番茄基因型在维持细胞氧化还原稳态方面有损失，而茉莉酸的积累和信号传导与抗性果实中的防御激活相吻合。我们确定并验证了敏感性因子果胶酸裂合酶（PL）。PL的基于CRISPR的敲除，但不是聚半乳糖醛酸酶（PG2a），可使成熟果实的敏感性降低> 50％。这项研究表明，靶向驱动敏感性的特定基因是提高番茄果实抗真菌病抗性的可行策略。易感的番茄基因型在维持细胞氧化还原稳态中失去作用，而茉莉酸的积累和信号传导与抗性果实的防御激活相吻合。我们确定并验证了敏感性因子果胶酸裂合酶（PL）。PL的基于CRISPR的敲除，但不是聚半乳糖醛酸酶（PG2a），可使成熟果实的敏感性降低> 50％。这项研究表明，靶向驱动敏感性的特定基因是提高番茄果实抗真菌病抗性的可行策略。易感的番茄基因型在维持细胞氧化还原稳态中失去了作用，而茉莉酸的积累和信号传导与抗性果实中的防御激活相吻合。我们确定并验证了敏感性因子果胶酸裂合酶（PL）。PL的基于CRISPR的敲除，但不是聚半乳糖醛酸酶（PG2a），可使成熟果实的敏感性降低> 50％。这项研究表明，针对特定的驱动敏感基因的基因是提高番茄果实抗真菌病抗性的可行策略。