Editorial: mobile elements and plant genome evolution, comparative analyzes and computational tools

Abstract

Multiple changes that occur constantly in the plant genome allow an organism to develop from a single-celled embryo to a multicellular organism. A significant part of these changes is associated with the recombination activity of numerous classes of interspersed repeats. These numerous families of interspersed repeats were often called "junk DNA" as they were not associated with vital protein-coding processes (1). Transposable elements (TEs), such as DNA transposons and retrotransposons, are the main part of these interspersed repeats (2). DNA transposons can rightfully be called true mobile elements, the activity of which can occur at any stage of cell development and manifest itself at any moment and stage of the organism's development. The diverse families of retrotransposons are highly abundant genetic elements that are related to retroviruses (3). Although retrotransposons are not true mobile elements like DNA transposons, retrotransposable elements (RTEs) form a variety of chromosomal structures, such as centromeric and telomeric regions (4), and are the main intergenic part of the genome (5). Retrotransposons move to new chromosomal locations via an RNA intermediate that is converted into extrachromosomal DNA by the encoded reverse transcriptase/RNaseH enzymes prior to reinsertion into the genome. This replicative mode of transposition can rapidly increase the copy number of elements and can thereby greatly increase plant genome size. RTEs can be clustered into distinct families each traceable to a single ancestral sequence or a closely related group of ancestral sequences. In contrast to multigene families, which are defined based on their biological role, repetitive families are usually defined based on their active ancestors (called master or source genes) and on their generation mechanisms. Over time, individual elements from repetitive families may acquire diverse biological roles. Some RTEs can provide evolutionary advantages to the host and increase their chances of survival (6). While the view that RTEs are beneficial to the host is not new, recent progress in the field has placed RTEs squarely in the center of the ongoing debate on eukaryotic evolution. To advance this important research field, in the Research Topic "Mobile Elements and Plant Genome Evolution, Comparative Analyses, and Computational Tools" we focus on the role of mobile elements with host genome evolution, discovery, and comparative and genome-wide profiling analysis of transposable elements. Different retrotransposon families, each with its own lineage and structure, may have been active at distinct phases in the evolution of a species. Retrotransposon sequences bear the promoters that bind the nuclear factors of transcription initialization and initiate RNA synthesis by polymerases II or III. In the article entitled "Additional ORFs in Plant LTR-Retrotransposons" by Vicient C.M. and Casacuberta J.M., LTR-retrotransposons that carry additional, not retrotransposon-specific open reading frames (aORF), were discovered and analyzed. This discovery expands on the unique potential of LTR-retrotransposons as evolutionary tools, as LTR-retrotransposons can be used to deliver new gene variants within a genome. The presence of a unique aORF in some characterized LTR-retrotransposon families like maize Grande, rice RIRE2, or Silene Retand, are just as typical as retrovirus gene transduction. As dispersed and ubiquitous mobile elements, the life cycle of replicative transposition leads to genome rearrangements that affect cellular function (7). Transposable elements are important drivers of species diversity and exhibit great variety in structure, size, and mechanisms of transposition, making them important putative actors in genome evolution. The research group led by Kashkush K., reported the potential impact of miniature transposable element insertions on the expression of wheat genes in different wheat species in the articles entitled "The Evolutionary Dynamics of a Novel Miniature Transposable Element in the Wheat Genome" and "Where the Wild Things Are: Transposable Elements as Drivers of Structural and Functional Variations in the Wheat Genome". The induced genetic rearrangements and insertions of mobile genetic elements in regions of active euchromatin contribute to genome alteration, which leads to "genomic stress" (8). TEmediated epigenetic modifications lead to phenotypic diversity, genetic variation, and environmental stress tolerance. TEs also contribute to genome plasticity and have a dramatic impact on the genetic diversity and evolution of the wheat genome. Using transposon display (9) and genome-wide profiling analysis of insertional polymorphisms of transposable elements (10), the authors discovered large genomic rearrangement events, such as deletions and introgressions in the wheat genome. High-throughput bioinformatics with next-generation sequencing (NGS) were key tools in these studies (11). Chromosomal rearrangements, gene duplications, and transposable element content may have a large impact on genomic structure, which could generate new phenotypic traits (7). In the article entitled "Genome Size Variation and Comparative Genomics Reveal Intraspecific Diversity in Brassica rapa", de Carvalho J.F. et al investigated structural variants and repetitive content between two accessions of Brassica rapa genomes and genome-size variation among a core collection using comparative genomics and cytogenetic approaches. Large genomic variants with a chromosome length difference of 17.6% between the A06 chromosomes of 'Z1' compared to 'Chiifu' belonging to different cultigroups of B. rapa highlighted the potential impact of differential insertion of repeat elements and inversions of large genomic regions in genome size intraspecific variability. Transposable elements are also the driving force in the evolution of epigenetic regulation and have a long-term impact on genomic instability and evolution. Remnants of RTEs appear to be overrepresented in transcription regulatory modules and other regions conserved among distantly related species, which may have implications for our understanding of their impact on speciation. RTEs are dynamic and play a role in chromosome crossing over recognition and in DNA recombination between homologous chromosomes. In the article entitled "Sequencing Multiple Cotton Genomes Reveals Complex Structures and Lays Foundation for Breeding", Wang X. et al revealed that post-polyploidization of cotton genome instability resulted in numerous genomic structural changes, DNA inversion and translocation, illegitimate recombinations, accumulation of repetitive sequences, and functional innovation accompanied by elevated evolutionary rates of genes. This genome study also revealed the evolutionary past of cotton plants, which were recursively affected by polyploidization, with a decaploidization contributing to the formation of the genus Gossypium, and a neo-tetraploidization contributing to the formation of the currently widely cultivated cotton plants. The centromere is a unique part of the chromosome that combines a conserved function with extreme variability in its DNA sequence. In the article entitled "Functional Allium fistulosum centromeres comprise arrays of a long satellite repeat, insertions of retrotransposons and chloroplast DNA" Kirov G.I., et al studied the largest plant genomic organization of the functional centromere in large-sized chromosomes in Allium fistulosum and A. cepa. Long, high-copy repeats are associated with insertions of retrotransposons and plastidial DNA, and the landscape of the centromeric regions of these species possess insertions of plastidial DNA. Among evolutionary factors, repetitive sequences play multiple roles in sex chromosome evolution. As such, the Spinacia genus serves as an ideal model to investigate the evolutionary mechanisms underlying the transition from homomorphic to heteromorphic sex chromosomes. This was studied in the article entitled "Genome-Wide Analysis of Transposable Elements and Satellite DNAs in Spinacia Species to Shed Light on Their Roles in Sex Chromosome Evolution" by Li N., et al. Major repetitive sequence classes in male and female genomes of Spinacia species and their ancestral relative, sugar beet, were elucidated in the evolutionary processes of sex chromosome evolution using NGS data. The differences of repetitive DNA sequences correlate with the formation of sex chromosomes and the transition from homomorphic sex chromosomes to heteromorphic sex chromosomes, as heteromorphic sex chromosomes existed exclusively in Spinacia tetrandra.