Oomycetes as biocontrol agents: unveiling their potential and mechanisms in plant disease control

Plant disease outbreaks represent significant global food security and environmental sustainability challenges, resulting in reduced primary productivity, biodiversity, and critical food/feed shortages worldwide. The indiscriminate use of synthetic fungicides has already caused substantial harm to human health and ecosystems. Certain human diseases, such as Alzheimer's and autism, have risen dramatically over the past decades, a trend partially attributed to the use/overuse of fungicides in modern agriculture and horticulture. Given these alarming signs, it should be time to reconsider plant disease management strategies. The use of certain beneficial microorganisms, referred to as biological control agents, holds promise as an eco-friendly approach to combating plant pathogens. Oomycetes are often cast as the bad guys in the plant world, causing chaos through destructive diseases like late blight, damping off, and dieback, which might have catastrophic consequences such as the Irish potato famine. However, not all oomycetes are harmful! Some are good guys in disguise, showing promising potential to help us fight plant diseases, acting as effective biological control agents. Understanding the mechanisms underlying the protective effects of biocontrol oomycetes is crucial for achieving desirable outcomes and developing innovative strategies. The biocontrol mechanisms of oomycetes can be categorized into five classes: i) mycoparasitism, ii) exudation of lytic enzymes, iii) competition with pathogens over nutrients and space, iv) induced systemic resistance (ISR), and v) production of injection cells (gun cells). This review elucidates the biocontrol mechanisms employed by oomycetes, highlighting their potential practical implications as well as their positive impact on plant growth. Edaphic and environmental factors influencing the efficacy of biocontrol oomycetes are also discussed, alongside diverse strategies aimed at enhancing their biocontrol efficiency or broadening the spectrum of target pathogens. Despite advancements in understanding biocontrol oomycetes, their commercial application faces challenges due to inconsistent field performance influenced by environmental conditions, soil types, inoculum viability, competing microorganisms. Enhancing biocontrol oomycetes efficacy through the development of stable formulations, genetic modification, synthetic biology, combining multiple strains, and integrating with other agronomic practices can help overcome these challenges and promote their adoption in sustainable agriculture. Performing comprehensive risk assessments to avoid non-target effects, and streamlining regulatory approval processes are also crucial. Understanding how biocontrol oomycetes counteract plant pathogens will improve our fundamental knowledge of interactions between beneficial and harmful microbes, enhance our ability to predict plant disease development dynamics influenced by oomycetes-pathogen interactions, and facilitate the development of new tools for plant disease management with minimal environmental footprint.