Journal of Plant Research

, Volume 130, Issue 4, pp 625–634 | Cite as

Phylogenetic analysis of proteins involved in the stringent response in plant cells

  • Doshun Ito
  • Yuta Ihara
  • Hidenori Nishihara
  • Shinji Masuda
Regular Paper

Abstract

The nucleotide (p)ppGpp is a second messenger that controls the stringent response in bacteria. The stringent response modifies expression of a large number of genes and metabolic processes and allows bacteria to survive under fluctuating environmental conditions. Recent genome sequencing analyses have revealed that genes responsible for the stringent response are also found in plants. These include (p)ppGpp synthases and hydrolases, RelA/SpoT homologs (RSHs), and the pppGpp-specific phosphatase GppA/Ppx. However, phylogenetic relationship between enzymes involved in bacterial and plant stringent responses is as yet generally unclear. Here, we investigated the origin and evolution of genes involved in the stringent response in plants. Phylogenetic analysis and primary structures of RSH homologs from different plant phyla (including Embryophyta, Charophyta, Chlorophyta, Rhodophyta and Glaucophyta) indicate that RSH gene families were introduced into plant cells by at least two independent lateral gene transfers from the bacterial Deinococcus-Thermus phylum and an unidentified bacterial phylum; alternatively, they were introduced into a proto-plant cell by a lateral gene transfer from the endosymbiotic cyanobacterium followed by gene loss of an ancestral RSH gene in the cyanobacterial linage. Phylogenetic analysis of gppA/ppx families indicated that plant gppA/ppx homologs form an individual cluster in the phylogenetic tree, and show a sister relationship with some bacterial gppA/ppx homologs. Although RSHs contain a plastidial transit peptide at the N terminus, GppA/Ppx homologs do not, suggesting that plant GppA/Ppx homologs function in the cytosol. These results reveal that a proto-plant cell obtained genes for the stringent response by lateral gene transfer events from different bacterial phyla and have utilized them to control metabolism in plastids and the cytosol.

Keywords

Chloroplast GppA ppGpp pppGpp Ppx RelA/SpoT homolog 

Supplementary material

10265_2017_922_MOESM1_ESM.pdf (343 kb)
Supplementary material 1 (PDF 342 KB)
10265_2017_922_MOESM2_ESM.zip (110 kb)
Supplementary material 2 (ZIP 110 KB)

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Copyright information

© The Botanical Society of Japan and Springer Japan 2017

Authors and Affiliations

  • Doshun Ito
    • 1
  • Yuta Ihara
    • 1
  • Hidenori Nishihara
    • 1
  • Shinji Masuda
    • 2
    • 3
  1. 1.Graduate School of Bioscience and BiotechnologyTokyo Institute of TechnologyYokohamaJapan
  2. 2.Center for Biological Resources and InformaticsTokyo Institute of TechnologyYokohamaJapan
  3. 3.Earth-Life Science InstituteTokyo Institute of TechnologyTokyoJapan

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