Comparative Genomic Analysis Reveals Multiple Long Terminal Repeats, Lineage-Specific Amplification, and Frequent Interelement Recombination for Cassandra Retrotransposon in Pear (Pyrus bretschneideri Rehd.)

Abstract

Cassandra transposable elements belong to a specific group of terminal-repeat retrotransposons in miniature (TRIM). Although Cassandra TRIM elements have been found in almost all vascular plants, detailed investigations on the nature, abundance, amplification timeframe, and evolution have not been performed in an individual genome. We therefore conducted a comprehensive analysis of Cassandra retrotransposons using the newly sequenced pear genome along with four other Rosaceae species, including apple, peach, mei, and woodland strawberry. Our data reveal several interesting findings for this particular retrotransposon family: 1) A large number of the intact copies contain three, four, or five long terminal repeats (LTRs) (∼20% in pear); 2) intact copies and solo LTRs with or without target site duplications are both common (∼80% vs. 20%) in each genome; 3) the elements exhibit an overall unbiased distribution among the chromosomes; 4) the elements are most successfully amplified in pear (5,032 copies); and 5) the evolutionary relationships of these elements vary among different lineages, species, and evolutionary time. These results indicate that Cassandra retrotransposons contain more complex structures (elements with multiple LTRs) than what we have known previously, and that frequent interelement unequal recombination followed by transposition may play a critical role in shaping and reshaping host genomes. Thus this study provides insights into the property, propensity, and molecular mechanisms governing the formation and amplification of Cassandra retrotransposons, and enhances our understanding of the structural variation, evolutionary history, and transposition process of LTR retrotransposons in plants.

Landscape and evolutionary dynamics of terminal-repeat retrotransposons in miniature (TRIMs) in 48 whole plant genomes

“…In addition to the typical TRIM elements (L 2 I 1 ), some TRIMs arranged tandemly and contained more than three LTRs and two internal regions, hereafter, referred to as tandemly arrayed (TA)-TRIMs. So far, this peculiar structure was reported only for the Cassandra TRIM which LTRs contain sequences similar to cellular 5S rRNA that is also tandemly arranged (Kalendar et al 2008; Yin et al 2014). However, 5S rRNA sequences were not found in other any TRIM families.…”

“…LTR retrotransposons are among the most prevalent elements in plants, but tandemly arrayed LTR retrotransposons have not been reported. The mechanism by which TA-TRIMs were created was likely due to homologous recombination between different elements (Devos et al 2002; Yin et al 2014). The factors that affect the generations of TA-TRIMs are not clear; however, our data indicate that it is not strongly correlated with TA-TRIM size.…”

“…The insertion times of TRIMs and other LTR retroelements were calculated using the formula: T = K/2r where T represents insertion time, K is average number of substitutions per aligned site and r means an average substitution rate which is 1.3 X 10 8 substitutions per synonymous site per year as suggested by Ma and Bennetzen in grasses (2004) but was also used in soybean and pear (Du et al 2010; Yin et al 2014). In this study, we used this substitution rate for other plants because no average substitution rate for transposons is available for many plants including V. carteri .…”

“…Owing to their extremely short length and lack of capacity to encode proteins, TRIMs are difficult to annotate. To date, only ten TRIM families, Katydid -At1, At2, At3 (Witte et al, 2001), Br1-Br4, Katydid -At4 (Yang et al, 2007), Cassandra (Kalendar et al 2008; Yin et al 2014) and SMART (Gao et al 2012), have been reported in the euphyllophytes. Recently, a TRIM was reported in the red harvester ant (PbTRIM, Pogonomyrmex barbatus , Zhou and Cahan 2012), the only one reported in animals and microbes.…”

Genome Size and the Role of Transposable Elements

“…For example, retrotransposon BARE2 of barley parasitizes BARE1 for its Gag (Tanskanen et al 2007). Non-autonomous groups of LTR retrotransposons including the Large Retrotransposon Derivative (LARD) elements (Kalendar et al 2004) and the Terminal-repeat Retrotransposons In Miniature, the TRIMs Witte et al 2001), both of which lack protein-coding capacity, are abundant and structurally conserved in plant genomes (AntoniusKlemola et al 2006;Wu et al 2012;Yin et al 2014) and found also in insects (Zhou and Cahan 2012), so therefore appear to have been successful at replication. The SINEs, which unlike the non-autonomous LTR retrotransposons constitute an order of their own , comprise the diverse sequences that can be propagated by the enzymatic machinery of the LINEs (Goodier and Kazazian 2008;Vassetzky and Kramerov 2013).…”