Sm/Lsm genes provide a glimpse into the early evolution of the spliceosome

Abstract

The spliceosome, a sophisticated molecular machine involved in the removal of intervening sequences from the coding sections of eukaryotic genes, appeared and subsequently evolved rapidly during the early stages of eukaryotic evolution. The last eukaryotic common ancestor (LECA) had both complex spliceosomal machinery and some spliceosomal introns, yet little is known about the early stages of evolution of the spliceosomal apparatus. The Sm/Lsm family of proteins has been suggested as one of the earliest components of the emerging spliceosome and hence provides a first in-depth glimpse into the evolving spliceosomal apparatus. An analysis of 335 Sm and Sm-like genes from 80 species across all three kingdoms of life reveals two significant observations. First, the eukaryotic Sm/Lsm family underwent two rapid waves of duplication with subsequent divergence resulting in 14 distinct genes. Each wave resulted in a more sophisticated spliceosome, reflecting a possible jump in the complexity of the evolving eukaryotic cell. Second, an unusually high degree of conservation in intron positions is observed within individual orthologous Sm/Lsm genes and between some of the Sm/Lsm paralogs. This suggests that functional spliceosomal introns existed before the emergence of the complete Sm/Lsm family of proteins; hence, spliceosomal machinery with considerably fewer components than today's spliceosome was already functional.

Figure 1. Phylogenetic tree of eukaryotic Sm/Lsm sequences.

Tree was built using maximum likelihood. The values on the nodes are bootstrapping values. The arks between branches indicate that sequences in both branches share an intron in the same position.

Figure 2. Phylogenetic tree of eukaryotic Lsm sequences.

Tree was built using maximum likelihood. The values on the nodes are bootstrapping values. The arks between branches indicate that sequences in both branches share an intron in the same position.

Figure 3. Phylogenetic tree of eukaryotic Sm sequences.

Tree was built using maximum likelihood. The values on the nodes are bootstrapping values. The arks between branches indicate that sequences in both branches share an intron in the same position.

Figure 4. Sequence alignment of eukaryotic Sm/Lsm proteins.

Overall alignment of the 14 district proteins: Lsm2–Lsm8, SmD1, SmD2, SmD3, SmE, SmF, SmG, SmB. Two representatives of each protein are shown from H.sapiens and P. falciparum. The protein secondary structure is illustrated above the alignment. The entire set of 355 sequences was aligned using ClustalW (see Text S1). Conserved positions in the alignment are shaded; positions conserved across most or all of the 355 sequences are labeled with a red dot below the alignment. Plots indicate the level of conservation, quality and consensus.

Figure 5. Sequence alignment of eukaryotic Lsm6 genes across the 17 eukaryotic species analyzed.

(For more details see legend in Figure 4.)

Figure 6. Structure of eukaryotic Sm/Lsm genes.

Intron positions are marked; intron phase is indicated as follows: green - phase 0 introns; blue - phase 1 introns; magenta - phase 2 introns. Arrows indicate common introns positions shared between two or more distinct Sm/Lsm genes. Intron positions in each of 14 Sm/Lsm genes: Lsm2–Lsm8, SmD1, SmD2, SmD3, SmE, SmF, SmG, SmB. There are two representatives per family: H.sapiens and P. falciparum.

Figure 7. Intron positions in the Lsm6 gene and its counterpart SmF gene across eukaryotic species.

Intron phase is indicated as follows: green- phase 0 introns; blue - phase 1 introns; magenta - phase 2 introns. Arrows indicate common introns positions shared between two or more distinct Sm/Lsm genes.

Figure 8. Intron positions in the Lsm7 gene and its counterpart SmG gene across eukaryotic species.

Intron phase is indicated as follows: green- phase 0 introns; blue - phase 1 introns; magenta - phase 2 introns. Arrows indicate common introns positions shared between two or more distinct Sm/Lsm genes.

Figure 9. Intron positions in the Lsm5 gene and its counterpart SmE gene across eukaryotic species.

Intron phase is indicated as follows: green- phase 0 introns; blue - phase 1 introns; magenta - phase 2 introns. Arrows indicate common introns positions shared between two or more distinct Sm/Lsm genes.

Figure 10. Intron positions in the Lsm2 gene and its counterpart SmD1 gene across eukaryotic species.

Intron phase is indicated as follows: green- phase 0 introns; blue - phase 1 introns; magenta - phase 2 introns.

Figure 11. Intron positions in the Lsm3 gene and its counterpart SmD2 gene across eukaryotic species.

Intron phase is indicated as follows: green - phase 0 introns; blue - phase 1 introns; magenta - phase 2 introns.

Figure 12. Intron positions in the Lsm4 gene and its counterpart SmD3 gene across eukaryotic species.

Intron phase is indicated as follows: green - phase 0 introns; blue - phase 1 introns; magenta - phase 2 introns.

Figure 13. Intron positions in the Lsm8 gene and its counterpart SmB gene across eukaryotic species.

Intron phase is indicated as follows: green - phase 0 introns; blue - phase 1 introns; magenta - phase 2 introns.