Genomic and Transcriptomic Survey Provides New Insight into the Organization and Transposition Activity of Highly Expressed LTR Retrotransposons of Sunflower (Helianthus annuus L.).

Ilya Kirov,Maxim Dudnikov,Elizaveta Kolganova,Pavel Merkulov,Murad Omarov,Gennady Karlov,Roman Komakhin,Sofya Gvaramiya,Alexander Soloviev

doi:10.3390/ijms21239331

Abstract

LTR retrotransposons (RTEs) play a crucial role in plant genome evolution and adaptation. Although RTEs are generally silenced in somatic plant tissues under non-stressed conditions, some expressed RTEs (exRTEs) escape genome defense mechanisms. As our understanding of exRTE organization in plants is rudimentary, we systematically surveyed the genomic and transcriptomic organization and mobilome (transposition) activity of sunflower (Helianthus annuus L.) exRTEs. We identified 44 transcribed RTEs in the sunflower genome and demonstrated their distinct genomic features: more recent insertion time, longer open reading frame (ORF) length, and smaller distance to neighboring genes. We showed that GAG-encoding ORFs are present at significantly higher frequencies in exRTEs, compared with non-expressed RTEs. Most exRTEs exhibit variation in copy number among sunflower cultivars and one exRTE Gagarin produces extrachromosomal circular DNA in seedling, demonstrating recent and ongoing transposition activity. Nanopore direct RNA sequencing of full-length RTE RNA revealed complex patterns of alternative splicing in RTE RNAs, resulting in isoforms that carry ORFs for distinct RTE proteins. Together, our study demonstrates that tens of expressed sunflower RTEs with specific genomic organization shape the hidden layer of the transcriptome, pointing to the evolution of specific strategies that circumvent existing genome defense mechanisms.

Highlights

long-terminal repeat (LTR) retrotransposons (RTEs) are mobile genetic elements capable of transposition via RNA intermediates
We showed that GAG-encoding open reading frame (ORF) are present at significantly higher frequencies in exRTEs, compared with non-expressed RTEs
We show that exRTEs are distinguished from their non-expressed counterparts by distinct genomic features, such as a recent insertion time, proximity to genes, low copy number, and enrichment in open reading frames (ORFs) encoding a GAG domain with one RNA-binding domain

Summary

Introduction

LTR retrotransposons (RTEs) are mobile genetic elements capable of transposition via RNA intermediates. Recent genome-wide surveys of RTE expression in animals and plants indicate that thousands of retrotransposons have detectable expressions [8,9]. This led to the coining of the term “retrotranscriptome” to describe the complement of RTE transcripts in a cell [10]. Genome-wide RTE expression analysis based on RNA-seq data established that up to 10.38% and 26.1% of all mapped reads were associated with long-terminal repeat (LTR) retrotransposons in tea tree (Camellia sinensis) and maize (Zea mays L.), respectively [15]. The environment of developing pollen cells favors TE expression

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