Biology

Document Type

Article

Abstract

Background. Glutamine synthetase (GS) is essential for ammonium assimilation and the biosynthesis of glutamine. The three GS gene families (GSI, GSII, and GSIII) are represented in both prokaryotic and eukaryotic organisms. In this study, we examined the evolutionary relationship of GSII from eubacterial and eukaryotic lineages and present robust phylogenetic evidence that GSII was transferred from -Proteobacteria (Eubacteria) to the Chloroplastida. Results. GSII sequences were isolated from four species of green algae (Trebouxiophyceae), and additional green algal (Chlorophyceae and Prasinophytae) and streptophyte (Charales, Desmidiales, Bryophyta, Marchantiophyta, Lycopodiophyta and Tracheophyta) sequences were obtained from public databases. In Bayesian and maximum likelihood analyses, eubacterial (GSIIB) and eukaryotic (GSIIE) GSII sequences formed distinct clades. Both GSIIBand GSIIEwere found in chlorophytes and early-diverging streptophytes. The GSIIBenzymes from these groups formed a well-supported sister clade with the -Proteobacteria, providing evidence that GSIIBin the Chloroplastida arose by horizontal gene transfer (HGT). Bayesian relaxed molecular clock analyses suggest that GSIIBand GSIIE coexisted for an extended period of time but it is unclear whether the proposed HGT happened prior to or after the divergence of the primary endosymbiotic lineages (the Archaeplastida). However, GSIIBgenes have not been identified in glaucophytes or red algae, favoring the hypothesis that GSIIBwas gained after the divergence of the primary endosymbiotic lineages. Duplicate copies of the GSIIBgene were present in Chlamydomonas reinhardtii, Volvox carteri f. nagariensis, and Physcomitrella patens. Both GSIIBproteins in C. reinhardtii and V. carteri f. nagariensis had N-terminal transit sequences, indicating they are targeted to the chloroplast or mitochondrion. In contrast, GSIIBproteins of P. patens lacked transit sequences, suggesting a cytosolic function. GSIIBsequences were absent in vascular plants where the duplication of GSIIEreplaced the function of GSII B. Conclusions. Phylogenetic evidence suggests GSIIBin Chloroplastida evolved by HGT, possibly after the divergence of the primary endosymbiotic lineages. Thus while multiple GS isoenzymes are common among members of the Chloroplastida, the isoenzymes may have evolved via different evolutionary processes. The acquisition of essential enzymes by HGT may provide rapid changes in biochemical capacity and therefore be favored by natural selection. © 2010 Ghoshroy et al; licensee BioMed Central Ltd.

Publication Title

BMC Evolutionary Biology

Publication Date

7-13-2010

Volume

10

Issue

1

DOI

10.1186/1471-2148-10-198

Creative Commons License

Creative Commons Attribution 3.0 License
This work is licensed under a Creative Commons Attribution 3.0 License.

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