Transposition of HOPPLA in siRNA-deficient plants suggests a limited effect of the environment on retrotransposon mobility in Brachypodium distachyon

Authors: THIEME, MICHAEL - University Of Zurich; MINADAKIS, NIKOLAOS - University Of Zurich; HIMBER, CHRISTOPHE - Université De Strasbourg: Accueil; KELLER, BETTINA - University Of Zurich; XU, WENBO - University Of Zurich; RUTOWICZ, KINGA - University Of Zurich; MATTEOLLI, CALVIN - Université De Strasbourg: Accueil; BOHRER, MARCEL - Université De Strasbourg: Accueil; RYMEN, BART - Université De Strasbourg: Accueil; L Chingcuanco, Debbie; VOGEL, JOHN - Joint Genome Institute; SIBOUT, RICHARD - Inrae; STRITT, CHRISTOPH - Swiss Tropical Institute(STI); BLEVINS, TODD - Université De Strasbourg: Accueil; ROULIN, ANNE - University Of Zurich

Submitted to: PLoS Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/23/2024
Publication Date: 3/12/2024
Citation: Thieme, M., Minadakis, N., Himber, C., Keller, B., Xu, W., Rutowicz, K., Matteolli, C., Bohrer, M., Rymen, B., Chingcuanco, D.L., Vogel, J., Sibout, R., Stritt, C., Blevins, T., Roulin, A. 2024. Transposition of HOPPLA in siRNA-deficient plants suggests a limited effect of the environment on retrotransposon mobility in Brachypodium distachyon. PLoS Genetics. https://doi.org/10.1371/journal.pgen.1011200.
DOI: https://doi.org/10.1371/journal.pgen.1011200

Interpretive Summary: Transposable elements are regarded as powerful mutagens that create genetic variations that drive evolution. In this paper the authors explored the role of genetic and environmental factors influence on the mobilization of long terminal repeat retrotransposons (LTR-RTs) which uncontrolled and selfish proliferation can lead to deleterious mutations and genome instability that affect host fitness. HOPPLA LTR-RT copy number variations in nine accessions of Brachypodium distachyon exposed to different eight different stresses showed that environmental stresses have little effect on LRT-RT mobilization. Instead, it was the loss of RNA polymerase IV (Pol IV), which mediates RNA-directed DNA methylation in plants, that results in high transcriptional and transposition activities of LTR-RT (HOPPLA) family elements, and that these effects are not stress-specific. This work supports the finding that LTR-RT mobility in B. distachyon, a wild grass model, is controlled by host RNA-directed DNA methylation rather than environmental factors.

Technical Abstract: Long terminal repeat retrotransposons (LTR-RTs) are powerful mutagens regarded as a major source of genetic novelty and important drivers of evolution. Yet, the uncontrolled and potentially selfish proliferation of LTR-RTs can lead to deleterious mutations and genome instability, with large fitness costs for their host. While population genomics data suggest that an ongoing LTR-RT mobility is common in many species, the understanding of their dual roles in evolution is limited. Here, we harness the genetic diversity of 320 sequenced natural accessions of the Mediterranean grass Brachypodium distachyon to characterize how genetic and environmental factors influence plant LTR-RT dynamics in the wild. When combining a coverage-based approach to estimate global LTR-RT copy number variations with mobilome-sequencing of nine accessions exposed to eight different stresses, we find little evidence for a major role of environmental factors in LTR-RT accumulations in B. distachyon natural accessions. Instead, we show that loss of RNA polymerase IV (Pol IV), which mediates RNA-directed DNA methylation in plants, results in high transcriptional and transposition activities of RLC_BdisC024 (HOPPLA) LTR-RT family elements, and that these effects are not stress-specific. This work supports findings indicating an ongoing mobility in B. distachyon and reveals that host RNA-directed DNA methylation rather than environmental factors controls their mobility in this wild grass model.