Tiny Transposons, Big Effects: How MITEs Organize Chromatin to Shape Gene Expression

Transposons are mobile elements that are commonly silenced to protect eukaryotic genome integrity. In plants, transposable element (TE)-derived inverted repeats (IRs) are commonly found near genes, where they affect host gene expression. However, the molecular mechanisms of such regulation are unclear in most cases. We found that the expression of these IRs is associated with production of 24-nt small RNAs, methylation of the IRs, and drastic changes in local 3D chromatin organization. Notably, many of these IRs differ between Arabidopsis thaliana accessions, causing variation in short-range chromatin interactions, gene expression and adaptative phenotypic traits. In a proof-of-concept case we found that an inverted-repeat transposon (EFR-associated IR, Ea-IR) located between the loci encoding the pathogen receptor EFR and myosin XI-k (XI-k) affects chromatin organization, promoting the formation of a repressive chromatin loop. Upon pathogen infection, chromatin changes correlate with increased EFR transcription. Arabidopsis accessions lacking Ea-IR have higher basal EFR levels and resistance to pathogens. We show a scenario in which a transposon, chromatin organization and gene expression interact to fine-tune immune responses, during both the course of infection and the course of evolution. Our data show that insertion of an IR near a gene provides an anchor point for chromatin interactions that profoundly impact the activity of neighboring loci. This turns IRs into powerful evolutionary agents that can contribute to rapid adaptation.

References

Mencia R, Arce AL, Houriet C, Xian W, Contreras A, Shirsekar G, Weigel D, Manavella PA. Transposon-triggered epigenetic chromatin dynamics modulate EFR-related pathogen response. Nat Struct Mol Biol. 2025. 32(1):199-211. doi:10.1038/s41594-024-01440-1.

Arce AL, Mencia R, Cambiagno DA, Lang PL, Liu C, Burbano HA, Weigel D, Manavella PA. Polymorphic inverted repeats near coding genes impact chromatin topology and phenotypic traits in Arabidopsis thaliana. Cell Rep. 2023. 31;42(1):112029. doi: 10.1016/j.celrep.2023.112029.

Gagliardi D, Cambiagno DA, Arce AL, Tomassi AH, Giacomelli JI, Ariel FD, Manavella PA. Dynamic regulation of chromatin topology and transcription by inverted repeat-derived small RNAs in sunflower. Proc Natl Acad Sci U S A. 2019. 27;116(35):17578-17583. doi: 10.1073/pnas.1903131116.