Acquisition of an Archaea-like ribonuclease H domain by plant L1 retrotransposons supports modular evolution

Abstract

Although a variety of non-LTR retrotransposons of the L1 superfamily have been found in plant genomes over recent decades, their diversity, distribution, and evolution have yet to be analyzed in depth. Here, we perform comprehensive comparative and evolutionary analyses of L1 retrotransposons from 29 genomes of land plants covering a wide range of taxa. We identify numerous L1 elements in these genomes and detect a striking diversity of their domain composition. We show that all known land plant L1 retrotransposons can be grouped into five major families based on their phylogenetic relationships and domain composition. Moreover, we trace the putative evolution timeline that created the current variants and reveal that evolutionary events included losses and acquisitions of diverse putative RNA-binding domains and the acquisition of an Archaea-like ribonuclease H (RNH) domain. We also show that the latter RNH domain is autonomously active in vitro and speculate that retrotransposons may play a role in the horizontal transfer of RNH between plants, Archaea, and bacteria. The acquisition of an Archaea-like RNH domain by plant L1 retrotransposons negates the hypothesis that RNH domains in non-LTR retrotransposons have a single origin and provides evidence that acquisition happened at least twice. Together, our data indicate that the evolution of the investigated retrotransposons can be mainly characterized by repeated events of domain rearrangements and identify modular evolution as a major trend in the evolution of plant L1 retrotransposons. E ver since the discovery of the first transposon by Barbara McClintock in 1948 in maize, plants have provided a prime model system to study transposition. Both DNA transposons and retrotransposons are abundant in plants (1) and play a major role in driving genetic diversity and evolution of these organisms. Interestingly, non-LTR retrotransposons, the class of retrotransposons that is most represented in mammals, are found less abundantly in plants (2-5). More recently, however, a variety of non-LTR retrotransposons has been discovered in plants, and they were classified to three non-LTR retrotransposon superfamilies: retrotransposable element (RTE), Dualen, and L1 (6-8).The L1 superfamily is perhaps the best-studied plant non-LTR retrotransposon group, members of which have been identified in most plants. Among other species, they occur in corn [Zea mays (Cin4)], thale cress [Arabidopsis thaliana (Ta11-1)], and the alga Chlorella vulgaris (Zepp) (9-11).In general, plant L1 retrotransposons carry two ORFs. The protein encoded by ORF1 (ORF1p) usually contains an RNA recognition motif (RRM) (12)(13)(14). Similarly, human L1 ORF1p, which presumably acts as an RNA chaperone (15), also contains an RRM that was shown to bind single-stranded nucleic acids in cooperation with the ORF1p C-terminal domain (14). The second ORF (ORF2) of plant L1 retrotransposons encodes a polyprotein (ORF2p) that exhibits apurinic/apyrimidinic endonuclease (APE) and reverse transcriptase (RT) activities....

Profiling of extensively diversified plant LINEs reveals distinct plant‐specific subclades

“…Although some LINE‐CS subclade members like L1‐1_Pt of poplar (6095 bp, Jurka et al ., ) harbor longer ORFs, all LINE‐CS lack the RNase H domain. RRM‐containing LINEs of the BNR subclade such as Belline1/BNR (Heitkam and Schmidt, ) harbor an additional N‐terminal RRM in ORF1, which most likely substitutes the RNA‐binding function of the zinc finger. Some BNR members have an RNase H domain. Members of the PUR subclade contain a homolog to a so‐called purine‐rich (PUR) domain in their ORF1 (Smyshlyaev et al ., ). This subclade has few members, nevertheless, an exceptional high number of PUR LINEs has been detected in the primitive V. vinifera genome (Table ).…”

“…L1 LINEs of eudicots group into the LIb, LINE‐CS, BNR, or PUR subclade, whereas L1 LINEs of monocots are assigned to the LIb, cin4, Karma, or nubo subclade. Very recently, 149 L1 elements were mined from multiple genomes and Repbase (Jurka et al ., ), dividing higher plant L1 elements into four main groups (Smyshlyaev and Blinov, ; Smyshlyaev et al ., ). Our comprehensive data not only supports these groups, but also further resolves them and establishes seven L1 subclades supported by RT similarity and structural hallmarks of representative full‐length copies.…”

“…RTE and L1 LINEs have one or two open reading frames (ORFs), respectively, encoding proteins required for retrotransposition: an endonuclease (EN), an RT, and often a ribonuclease (RNase H, (RH)) (Smyshlyaev et al ., ). The functions of the L1 ORF1 comprise the binding, protection and transport of the LINE mRNA to its genomic target site (Martin, ).…”

Mobile Bacterial Group II Introns at the Crux of Eukaryotic Evolution

“…6). As both REL and RNase H domains are found in some subgroups of nuclear non-LTR-retrotransposons (135,191), these findings raise the possibility that Prp8 may be derived from another non-LTR-retroelement that is evolutionarily related to and possibly a missing link between group II introns and the spliceosome (192).…”

“…The Prp8 configuration of the thumb, long linker, and REL domain is similar to that in the R2Bm RT. Although group II intron RTs and the R2Bm RT lack an RNase H domain, RNase H domains are known to be acquired sporadically in different non-LTR-retrotransposon lineages (135,191). RVT RTs, another potential candidate for an ancestor of Prp8 (181), lack En and integrase domains and are further distinguished from group II intron and non-LTR-retrotransposon RTs by a large acidic insertion within RT-2a and by conserved N-and C-terminal domains that are not found in other proteins (212).…”