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

• Published in: PLoS genetics Vol. 20; no. 3; p. e1011200
• Main Authors: Thieme, Michael, Minadakis, Nikolaos, Himber, Christophe, Keller, Bettina, Xu, Wenbo, Rutowicz, Kinga, Matteoli, Calvin, Böhrer, Marcel, Rymen, Bart, Laudencia-Chingcuanco, Debbie, Vogel, John, Sibout, Richard, Stritt, Christoph, Blevins, Todd, Roulin, Anne C
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 12.03.2024; Public Library of Science (PLoS)
• Subjects: BASIC BIOLOGICAL SCIENCES; Brachypodium distachyon; Copy number; DNA methylation; DNA polymerases; DNA-directed RNA polymerase; Environmental aspects; Environmental factors; Enzymes; Evolution; Gene expression; Genetic aspects; Genetic diversity; Genetic transcription; Genetics; Genomes; Genomic instability; Genomics; Grasses; Life Sciences; Long terminal repeat; Methylation; Mobility; Mutagens; Mutation; Physiological aspects; Physiology; Plants genetics; RNA; siRNA; Transposition; Transposons; Vegetal Biology; Switzerland; Turkey
• ISSN: 1553-7404; 1553-7390; 1553-7404
• DOI: 10.1371/journal.pgen.1011200

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 role 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 transpositional 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.