Fruitlet Core Rot disease in ‘Queen Victoria’ pineapple infructescence triggers local and systemic metabolome reconfigurations

We studied the metabolomes of ’Queen Victoria’ pineapples subjected to the fungi-induced fruitlet core rot (FCR) disease, a major quality issue in the pineapple industry. Analyses were carried out on the pulp and skin of individual fruitlets within healthy or black spotted infructescences, in order to profile three types of samples: healthy, infected and asymptomatic fruitlets. Our results reveal distinct responses to FCR in pulp and skin of infected fruitlets, both quantitatively and qualitatively. The pulp displayed much stronger and diverse changes, including the implementation of a local phenolic-based defense reflecting both antimicrobial activity and cell wall turnover. Evidence of strong redox regulation linked to the presence of the pathogen was observed through variations in proline and glutathione-conjugated compounds. Moreover, among the numerous sugar variations, a particular trehalose pattern emerged as an antagonistic issue between the plant and the fungus. The activation of signaling pathways following the fungal attack was also revealed, with the accumulation of pipecolate and alpha-aminobutyrate, involved in defense priming and systemic acquired resistance. Interestingly, we also found significant metabolic changes in asymptomatic fruitlets, similar in nature but smaller in magnitude, demonstrating the existence of a systemic response to infection. This work opens the way to a better understanding of the infection and defense mechanisms involved in FCR and their consequences on organoleptic quality. • Profiling of primary and secondary metabolites in pineapple due to FCR infection. • Highlighting of FCR-induced variations in major amino acids and carbohydrates. • Identification of phenolics implicated in pineapple defense mechanism following FCR. • Uncovering of a systemic response to the FCR infection in pineapple fruit.