Origin of the plant Tm-1-like gene via two independent horizontal transfer events and one gene fusion event

Abstract

The Tomato mosaic virus (ToMV) resistance gene Tm-1 encodes a direct inhibitor of ToMV RNA replication to protect tomato from infection. The plant Tm-1-like (Tm-1L) protein is predicted to contain an uncharacterized N-terminal UPF0261 domain and a C-terminal TIM-barrel signal transduction (TBST) domain. Homologous searches revealed that proteins containing both of these two domains are mainly present in charophyte green algae and land plants but absent from glaucophytes, red algae and chlorophyte green algae. Although Tm-1 homologs are widely present in bacteria, archaea and fungi, UPF0261- and TBST-domain-containing proteins are generally encoded by different genes in these linages. A co-evolution analysis also suggested a putative interaction between UPF0261- and TBST-domain-containing proteins. Phylogenetic analyses based on homologs of these two domains revealed that plants have acquired UPF0261- and TBST-domain-encoding genes through two independent horizontal gene transfer (HGT) events before the origin of land plants from charophytes. Subsequently, gene fusion occurred between these two horizontally acquired genes and resulted in the origin of the Tm-1L gene in streptophytes. Our results demonstrate a novel evolutionary mechanism through which the recipient organism may acquire genes with functional interaction through two different HGT events and further fuse them into one functional gene.

Figure 1

The phylogenetic tree of the green plant Tm-1L genes (A) and their exon/intron structures (B). The numbers above the branches represent the bootstrap values for the maximum likelihood and distance analyses, respectively. The asterisks indicate values <50%. The exons are indicated by boxes, whereas introns are indicated by lines. The UPF0261 domain regions are indicated by red boxes, while the TBST domain regions are indicated by green boxes. The number above an intron indicates the phase.

Figure 2. Phylogenetic analyses and the domain structures of the genes encoding UPF0261-domain-containing proteins.

(A) Phylogenetic analyses of the proteins containing a UPF0261 domain. The numbers above the branches represent the bootstrap values for the maximum likelihood and distance analyses. All of the sequences were obtained from NCBI, except for those in the green plants, and each protein is indicated by the GI numbers in NCBI and its genus. (B) The domain structure of the proteins that were used in the phylogeny.

Figure 3. Phylogenetic analyses and the domain structures of the genes encoding TBST-domain-containing proteins.

(A) Phylogenetic analyses of the proteins containing a TBST domain. The numbers above the branches represent the bootstrap values for the maximum likelihood and distance analyses. All of the sequences were obtained from the NCBI, except for those in the green plants, and each protein is indicated by the GI numbers in NCBI and its genus. (B) The domain structure of the proteins that were used in the phylogeny.

Figure 4. An evolutionary scenario for the origin of the plant Tm-1L gene.

(A) Horizontal gene transfer events associated with the origin of Tm-1 homologs in land plants and fungi. Solid blue arrows indicate the HGT of the UPF0261-domain-containing gene. Two solid red arrows indicate the HGT of the TBST-domain-containing gene from prokaryotes to plants and fungi, respectively. Dashed red arrows indicate the HGT of the TBST-domain-containing gene between plants and fungi. (B) Evolutionary history of the green plant Tm-1L gene.