Evolutionary genomics revealed interkingdom distribution of Tcn1-like chromodomain-containing Gypsy LTR retrotransposons among fungi and plants

Abstract

Background: Chromodomain-containing Gypsy LTR retrotransposons or chromoviruses are widely distributed among eukaryotes and have been found in plants, fungi and vertebrates. The previous comprehensive survey of chromoviruses from mosses (Bryophyta) suggested that genomes of non-seed plants contain the clade which is closely related to the retrotransposons from fungi. The origin, distribution and evolutionary history of this clade remained unclear mainly due to the absence of information concerning the diversity and distribution of LTR retrotransposons in other groups of non-seed plants as well as in fungal genomes.

Results: In present study we preformed in silico analysis of chromodomain-containing LTR retrotransposons in 25 diverse fungi and a number of plant species including spikemoss Selaginella moellendorffii (Lycopodiophyta) coupled with an experimental survey of chromodomain-containing Gypsy LTR retrotransposons from diverse non-seed vascular plants (lycophytes, ferns, and horsetails). Our mining of Gypsy LTR retrotransposons in genomic sequences allowed identification of numerous families which have not been described previously in fungi. Two new well-supported clades, Galahad and Mordred, as well as several other previously unknown lineages of chromodomain-containing Gypsy LTR retrotransposons were described based on the results of PCR-mediated survey of LTR retrotransposon fragments from ferns, horsetails and lycophytes. It appeared that one of the clades, namely Tcn1 clade, was present in basidiomycetes and non-seed plants including mosses (Bryophyta) and lycophytes (genus Selaginella).

Conclusions: The interkingdom distribution is not typical for chromodomain-containing LTR retrotransposons clades which are usually very specific for a particular taxonomic group. Tcn1-like LTR retrotransposons from fungi and non-seed plants demonstrated high similarity to each other which can be explained by strong selective constraints and the 'retained' genes theory or by horizontal transmission.

Figure 1

Neighbor-joining (NJ) phylogenetic trees based on RT and partial Int amino acid sequences of Gypsy LTR belonging to Ylt1 and SN_1006 clades. Statistical support was evaluated by bootstrapping (1000 replications); nodes with bootstrap values over 50% are indicated. The Gypsy LTR retrotransposons clades are shown on the right and include Chromovirus, Osvaldo, mag, Gypsy, mdg3, SN_1006 and Ylt1. Sequences of human immunodeficiency viruses (Retroviridae) were used as outgroup. The name of the host species and accession number are indicated for all elements taken from GenBank. Newly identified retrotransposons are highlighted by bold; localization in genomic sequence is indicated for each of them. Genomic sequences of Laccaria bicolor S238N and Nectria haematococca MPVI have been taken from The DOE Joint Genome Institute [55]; the following species are available at Broad Institute [54]: Botrytis cinerea B05.10; Pyrenophora tritici-repentis Pt-1C-BFP; Coprinus cinereus okayama7#130; Puccinia graminis f. sp. tritici. For more details: Additional files 1, 5 and 6.

Figure 2

Neighbor-joining (NJ) phylogenetic trees based on RT and partial Int amino acid sequences of Gypsy LTR retrotransposons including newly described fungal chromodomain-containing LTR retrotransposons. Statistical support was evaluated by bootstrapping (1000 replications); nodes with bootstrap values over 50% are indicated. The clades are shown on the right. The name of the host species and accession number are indicated for all elements taken from GenBank. Newly identified retrotransposons are highlighted in bold; localization in genomic sequence is indicated for each of them. Genomic sequences of Trichoderma reesei QM6a, Trichoderma virens Gv29-8, Nectria haematococca MPVI, Aspergillus niger ATCC1015, Alternaria brassicicola ATCC 96866, Stagonospora nodorum SN15, Laccaria bicolor S238N, Postia placenta MAD-698, and Sporobolomyces roseus have been taken from The DOE Joint Genome Institute [55]; the following species are available at Broad Institute [54]: Chaetomium globosum CBS 148.51; Fusarium oxysporum 4286 FGSC;Fusarium verticillioides 7600; Aspergillus clavatus NRRL 1; Aspergillus terreus NIH2624; Coccidioides immitis RS; Histoplasma capsulatum NAm1; Uncinocarpus reesii 1704; Sclerotinia sclerotiorum 1980; Botrytis cinerea B05.10; Pyrenophora tritici-repentis Pt-1C-BFP; Coprinus cinereus okayama7#130; Puccinia graminis f. sp. tritici; Batrachochytrium dendrobatidis JEL423. The possible horizontal transmission (HT) is marked. For more details: Additional files 1, 5 and 6.

Figure 3

Structural organization of a number of full-length LTR retrotransposons from fungi and SM-Tcn1 LTR retrotransposon from spikemoss Selaginella moellendorffii identified in present study. The clade for each of elements is shown on the left. Abbreviations: LTR - long terminal repeat, TSD - target site duplication, PR - proteinase, RT - reverse transcriptase, RH - ribonuclease H, Int - core integrase, chromo - chromodomain, dUTPase - deoxyuridine triphosphatase domain, CCHC and HHCC - Zn-finger motifs, add. ORF - additional open reading frame with unknown function, PPT - polypurine tract, PBS? - no putative primer-binding site was found for SM-Tcn1.

Figure 4

Neighbor-joining (NJ) phylogenetic tree based on RT nucleotide sequences of CHD-containing Gypsy LTR retrotransposons including newly described elements from monilophytes and lycophytes plants (highlighted in bold). Statistical support was evaluated by bootstrapping (1000 replications); nodes with bootstrap values over 50% are indicated. The name of the host species and accession number are indicated for LTR retrotransposons taken from GenBank. Four diverse clusters of LTR retrotransposons from mosses, monilophytes and lycophytes are shown by arrows. The group of Tcn1-like LTR retrotransposons from mosses (Bryophyta) is also indicated. Previously known clades, clades described in this study, and unclassified lineages (a-f) are shown on the right.

Figure 5

Distribution of different clades of CHD-containing Gypsy LTR retrotransposons in plants. 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 [27]. Data suggest that Tcn1-like LTR retrotransposons were horizontally transmitted between fungi and non-seed plants (indicated by arrows). Presumably HT took place among fungi and the last common ancestor (LCA) of mosses and lycophytes (indicated as 1). Alternatively, it is possible that two independent acts of HT occurred (indicated as 2). First HT event could happen among fungi and LCA of mosses since all investigated mosses contain Tcn1-like LTR retrotransposons. The second HT could occur among fungi and LCA of Selaginella since only representatives of this genus carry this group of retrotransposons among all the investigated lycophytes.