Trained immunity and immune priming in plants and invertebrates

Kurtz, Joachim; Andino, Raul; Boraschi, Diana; Contreras-Garduño, Jorge; Kachroo, Aardra; Khan, Imroze; Lanz Mendoza, Humberto; Mukherjee, Krishnendu; Peuß, Robert; Ton, Jurriaan

Abstract

Immune memory has long been thought to be restricted to the adaptive immune system of vertebrates. However, several lines of evidence have changed our understanding of immune memory and have shattered the strict separation between innate and adaptive immunity. In vertebrates, a form of innate immunity that is called ‘trained immunity’ has been intensively studied for over a decade. For more than two decades, studies in plants and an increasing number of invertebrate taxa have clearly demonstrated that these organisms also possess immune memory, despite the absence of an adaptive immune system. These phenomena are mostly known as ‘immune priming’. The mechanistic underpinnings of immune priming vary across taxa and may or may not partially include the epigenetic and metabolic mechanisms involved in trained immunity. Here, we offer an evolutionary perspective on immune priming, uniquely integrating key aspects across plants and invertebrates for the first time. As a basis, we provide a conceptual clarification regarding the terms trained immunity and immune priming and give a brief overview of these phenomena across taxa. We then analyze which processes of immune priming share potentially evolutionary conserved epigenetic and metabolic processes with trained immunity and explore signaling processes involved in immune priming. We discuss the aspect of specificity as one of the key defining criteria for immune memory and incorporate the potential role of soil and gut microbiota for acquiring innate immune memory in plants and invertebrates. Finally, we argue that immune priming has enormous potential for application beyond the medical field when involving the protection against parasites and pathogens in agriculture and aquaculture.