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Coumaroyl-isocitric and caffeoyl-isocitric acids as markers of pineapple fruitlet core rot disease
Abstract
Introduction – Fruitlet core rot is the major postharvest disease affecting ‘Queen’ pineapple in La Réunion island. The symptoms are black spots located in the pineapple fruitlets. Materials and methods – Fusarium ananatum, the main causal agent of fruitlet core rot was inoculated in ‘MD-2’ and ‘Queen’ (Victoria), a tolerant and a susceptible cultivar, respectively. A metabolomics approach to healthy and inoculated fruitlets allowed to determine which putative metabolites are involved in fruitlet core rot disease. The evolution of fruitlet core rot was then followed-up with a focus on the phenolic compounds. Results and discussion – Based on the metabolomics results, the phenolic compounds seemed to be determining markers of black spots. Coumaroylisocitrate and caffeoylisocitrate dramatically increased in the infected fruitlets in both cultivars post-inoculation. The ‘MD-2’-infected fruitlets reached higher hydroxycinnamic acid levels in a shorter time than those of the ‘Queen’-infected fruitlets. In healthy fruits of ‘MD-2’, coumaroyl-isocitric acid and hydroxybenzoic acids were naturally produced as the fruit mature. Conclusion – These phenolic compounds play a major role in the pineapple disease resistance.
... The pineapple 'Queen Victoria' (Ananas comosus (L.) Merr.) is one of the major crops of Reunion Island, where its production is of high socioeconomic importance as it is exported to the european markets (CBI Ministry of Foreign Affairs, 2022;FAO, 2022). However, this cultivar is particularly susceptible to fungal pathogens responsible for fruitlet core rot (FCR) disease (Jacobs et al., 2010;Barral et al., 2019bBarral et al., , 2020, which restricts its compliance with commercial quality standards. ...
... Metabolomics has proven its relevance in the study of metabolic stress responses in plants (Allwood et al., 2008;Arbona and Gómez-Cadenas, 2016), in particular to highlight the metabolic mechanisms implicated in resistance to fungal pathogens (Ballester et al., 2013;Luna et al., 2020;Duan et al., 2022). The metabolic responses to FCR disease in pineapple was explored for the first time by Barral et al. (2017Barral et al. ( , 2019b, by comparing the fruit metabolic profiles of the resistant cultivar 'MD-2' and the susceptible 'Queen Victoria' inoculated with the pathogen Fusarium ananatum, one of the main causal agents of FCR disease in Reunion Island . The disease provoked an accumulation of phenolic compounds, notably coumaroylisocitrate and caffeoylisocitrate, which were more abundant in 'MD-2'. ...
... In this study, we investigated the metabolic changes induced by FCR disease in 'Queen Victoria' pineapple tissues. Unlike Barral et al. (2019b), who focused solely on the pulp metabolome of inoculated pineapples, we worked on both pulp and skin metabolomes from naturally infected fruit in the field. We also explored a potential systemic effect of infection by comparing the metabolome of healthy fruitlets from fully healthy pineapples with that of asymptomatic fruitlets from pineapples bearing infected fruitlets. ...
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.
... A similar mechanism could also affect mealybugs after SAR induction in pineapples, particularly young instars that are highly active feeders. Additionally, Queen Victoria and MD2 also naturally produce a high level of phenolic compounds such as p-coumaroyl-isocitric acid and several hydroxybenzoic acids, among other phenolic compounds that play a role in fungal disease resistance in pineapple [46]. ...
Pineapples are highly susceptible to “Wilt disease”, caused by the biotrophic insect Dysmicoccus brevipes that also transmits several Wilt-associated viruses (PMWaVs). Conventional farms manage mealybugs and Wilt disease using chemicals. However, many of these chemicals have been banned in Europe due to safety concerns, leading to a critical need for studies on pesticide-free control methods. During their evolution, plants have developed natural defences, such as systemic acquired resistance (SAR), against pathogens and pests. In this study, salicylic acid (10⁻³ M) was applied to MD2 and Queen Victoria pineapple plants as a foliar spray or soil drench, followed by mealybug infestation. This treatment enhanced defences, assessed through mealybug multiplication rates, and biochemical and molecular responses of tissue-cultured plantlets under controlled conditions. Phenylalanine ammonia-lyase activity (PAL) was measured as a potential SAR signalling enzymatic marker. Additionally, the expression levels of four genes were analyzed, which included AcPAL and AcICS2, both linked to salicylic acid synthesis; AcMYB-like, a transcription factor regulating salicylic acid biosynthesis; and AcCAT, which is involved in H2O2 level control in plants. SA elicitation reduced the mealybug multiplication rate by 70% on pineapples compared to untreated plants. In this study, the biochemical marker (PAL) and three molecular markers (AcPAL, AcICS2, and AcCAT) showed significant differences between primed and unprimed plants, indicating SAR induction and its role in the pineapple–mealybug interaction. In MD2 and Queen Victoria, PAL increased by 2.3 and 1.5, respectively, while AcPAL increased by 4 and more than 10. The other molecular markers, AcICS2, AcCAT, and AcMYB-like (a transcription factor), increased by 3, except for the last one in Queen Victoria. The reduction in mealybug populations with SAR is less effective than with pesticides, but it provides a valuable alternative on Réunion Island, where the only remaining insecticide will soon be banned. In addition, SAR priming offers a promising, eco-friendly strategy for managing mealybug populations and reducing Wilt disease in pesticide-free pineapple cropping systems.
... A similar mechanism could also affect mealybugs after SAR induction in pineapple, particularly young instars which are highly active feeders. Additionally, Queen Victoria and MD2 naturally produce also a high level of phenolic compounds as coumaroyl-isocitric acid and hydroxybenzoic acids, two phenolic compounds that play a role in fungal disease resistance in pineapple [45]. ...
Pineapple is highly susceptible to "Wilt disease," caused by the biotrophic insect Dysmicoccus brevipes, which also transmits for several wilt-associated viruses (PMWaVs). Conventional farms manage mealybugs and wilt disease. However, many of these chemicals have been banned in Europe due to safety concerns, leading to researches on pesticide-free control methods. Plants have developed natural defences, such as systemic acquired resistance (SAR), against pathogens and pests. In this study, salicylic acid (10⁻³ M) was applied to MD2 and Queen Victoria pineapple plants, followed by mealybug infestation. This treatment enhanced defences, assessed through mealybug multiplication rates, and biochemical and molecular responses of tissue-cultured plantlets under controlled conditions. Phenylalanine ammonia-lyase activity (PAL) was measured as a potential SAR signalling enzymatic marker. Additionally, four gene expressions were analyzed: AcPAL and AcICS2) both linked to salicylic acid synthesis; AcMYB-like, a transcription factor regulating salicylic acid biosynthesis; and AcCAT involved in H2O2 level control in plants. SA elicitation reduced the mealybug multiplication rate by 70% on pineapples. Under our conditions, the biochemical marker (PAL) and three molecular markers (AcPAL, AcICS2, AcCAT) showed significant differences between primed and unprimed plants, indicating SAR induction and its role in the pineapple-mealybug interaction. SAR priming offers a promising, eco-friendly strategy for managing mealybug populations and reducing Wilt disease in pesticide-free pineapple cropping systems.
... Mobile phase A consisted of formic acid and ultra-pure water 0.1%, and mobile phase B consisted of formic acid and methanol 0.1%. The gradient elution was adapted from [19] as follows: 5% B for 10 min, 7% B for 45 min, 35% B for 12 min, 80% B for 28 min, 100% B for 35 min, and 5% B for 10 min. The flow rate was 0.5 mL/min. ...
Objectives: This study provides an overview of the composition of the raw root flesh of a panel of 22 sweet potato (Ipomoea batatas L.) cultivars, with a focus on bioactive compounds. The large diversity of the proximate and phytochemical compositions observed between cultivars and within and between different flesh colors pointed out the importance of composition analysis and not only color choice for the design of foods with nutritional benefits. Methods: The nutritional composition (starch, protein, total dietary fibers) and bioactive compound composition of 22 cultivars from Reunion Island, maintained in the Vatel Biological Resource Center, were investigated. Results: Orange and purple cultivars stood out from white and yellow cultivars for their higher nutritional composition. Purple sweet potatoes were notable for their high contents of anthocyanins (55.7 to 143.4 mg/g dry weight (DW)) and phenolic compounds, in particular chlorogenic acid and ferulic acid, contributing to antioxidant activities, as well as their fiber content (14.1 ± 2.1% DW). Orange cultivars were rich in β-carotene (47.2 ± 0.7 mg/100 g DW) and to a lesser extent α-carotene (4.8 ± 1.2 mg/100 g DW). In contrast, certain white cultivars demonstrated suboptimal nutritional properties, rendering them less relevant even for applications where the lack of coloration in food is desired. Conclusions: Those characteristics enable the selection of sweet potato varieties to design food products ensuring optimal nutritional benefits and culinary versatility.
... This browning is the result of the phenolic compounds oxidation into quinones by the enzymes polyphenol oxidase and laccase (Avallone et al., 2003). Several studies revealed that soluble and cell wall-bound phenolic acids in the pineapple fruit parenchyma increase significantly after the onset of the first symptoms of FCR (Barral et al., 2019(Barral et al., , 2020Steingass et al., 2015). ...
Pineapple (Ananas comosus L. Merr) is a tropical fruit with sweet taste, vibrant tropical flavour, and contains enormous health benefits. Currently, pineapple is ranked as the second in the list of commercial tropical fruits for worldwide production after mangoes. Like other crops, pineapple is prone to various diseases caused by different groups of plant pathogens. Several common pineapple diseases have been reported particularly in Malaysia and other countries including bacterial and fungal heart rots, fruit collapse, butt and black rots, fruitlet core rot, internal black spot, fusariosis, mealybug wilt-associated virus, yeasty, stem end rot, leaf spot disease, and parasitic nematodes-associated disease. These diseases can cause huge losses to pineapple production by reducing quantity and quality of fruit. Knowledge on the causal pathogen, disease symptoms and dissemination of pathogen in pineapple farms are important to prevent and control these diseases. Therefore, this chapter presents more than 10 common diseases in pineapple with the descriptions of causal pathogen and symptoms, as well as the available control methods to manage the diseases.
... This browning is the result of the phenolic compounds oxidation into quinones by the enzymes polyphenol oxidase and laccase (Avallone et al., 2003). Several studies revealed that soluble and cell wall-bound phenolic acids in the pineapple fruit parenchyma increase significantly after the onset of the first symptoms of FCR (Barral et al., 2019(Barral et al., , 2020Steingass et al., 2015). ...
Pineapple (Ananas comosus L. Merr) is a tropical fruit with sweet taste, vibrant tropical flavour, and contains enormous health benefits. Currently, pineapple is ranked as the second in the list of commercial tropical fruits for worldwide production after mangoes. Like other crops, pineapple is prone to various diseases caused by different groups of plant pathogens. Several common pineapple diseases have been reported particularly in Malaysia and other countries including bacterial and fungal heart rots, fruit collapse, butt and black rots, fruitlet core rot, internal black spot, fusariosis, mealybug wilt-associated virus, yeasty, stem end rot, leaf spot disease, and parasitic nematodes–associated disease. These diseases can cause huge losses to pineapple production by reducing quantity and quality of fruit. Knowledge on the causal pathogen, disease symptoms and dissemination of pathogen in pineapple farms are important to prevent and control these diseases. Therefore, this chapter presents more than 10 common diseases in pineapple with the descriptions of causal pathogen and symptoms, as well as the available control methods to manage the diseases.
... This browning is the result of the oxidation of phenolic compounds into quinones by the enzymes polyphenol oxidase and laccase (Avallone et al., 2003). Several studies revealed that soluble and cell wall-bound phenolic acids in the pineapple fruit parenchyma increase significantly after the onset of the first symptoms of FCR (Steingass et al., 2015;Barral et al., 2019;Barral et al., 2020). These compounds provide antifungal activity on several species of fungi including causal pathogens of FCR (Barral et al., 2020). ...
Pineapple is a perennial fruit-bearing tropical plant that belongs to the Bromeliaceae family, which has more than 2500 species. Pineapple is known excellent source of minerals and vitamins. It produces substantial calcium, potassium, glucose, the proteindigesting enzyme bromelain, fibre, vitamin A, B and C. In Malaysia, twelve registered varieties of pineapple have been introduced and commercially planted such as Moris (AC1), Sarawak (AC2), Gandul (AC3), Maspine (AC4), Josapine (AC5) Yankee (AC6) Moris Gajah (AC7), N36 (AC8), MD2 (AC9), View of Sunset (AC10), Madu Kaca (AC11), and Keningau Diamond (AC12). The disease is one of the important factors that can contribute to the huge losses of pineapple yield worldwide. This review paper aimed to discuss the main diseases of pineapple and their control management, particularly in Malaysia. The common diseases of pineapple that cause significant yield losses in the farms such as mealybug wilt-associated virus, bacterial heart rot, fruit collapse, butt rot, fruitlet core rot, black rot, yeasty and fusariosis are highlighted and discussed in detail on the causal pathogens, disease symptoms and signs, disease infection and development. The available control measures for managing pineapple diseases were also included in this paper.
The identity of the fungi responsible for fruitlet core rot (FCR) disease in pineapple has been the subject of investigation for some time. This study describes the diversity and toxigenic potential of fungal species causing FCR in La Reunion, an island in the Indian Ocean. One-hundred-and-fifty fungal isolates were obtained from infected and healthy fruitlets on Reunion Island and exclusively correspond to two genera of fungi: Fusarium and Talaromyces. The genus Fusarium made up 79% of the isolates, including 108 F. ananatum, 10 F. oxysporum, and one F. proliferatum. The genus Talaromyces accounted for 21% of the isolated fungi, which were all Talaromyces stollii. As the isolated fungal strains are potentially mycotoxigenic, identification and quantification of mycotoxins were carried out on naturally or artificially infected diseased fruits and under in vitro cultures of potential toxigenic isolates. Fumonisins B1 and B2 (FB1-FB2) and beauvericin (BEA) were found in infected fruitlets of pineapple and in the culture media of Fusarium species. Regarding the induction of mycotoxin in vitro, F. proliferatum produced 182 mg kg⁻¹ of FB1 and F. oxysporum produced 192 mg kg⁻¹ of BEA. These results provide a better understanding of the causal agents of FCR and their potential risk to pineapple consumers.
Purslane (Portulaca oleracea) is a weed naturally found in driveways, lawns, and fields and edible in many regions of Europe, Asia, the Middle East, Africa, and Australia. The purpose of this study was to compare the nutritional and phytochemical components of cultivated and wild purslane. Omega-3 contents of both purslane genotypes were comparable with 189.16 ± 25.52 mg/100 g dry weight and 188.48 ± 6.35 mg/100 g dry weight in cultivated and wild purslane leaves, respectively. Omega-6/omega-3 ratio (1:1-1:3) were low in both genotypes. However, high levels of oxalic acid were observed. Cultivated contained greater amounts of amino acids and vitamins than wild purslane. Of the 184 compounds identified in both genotypes by LC-MS/MS, including phenolic acids, organic acids, flavonoids, alkaloids, and betanin more than 80 showed greater than two-fold abundance in the wild compared to cultivated purslane. Purslane has the potential to be cultivated as a food ingredient for nutraceutical applications.
Fruitlet core rot is one of the major postharvest disease of pineapple (Ananas comosus var. comosus). In the past, control strategies were designed to eliminate symptoms without addressing their causes or mechanisms, thus achieving only moderate success. In this study, (i) we focused on the anatomy of the fruitlets in the resistant “MD-2” and susceptible “Queen” pineapple cultivars; (ii) we identified the key role of the carpel margin in the infection process; (iii) we identified the key role of the sinuous layer of thick-walled cells in the inhibition of Fusarium ananatum colonization; and (iv) we linked the anatomy of the fruitlets with the phenolic content of cell walls. The fruitlet anatomy of the two cultivars was studied using X-ray, fluorescence, and multiphoton microscopy. Sepals and bracts were not perfectly fused with each other, allowing the pathogen to penetrate the fruit even after flowering. In fact, the fungi were found in the blossom cups of both cultivars but only became pathogenic in the flesh of the “Queen” pineapple fruit under natural conditions. The outer layer of the “MD-2” cavity was continuous with thick cell walls composed of ferulic and coumaric acids. The cell walls of the “Queen” blossom cup were less lignified at the extremities, and the outer layer was interspersed with cracks. The carpel margins were fused broadly in the “MD-2” pineapple, in contrast to the “Queen” pineapple. This blemish allows the fungus to penetrate deeper into the susceptible cultivar. In pineapple fruitlets, the hyphae of F. ananatum mainly progressed directly between cell walls into the parenchyma but never reached the vascular region. A layer of thick-walled cells, in the case of the resistant cultivar, stopped the colonization, which were probably the infralocular septal nectaries. Anatomical and histochemical observations coupled with spectral analysis of the hypodermis suggested the role of lignin deposition in the resistance to F. ananatum. The major phenolics bound to the cell walls were coumaric and ferulic acids and were found in higher amounts in the resistant cultivar postinoculation. The combination of fruitlet anatomy and lignification plays a role in the mechanism of host resistance to fruitlet core rot.
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