Evolutionary history of LTR retrotransposon chromodomains in plants

Abstract

Chromodomain-containing LTR retrotransposons are one of the most successful groups of mobile elements in plant genomes. Previously, we demonstrated that two types of chromodomains (CHDs) are carried by plant LTR retrotransposons. Chromodomains from group I (CHD_I) were detected only in Tcn1-like LTR retrotransposons from nonseed plants such as mosses (including the model moss species Physcomitrella) and lycophytes (the Selaginella species). LTR retrotransposon chromodomains from group II (CHD_II) have been described from a wide range of higher plants. In the present study, we performed computer-based mining of plant LTR retrotransposon CHDs from diverse plants with an emphasis on spike-moss Selaginella. Our extended comparative and phylogenetic analysis demonstrated that two types of CHDs are present only in the Selaginella genome, which puts this species in a unique position among plants. It appears that a transition from CHD_I to CHD_II and further diversification occurred in the evolutionary history of plant LTR retrotransposons at approximately 400 MYA and most probably was associated with the evolution of chromatin organization.

Figure 1

A neighbor-joining (NJ) phylogenetic tree based on multiple alignment of reverse transcriptase aminoacid sequences of LTR retrotransposons, including newly identified chromodomain-containing LTR retrotransposons from Selaginella moellendorffii (a) and the structural organization of novel retroelements from Selaginella (b). Statistical support was evaluated by bootstrapping (1000 replications); nodes with bootstrap values over 50% are shown. The plant-specific clades: Reina, CRM, Galadriel, and Tekay, as well as the Tcn1 clade, are indicated. The name of the host species and the accession number is indicated for the LTR elements that were taken from GenBank. Abbreviations: ORF: open reading frame, PR: aspartyl protease, RT: reverse transcriptase, RNH: ribonuclease H, INT: integrase, CHD_I and CHD_II: chromodomain group I and group II, CCHC: Zn-finger motif, TSD: target site duplications, and 5′ and 3′LTRs: 5′ and 3′ long terminal repeats. The positions of stop-codons (SM-Cranky) are marked by asterisks.

Figure 2

Maximum likelihood (ML) phylogenetic tree based on LTR retrotransposon chromodomain (CHD) aminoacid sequences including CHDs from newly identified chromodomain-containing LTR retrotransposons from Selaginella moellendorffii. Statistical support was evaluated by using aLTR; nodes with aLTR statistics over 50% are shown. The plant-specific clades Chlamyvir, Reina, CRM, Galadriel, and Tekay, as well as the Tcn1 clade, are indicated. The names of the host species and the accession numbers for the LTR elements are available in Supporting Information Figure 1S. The taxonomic range of the host species is indicated by colored boxes and includes angiosperms, gymnosperms, green algae, and nonseed plants (Selaginella and Physcomitrella).

Figure 3

Multiple alignment of chromodomains. The following were used in the alignment: the “classical” and “shadow” chromo-like motifs of functional proteins from diverse animal species and Arabidopsis (At_CMT1); group I and group II chromodomains from diverse plant LTR retrotransposons belonged to Tcn1, Galadriel, Reina, and Tekay clades as well as unclassified (Other); CHD_I from Tcn1 LTR retrotransposons of fungi Cryptococcus neoformans. The GenBank accession numbers are indicated for each sequence. The most conservative domains for each of the groups are shown on the top. The chromo-box is indicated on the very top, which also shows the secondary structure elements (arrows indicate β-strands; rectangle α-helix) and conserved residues that form the complementary surface that is responsible for H3 peptide recognition (green boxes) [–7]. Three aminoacids that have been shown to be under positive selection are highlighted in yellow.

Figure 4

Maximum likelihood (ML) phylogenetic trees of sampled reverse transcriptase (a), integrase (b), and chromodomains (c) from 39 LTR retrotransposons. The plant-specific clades: Reina, Galadriel, and Tekay, as well as the Tcn1 clade, are indicated. Statistical support was evaluated by bootstrapping (100 replications); bootstrap values within clades are not shown. The changing in position of SM1-Galahad and SM2-Galahad LTR retrotransposons from Selaginella are shown by a gray box for each tree. The results of selection tests are reported for the tested branches, as is the proportion of sites under particular selective regimes for clades/groups. The red color indicates branches where sites under positive selection at the cutoff posterior probability 90% were identified.

Figure 5

Multiple alignment including the “classical” chromodomain (dmHP1 from Drosophila melanogaster) and sampled representatives of group I and group II chromodomains from LTR retrotransposons (a); estimated tertiary structure for dmHP1 CHD (pdb : 1q3l; [7]) and predicted tertiary structures for some LTR retrotransposon CHDs (b). The GenBank accession numbers are indicated for each sequence used. The secondary structure elements are shownon the top (arrows indicate β-strands; rectangle α-helix) [–7]. Three aminoacids that were shown to be under positive selection in the Tekay-Reina cluster are highlighted in yellow. The aminoacids that are potentially under positive selection in the Galadiriel-Reina-Tekay cluster are highlighted in red. An additional helix structure is indicated by an arrow for representatives of the Reina and Tekay clades.

Figure 6

Distribution of different clades of chromodomain-containing LTR retrotransposons in plants as well as CHD_I and CHD_II. The evolutionary tree is represented according to Bowman et al., 2007 [40] and Berbee and Taylor, 2001 [41] with minor modifications. Divergence times (Mya: million years ago) are indicated according to Hedges, 2002 [42]. Other: SM-Diluvium and SM-Cranky.