The extent of Ds1 transposon to enrich transcriptomes and proteomes by exonization

Abstract

BackgroundExonization is an event which an intronic transposed element (TE) provides splice sites and leads to alternatively spliced cassette exons. Without disrupting of the inserted gene’s function, TEs can expand the proteome diversity by adding the splice variant that encodes a different, yet functional protein. Previously, we found that the main contribution of Ds exonization for gene divergence is not providing genetic messages but incorporating the intron sequences with different reading frame patterns to enrich the plant proteome. Ds1, another member of Ac/Ds transposon system, differs from Ds by providing 3 splice donor sites and 2 acceptor sites for alternative splicing, which may greatly increase the extent for proteome expansion.ResultsIn this study, we performed a genome-wide survey of Ds1 exonization events to assess its extent to enrich proteomes in plants. Each Ds1 insertion yielded 11 transcript isoforms by integrating the splice donor and/or acceptor sites, which composed a bulk of all exonized transcript orthologs from the dicot Arabidopsis thaliana and the monocot Oryza sativa (rice). The exonized transcripts were analyzed by the locations of the termination codon (PTC) and the putative targets for the nonsense-mediated decay (NMD) pathway were then excluded. Compared with the Ds element, Ds1 harbors more contents of non-NMD transcripts for protein isoforms.ConclusionsThe contribution of Ds1 exonization for gene divergence is incorporating the intron sequences with different reading frame patterns to enrich the plant proteome. All these simulation results direct new experimental analysis at the molecular level.Electronic supplementary materialThe online version of this article (doi:10.1186/1999-3110-54-14) contains supplementary material, which is available to authorized users.

The Ds1 Transposon Provides Messages That Yield Unique Profiles of Protein Isoforms and Acts Synergistically With Ds to Enrich Proteome Complexity via Exonization

“…Functional profile analyses were performed on the previously simulated Ds1 -exonized non-NMD protein variants in rice 11 according to the patterned-profile database in PROSITE. 12 From a total of 38 427 898 non-NMD variants, only 14 258 780 (4 303 236 interior and 9 955 544 C-terminal) variants yielding additional functional profile(s) were collected and termed as functional variants ( Table 1 and Figure 2 ).…”

“…Because only a maximum of 59 bp from a Ds1 message would be incorporated into the resulting protein isoforms, the major contribution of a TE to exonization was expected to be the incorporation of the message of TE-inserted intron of the affected transcripts rather than the message itself. 11 However, the Ds1 -independent and Ds1 -dependent profiles were composed of 314 and 398 unique profiles, respectively, with 253 overlapping profiles (Supplementary Table 2). This implies that the exonized Ds1 message is important for building functional profiles for selective advantage, either via the Ds1 message alone or together with its flanking intron/exon.…”

“…The Ds1 -exonized transcripts of rice were constructed previously. 11 In this study, open reading frame (ORF) analysis was conducted for all of these exonized transcripts beginning at the original start codon and ending at the first in-frame stop codon. The transcripts were categorized as type I, type II, type III, or type IV transcripts depending on, respectively, whether the in-frame stop codon was located at the conserved region of the original splice junction, at the intron inserted by Ds1 , at the Ds1 transposon itself, or at any exon occurring after the Ds1 insertion.…”

“… 5 , 9 Ds provides only donors (1 forward and 4 reverse insertion patterns), whereas Ds1 provides 3 donors and 2 acceptors associating with 11 possible exonizing patterns (all in reverse insertion patterns). 10 , 11 These different features between Ds and Ds1 imply possibly independent evolutionary impacts of Ds and Ds1 induced through exonization. To investigate their roles from an evolutionary perspective, we have simulated all putative Ds -exonized as well as Ds1 -exonized transcripts in the rice genome.…”

Analysis of New Functional Profiles of Protein Isoforms Yielded by Ds Exonization in Rice

“…In conclusion, via exonization events, TE inserts in introns of genes can yield protein variants with abundant and complex functional profiles by providing splice donor and/or acceptor sites. 21 Therefore, TE exonization can enrich the proteome for evolution because the TE is a medium to add and/or change the local domain, in large or small scale, of the reference protein. As a consequence, TE exonization diversifies a gene's products for selective advantage without disrupting the gene's function.…”