Twenty years of transposable element analysis in the Arabidopsis thaliana genome

Abstract

Transposable elements (TEs) are mobile repetitive DNA sequences shown to be major drivers of genome evolution. As the first plant to have its genome sequenced and analyzed at the genomic scale, Arabidopsis thaliana has largely contributed to our TE knowledge. The present report describes 20 years of accumulated TE knowledge gained through the study of the Arabidopsis genome and covers the known TE families, their relative abundance, and their genomic distribution. It presents our knowledge of the different TE family activities, mobility, population and long-term evolutionary dynamics. Finally, the role of TE as substrates for new genes and their impact on gene expression is illustrated through a few selected demonstrative cases. Promising future directions for TE studies in this species conclude the review.

Fig. 1

Transposable element structures. a)LTR retrotransposons: gag encodes a polyprotein with a capsid and a nucleocapsid domain. The Pol gene produces three proteins: a protease (PR), a reverse-transcriptase endowed with an RT (reverse-transcriptase) and an RNAse H domain, and an integrase (INT). The gag and pol genes are expressed either as a fusion into a single open reading frame (ORF) that is then cleaved, or by the introduction of a frameshift between the two ORFs. Sometimes an envelope gene (ENV) is found. LTRs are divided into 3 regions: U3 may contain regulatory motifs and a promoter region, R contains both the start and termination sites for transcription, and U5 is the remaining part. The PBS operates as tRNA primer-binding to prime the first strand DNA synthesis, the minus-strand. The PPT is a short purine-rich sequence that primes the second strand DNA synthesis, the plus-strand. TSD: Target Site Duplication is a short direct repeat that is generated on both flanks of a TE upon insertion. Gypsy and Copia superfamilies differ according to the position of the integrase in the polyprotein pol.b)LINE: Encodes two open reading frame: ORF1 and ORF2. ORF1 encodes a non-sequence-specific RNA binding protein that functions as chaperone. ORF2 encodes an endonuclease (EN), which makes a single-stranded nick in the genomic DNA and a reverse transcriptase (RT), which uses the nicked DNA to prime reverse transcription. They are terminated by a polyA or A/T-rich tail. SINE: SINE sequences contain the box A and B conserved motifs that serve as an internal promotor. c)TIR: TIR transposons encode a transposase protein necessary for mobility, and are bordered by Terminal Inverted Repeats (TIRs). Helitrons: generally contain a Y2-type tyrosine recombinase (YR) along with Replication protein A (RPA) and other proteins to catalyze their mobility, a hairpin structure, 5′ TC and 3′ CTRR termini (R = A or G). Insertion occurs into the target dinucleotide AT (shown in lowercase)

Fig. 2

TE genomic distributions. a) TE category genome coverage. b) Relative TE category copy numbers. c) Chromosomal copy number distribution per 100 kb windows overlapping by 10 kb. Red bars indicate regions with more than 30 copies in the window

Fig. 3

Ten most abundant TE families per TE category

Fig. 4

Some examples of TE insertion impact on genes. a) The FWA locus is repressed in vegetative tissues and the parentally-derived allele through an epigenetic mechanism induced by an old SINE insertion. Ectopic expression of the locus in a demethylated context causes a late-flowering phenotype. b) The FLC locus has a lower expression in the Ler accession caused by a Mutator-like insertion that affects the mRNA structure. c) The BONSAI locus is repressed by the loss of methylation of a LINE element inserted downstream. The TE is transcriptionally reactivated and produces small RNAs that repress the APC13-like gene to provoke a Bonsai phenotype