Potential novel bacteria VOC-based tool to control postharvest diseases

The United Nations Food and Agriculture Organization (FAO) estimates that post-harvest of fruit and vegetables is the highest among all types of food losses, reaching up to 40% (FAO?2019). Recent estimations indicate that loss at the retail and consumer levels in the USA includes 6.7?M?kg of fruit and 10.6?M?kg of vegetables per year, adding up to a loss of?~?US$ 40,000 million (Buzby et al.?2011; Buzby and Hyman?2012). Storage, transport, and household waste are the most critical loss points in the fruit and vegetable supply chains, owing largely to inadequate use of bulk packaging and management (Watada et al.?1996). These conditions cause abiotic stresses such as extreme temperatures, desiccation, mechanical injury, low O2, and high CO2?percentage that often result in food loss (Toivonen and Hodges?2011). In addition, fruit and vegetables are highly perishable because, once harvested, they can also suffer biotic stresses such as infections of wound-invading necrotrophic pathogens (Sharma et al.?2009) that compromise both quantity and quality (Delgado et al.?2017). Tools to reduce postharvest loosesSeveral chemical and physical tools have been used to reduce post-harvest losses of fruit and vegetables due to fungal pathogen infections, but their efficiency, economic, and environmental costs are intensely debated (Romanazzi et al.?2012; De Simone et al.?2020). For instance, synthetic fungicides have proven to provide long-lasting control of many target plant pathogens and still contribute heavily to disease control in conventional farming (Oliver and Hewitt?2014). However, their widespread use has triggered severe environmental problems due to their persistence in the air, soil, water, and food, as well as the development of pathogen resistance (Narayanasamy?2006; Gyawali and Ibrahim?2014). As a result, European Union (EU), through the European Green Deal, aims at reducing the use of chemical fungicides by half by 2030, recommending their limited application, adopting prevention measures, and pushing non-chemical control methods (European Commission?2020). Alternatively, physical technologies such as variations in temperature, UV-C irradiation, pressure, or changing atmospheric composition can increase fruit and vegetable resistance against abiotic and biotic stresses after harvesting. Although these methods are often considered non-harmful and residue-free emerging technologies, they involve high energy inputs and costs (Usall et al.?2016). Overall, there has been a pressing need for developing environmentally friendly and economical methods for the management of pathogen infections in fruit and vegetables after harvesting. Microbial-based toolThe use of microbial-based tools for pathogen management can provide new alternatives. In this sense, various defense-related phytohormones, biological elicitors, and non-organic elicitors have been used as biopesticides against plant pathogens and thus might be also useful on detached fruit (Sharma et al.?2009; Poveda?2021). In particular, volatile organic compounds (VOCs) emitted by microbes (e.g., bacteria) are emerging as an alternative to conventional chemical and physical treatments, mostly in circumstances where direct contact between the pathogen and its antagonist is not practical (Tilocca et al.?2020; Poveda?2021). Bacterial VOCs might increase toxicity against fungal pathogens in post-harvest fruit (Mari et al.?2016) and/or induce fruit defense response (Romanazzi et al.?2016). Unfortunately, the mechanisms underlying these antagonistic effects are still poorly understood. In-depth investigations are thus needed to investigate the antifungal activity, efficacy, and preventive effects of bacterial VOCs in controlling pathogen infections in harvested fruit (Cellini et al.?2021). Grape and wine processing industries yearly generate around 5?9?M?kg of solid waste worldwide, which constitutes 20?30% of processed materials (Schieber et al.?2001). Likewise, tomato is the second most consumed vegetable in the world (Savatovi? et al.?2012) and its industrial processing generates a considerable amount of waste (10?30% of their raw weight;?Rahmatnejad et al.?2009). A critical problem in these industries is the losses and waste generated by post-harvest fungal pathogens due to the lack of proper handling methods and infrastructure (Calicioglu et al.?2019). VOCs emitted by?Xenorhabdus nematophila?and?Photorhabdus laumondii?subsp.?laumondiiThe gram-negative entomopathogenic bacteria?Xenorhabdus?spp. and?Photorhabdus?spp. produce a huge range of bioactive compounds (peptides, polyketides, and toxins) with antibacterial (B?sz?rm?nyi et al.?2009; Muangpat et al.?2020), antifungal (Fang et al.?2011,?2014; Chac?n-Orozco et al.?2020; Alforja et al.?2021; Cimen et al.?2021; Li et al.?2021), insecticidal (ffrench-Constant et al.?2007; Vitta et al.?2018; Vicente-D?ez et al.?2021a,?b) and nematicidal (Kusakabe et al.?2021; Abebew et al.?2022) activity. However, the application of these bacterial VOCs to reduce the impact of fungal pathogens has been poorly explored, and their practical use is at an early stage (Crawford et al.?2012; Fl?rez et al.?2015; Kajla et al.?2019). In this study, we investigated the effects of VOCs emitted by?Xenorhabdus nematophila?and?Photorhabdus laumondii?subsp.?laumondii?on the infection and growth of the pathogenic mold?Botrytis cinerea?on post-harvest red grapes and tomatoes. In addition, we evaluated the preventive effects of these bacterial VOCs against this pathogen in post-harvest wounded and intact grapes. Overall, this study contributes to a better understanding of the effects of these bacterial VOCs on one pathogen infection in two post-harvest fruit systems, illustrating the potential of this new tool to reduce post-harvest losses in the context of current global agriculture and economy.AbstractPost-harvest fruit and vegetable rot produced by?Botrytis cinerea?(Helotiales: Sclerotiniaceae) causes significant reductions in food availability and drastically increases economic losses. The use of microbial-based tools for pathogen management holds promise. In particular, volatile organic compounds (VOCs) emitted by microbes (e.g., bacterial compounds) are becoming increasingly more frequent as an alternative to chemical and physical treatments. In this study, we performed three laboratory experiments to investigate the effects of VOCs emitted by two gram-negative entomopathogenic bacteria,?Xenorhabdus nematophila, and?Photorhabdus laumondii?subsp.?laumondii, on the infection and growth of the pathogenic mold?B. cinerea?on post-harvest red grapes and tomatoes. In addition, we evaluated the preventive effects of these bacterial VOCs against pathogens in post-harvest wounded and intact grapes. Overall, VOCs emitted by?X. nematophila?and?P. laumondii?limited the lesion area of?B. cinerea?to 0.5% and 2.2%, respectively, on the grapes. Similarly, VOCs emitted by?X. nematophila?and?P. laumondii?limited the lesion area of?B. cinerea?to 0.5% and 0.02%, respectively, in tomatoes. In addition, the emission of VOCs by both bacteria showed strong preventive fungal effects. In particular, VOCs emitted by?P. laumondii?reduced to 13%?B. cinerea?incidence in damaged grapes exposed to VOCs. Moreover, intact grapes exposed to VOCs emitted by?X. nematophila?and?P. laumondii?decreased?B. cinerea?incidence by 33%. This study provides insightful information about a potential novel bacteria-based tool that can be used as an alternative in the integrated control of post-harvest diseases. The figure is Fig. 2 of the original paper -?In vivo antifungal effect of VOCs emitted by three-day-old?Xenorhabdus nematophila?and?Photorhabdus laumondii?subsp.?laumondii?Triptone Soya Broth (TSB)?ferments against?Botrytis cinerea?bunch rot on grapes four?days after infection.?a?Schematic diagram showing the methodological approach for testing antifungal activity of the VOCs emitted by?X. nematophila?and?P. laumondii?subsp.?laumondii.?b?Disease incidence.?c?Relative lesion area caused by?B. cinerea?mycelial growth. Different lower-case letters represent statistically significant differences between treatments according to Tukey?s multiple comparison test (P?