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Bohrer AS, Yoshimoto N, Sekiguchi A, et al. Alternative translational initiation of ATP sulfurylase underlying dual localization of sulfate assimilation pathways in plastids and cytosol in Arabidopsis thaliana. Front Plant Sci. 2015;5:750doi: 10.3389/fpls.2014.00750.
Bohrer, A. S., Yoshimoto, N., Sekiguchi, A., Rykulski, N., Saito, K., & Takahashi, H. (2014). Alternative translational initiation of ATP sulfurylase underlying dual localization of sulfate assimilation pathways in plastids and cytosol in Arabidopsis thaliana. Frontiers in plant science, 5750. https://doi.org/10.3389/fpls.2014.00750
Bohrer, Anne-Sophie, et al. "Alternative translational initiation of ATP sulfurylase underlying dual localization of sulfate assimilation pathways in plastids and cytosol in Arabidopsis thaliana." Frontiers in plant science vol. 5 (2014): 750. doi: https://doi.org/10.3389/fpls.2014.00750
Bohrer AS, Yoshimoto N, Sekiguchi A, Rykulski N, Saito K, Takahashi H. Alternative translational initiation of ATP sulfurylase underlying dual localization of sulfate assimilation pathways in plastids and cytosol in Arabidopsis thaliana. Front Plant Sci. 2015 Jan 05;5:750. doi: 10.3389/fpls.2014.00750. eCollection 2014. PMID: 25601874; PMCID: PMC4283515.
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Front Plant Sci. 2015 Jan 05;5:750. doi: 10.3389/fpls.2014.00750. eCollection 2014.

Alternative translational initiation of ATP sulfurylase underlying dual localization of sulfate assimilation pathways in plastids and cytosol in Arabidopsis thaliana.

Frontiers in plant science

Anne-Sophie Bohrer, Naoko Yoshimoto, Ai Sekiguchi, Nicholas Rykulski, Kazuki Saito, Hideki Takahashi

Affiliations

  1. Department of Biochemistry and Molecular Biology, Michigan State University East Lansing, MI, USA.
  2. Graduate School of Pharmaceutical Sciences, Chiba University Chiba, Japan.
  3. Graduate School of Pharmaceutical Sciences, Chiba University Chiba, Japan ; RIKEN Center for Sustainable Resource Science Yokohama, Japan.

PMID: 25601874 PMCID: PMC4283515 DOI: 10.3389/fpls.2014.00750

Abstract

Plants assimilate inorganic sulfate into sulfur-containing vital metabolites. ATP sulfurylase (ATPS) is the enzyme catalyzing the key entry step of the sulfate assimilation pathway in both plastids and cytosol in plants. Arabidopsis thaliana has four ATPS genes (ATPS1, -2, -3, and -4) encoding ATPS pre-proteins containing N-terminal transit peptide sequences for plastid targeting, however, the genetic identity of the cytosolic ATPS has remained unverified. Here we show that Arabidopsis ATPS2 dually encodes plastidic and cytosolic ATPS isoforms, differentiating their subcellular localizations by initiating translation at AUG(Met1) to produce plastid-targeted ATPS2 pre-proteins or at AUG(Met52) or AUG(Met58) within the transit peptide to have ATPS2 stay in cytosol. Translational initiation of ATPS2 at AUG(Met52) or AUG(Met58) was verified by expressing a tandem-fused synthetic gene, ATPS2 (5'UTR-His12) :Renilla luciferase:ATPS2 (Ile13-Val77) :firefly luciferase, under a single constitutively active CaMV 35S promoter in Arabidopsis protoplasts and examining the activities of two different luciferases translated in-frame with split N-terminal portions of ATPS2. Introducing missense mutations at AUG(Met52) and AUG(Met58) significantly reduced the firefly luciferase activity, while AUG(Met52) was a relatively preferred site for the alternative translational initiation. The activity of luciferase fusion protein starting at AUG(Met52) or AUG(Met58) was not modulated by changes in sulfate conditions. The dual localizations of ATPS2 in plastids and cytosol were further evidenced by expression of ATPS2-GFP fusion proteins in Arabidopsis protoplasts and transgenic lines, while they were also under control of tissue-specific ATPS2 promoter activity found predominantly in leaf epidermal cells, guard cells, vascular tissues and roots.

Keywords: ATP sulfurylase; Arabidopsis; alternative translational initiation; dual localization; sulfur metabolism

References

  1. Plant Cell. 2012 Oct;24(10):4187-204 - PubMed
  2. Arch Biochem Biophys. 2006 Jun 1;450(1):20-9 - PubMed
  3. Gene. 2000 May 2;248(1-2):51-8 - PubMed
  4. Plant J. 2000 Dec;24(5):583-9 - PubMed
  5. Nat Protoc. 2007;2(7):1565-72 - PubMed
  6. Plant Physiol. 1990 Nov;94(3):1345-52 - PubMed
  7. Plant J. 2014 May;78(4):659-73 - PubMed
  8. Plant Physiol. 1995 Feb;107(2):653-4 - PubMed
  9. Proc Natl Acad Sci U S A. 1996 Nov 12;93(23):13383-8 - PubMed
  10. Plant J. 1998 Dec;16(6):735-43 - PubMed
  11. Plant Physiol. 2014 May;165(1):52-61 - PubMed
  12. Plant Mol Biol. 1997 Dec;35(6):993-1001 - PubMed
  13. Plant Physiol. 2001 Dec;127(4):1750-63 - PubMed
  14. Plant Cell Environ. 2012 Feb;35(2):454-84 - PubMed
  15. Plant J. 1994 Jul;6(1):105-12 - PubMed
  16. Proc Natl Acad Sci U S A. 1996 Nov 12;93(23):13377-82 - PubMed
  17. Arch Biochem Biophys. 2001 Aug 15;392(2):303-10 - PubMed
  18. Arch Biochem Biophys. 1993 Dec;307(2):272-85 - PubMed
  19. Plant Physiol. 1994 Jul;105(3):897-902 - PubMed
  20. Curr Biol. 1996 Mar 1;6(3):325-30 - PubMed
  21. Biochem Biophys Res Commun. 1998 Jun 9;247(1):171-5 - PubMed
  22. Arch Biochem Biophys. 1995 Oct 20;323(1):195-204 - PubMed
  23. Plant J. 2005 Mar;41(5):722-31 - PubMed
  24. J Biol Chem. 1996 May 24;271(21):12227-33 - PubMed
  25. Prog Lipid Res. 2011 Jul;50(3):234-9 - PubMed
  26. Annu Rev Plant Biol. 2011;62:157-84 - PubMed
  27. J Biol Chem. 2000 Jan 14;275(2):930-6 - PubMed
  28. Plant J. 2013 Nov;76(3):481-93 - PubMed
  29. Plant Cell. 2009 Jan;21(1):157-67 - PubMed
  30. Nucleic Acids Res. 1988 Oct 25;16(20):9877 - PubMed
  31. Plant Physiol. 2000 Oct;124(2):715-24 - PubMed
  32. EMBO J. 2002 Jun 3;21(11):2692-702 - PubMed
  33. Plant J. 2009 Jan;57(2):313-21 - PubMed
  34. Anal Biochem. 1976 May 7;72:248-54 - PubMed
  35. Plant J. 2011 Jun;66(5):863-76 - PubMed
  36. Annu Rev Plant Biol. 2006;57:303-33 - PubMed
  37. Proc Natl Acad Sci U S A. 2008 Apr 22;105(16):6196-201 - PubMed
  38. Proc Natl Acad Sci U S A. 1988 Aug;85(15):5536-40 - PubMed
  39. Plant Cell. 2009 Mar;21(3):910-27 - PubMed

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