Trained immunity and immune priming in plants and invertebrates
- Institute for Evolution and Biodiversity, University of Münster, Germany
- Department of Microbiology and Immunology, University of California, San Francisco, United States
- Shenzhen University of Advanced Technology, China
- Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, China
- National Research Council, Italy
- Stazione Zoologica Anton Dohrn, Italy
- Escuela Nacional de Estudios Superiores, Universidad Nacional Autónoma de Mexico, Mexico
- Department of Plant Pathology, University of Kentucky, United States
- Trivedi School of Biosciences, Ashoka University, India
- Instituto Nacional de Salud Pública. Centro de Investigaciones sobre Enfermedades Infecciosas, Mexico
- Institute of Hygiene, University of Münster, Germany
- Institute for Integrative Cell Biology and Physiology, University of Münster, Germany
- School of Biosciences University of Sheffield, United Kingdom
Figures
Figure 1
Immune priming in plants.
Plants use internal and external mechanisms to generate and maintain defense memory. In response to stress by pathogens or herbivores, plants change the epigenetic makeup of their genome, providing a long-lasting increase in defense capacity via priming of the innate immune system (red). In addition, stressed plants can alter the chemical composition of their root exudates, thereby recruiting and selecting plant-beneficial soil microbes, which in turn can suppress pests and diseases through a range of direct and indirect mechanisms. Together, both strategies provide the plant with long-lasting defense memory, making them more capable of resisting recurrent attacks by pathogens and herbivores.
Figure 2
Potential mechanisms of immune priming in invertebrate animals.
The figure combines selected examples from different invertebrates, with a focus on arthropods, to show some of the mechanisms involved in immune priming. 1. Dscam acting as a phagocytosis receptor or opsonin mediating specificity in priming Dong et al., 2025; Ng and Kurtz, 2020; Watson et al., 2005; 2. Specificity of phagocytosis based on other pattern recognition receptors (PRRs) Moné et al., 2010; Pham et al., 2007; Roth and Kurtz, 2009; 3. Pathogen-specific effectors differentially regulated upon priming, e.g., detected in transcriptome studies Ferro et al., 2019; Tate et al., 2017; 4. Endoreplication in the midgut of mosquitoes upon priming with Plasmodium Cime-Castillo et al., 2018; Maya-Maldonado et al., 2021; 5. Midgut epithelial cells release PGE2 upon contact with gut microbiota, leading to release of a hemocyte differentiation factor (HDF) from oenocytes, which is dependent on Tip60-mediated histone acetylation Gomes et al., 2021; 6. Epigenetically controlled expression of PGRP-SC in the gut mediating AMP secretion by the fat body Deng et al., 2025; 7. Oral priming may depend on the presence of microbiota (Futo et al., 2015; Prakash et al., 2023), lead to changes in microbiota composition (Korša et al., 2022) and gut morphology (Baur et al., 2025). Figure based on Milutinović et al., 2016 with updates informed by recent literature.
Figure 3
Two models of epigenetically controlled immune memory in plants.
The trans-regulatory model involves major induced DNA de-methylation in TE-rich peri-centromeric regions by ROS1, which antagonizes the heterochromatin maintenance machinery by DNA methyltransferases (DMTs), chromatin re-modelers (e.g. DDM1) and canonical RNA-directed DNA methylation (RdDM). To prevent large-scale pericentromeric TE expression and nuclear disruption, post-translational gene silencing and RDR6-dependent non-canonical RdDM (ncRdDM) rapidly generate 21/22-nt small RNAs (sRNAs) that are loaded onto AGO1. Due to partial sequence complementarity between TEs and distant defense genes, sRNAs-AGO1 complex interacts with gene bodies/promoters of distant defense genes and recruits the SWI-SNF chromatin re-modeling complex, which relaxes the chromatin environment and primes the defense genes for enhanced induction by transcription factors (TFs) upon secondary stress. The cis-regulatory model on the right involves stress-induced DNA demethylation of TEs near defense genes within the chromosome arms. Due to a delayed DNA re-methylation response in these regions, the relaxed chromatin environment of the hypo-methylated TE mediates long-term priming of the nearby defense gene. The trans-model is based on Liu et al., 2018 and Wilkinson et al., 2023; the cis-model is based on López Sánchez et al., 2016 and Halter et al., 2021.
Figure 4
Signaling and epigenetic processes.
The figure provides a simplified overview of some of the key mechanisms involved in immune priming in plants and invertebrates. Created with BioRender.
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Trained immunity and immune priming in plants and invertebrates
eLife 14:e106597.
https://doi.org/10.7554/eLife.106597
