Evidence for lateral gene transfer (LGT) in the evolution of eubacteria-derived small GTPases in plant organelles.

I Nengah Suwastika,Jeong Dong Bahk,Saki Yomogihara,Woo Young Bang,Takashi Shiina,Chak Han Im,Masatsugu Denawa,Ryosuke L Ohniwa,Kunio Takeyasu

doi:10.3389/fpls.2014.00678

Abstract

The genomes of free-living bacteria frequently exchange genes via lateral gene transfer (LGT), which has played a major role in bacterial evolution. LGT also played a significant role in the acquisition of genes from non-cyanobacterial bacteria to the lineage of “primary” algae and land plants. Small GTPases are widely distributed among prokaryotes and eukaryotes. In this study, we inferred the evolutionary history of organelle-targeted small GTPases in plants. Arabidopsis thaliana contains at least one ortholog in seven subfamilies of OBG-HflX-like and TrmE-Era-EngA-YihA-Septin-like GTPase superfamilies (together referred to as Era-like GTPases). Subcellular localization analysis of all Era-like GTPases in Arabidopsis revealed that all 30 eubacteria-related GTPases are localized to chloroplasts and/or mitochondria, whereas archaea-related DRG and NOG1 are localized to the cytoplasm and nucleus, respectively, suggesting that chloroplast- and mitochondrion-localized GTPases are derived from the ancestral cyanobacterium and α-proteobacterium, respectively, through endosymbiotic gene transfer (EGT). However, phylogenetic analyses revealed that plant organelle GTPase evolution is rather complex. Among the eubacterium-related GTPases, only four localized to chloroplasts (including one dual targeting GTPase) and two localized to mitochondria were derived from cyanobacteria and α-proteobacteria, respectively. Three other chloroplast-targeted GTPases were related to α-proteobacterial proteins, rather than to cyanobacterial GTPases. Furthermore, we found that four other GTPases showed neither cyanobacterial nor α-proteobacterial affiliation. Instead, these GTPases were closely related to clades from other eubacteria, such as Bacteroides (Era1, EngB-1, and EngB-2) and green non-sulfur bacteria (HflX). This study thus provides novel evidence that LGT significantly contributed to the evolution of organelle-targeted Era-like GTPases in plants.

Highlights

Plant cells contain two types of endosymbiotic organelle, chloroplasts and mitochondria, which arose from cyanobacterium and α-proteobacterium-like ancestors, respectively
We found that all 13 eubacteria-related GTPases were localized to chloroplasts and/or mitochondria in Arabidopsis, whereas archaea-related DRG and NOG1 were localized to the cytoplasm and nuclei, respectively
Four Era-like GTPases were closely related to clades from other eubacteria, such as Bacteroides (Era1, EngB-1, and EngB-2) and green non-sulfur bacteria (HflX). These results suggest that Lateral gene transfer (LGT) from Bacteroides and green non-sulfur bacteria has played a significant role in the evolution of genes for chloroplast- and mitochondria-target GTPases in land plants

Summary

Introduction

Plant cells contain two types of endosymbiotic organelle, chloroplasts and mitochondria, which arose from cyanobacterium and α-proteobacterium-like ancestors, respectively. Several lines of evidence suggest that there were ancient gene transfers from non-cyanobacterial bacteria to the lineage of “primary” algae and land plants. At least 55 Chlamydiae-derived genes have been identified in algae and plants, most of which are predominantly involved in plastid functions (Moustafa et al, 2008), suggesting an ancient LGT from Chlamydiae to the ancestor of primary photosynthetic eukaryotes (Huang and Gogarten, 2007; Becker et al, 2008; Moustafa et al, 2008; Ball et al, 2013).

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Conclusion