MITE Annotation and Landscape in 207 Plant Genomes Reveal Their Evolutionary Dynamics and Functional Roles.

Abstract

Miniature inverted-repeat transposable elements (MITEs) are short, non-autonomous class II transposable elements prevalent in eukaryotic genomes, contributing to various genomic and genic functions in plants. However, research on MITEs mainly targets a few species, limiting a comprehensive understanding and systematic comparison of MITEs in plants. Here, we developed a highly sensitive MITE annotation pipeline with a low false positive rate and applied it to 207 high-quality plant genomes. We found over a 20,000-fold variation in MITE copy numbers among species. The Mutator superfamily accounted for 41.5% of MITEs, whereas the Tc1/Mariner and PIF/Harbinger superfamilies expanded rapidly in monocots, particularly in Poaceae. Insertion time analysis revealed a general pattern of a single amplification wave, with initial insertions occurring around 30 million years ago (Mya) and peaking at 0-9 Mya. In addition, some species exhibited evidence of another ancient, slower expansion phase. In three representative families, we identified many more species-specific MITE loci than shared MITE loci, underscoring MITEs' significant role in genome diversity. Phylogenomic analyses indicate that MITEs accumulated gradually and specifically during speciation, primarily through recent insertions rather than the retention of ancient elements. MITEs preferentially insert near genes and are often associated with enhanced gene expression. Furthermore, we identified 985 MITE-derived miRNAs from 392 families across 56 species, mainly from Mutator, Tc1/Mariner, and PIF/Harbinger, targeting a variety of gene functions. This study enhances our understanding of the evolution and functional roles of MITEs in plants and provides a basis for exploring their function in further research.