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Plant Molecular Biology

, Volume 99, Issue 1–2, pp 123–134 | Cite as

Characterization of the O-acetylserine(thiol)lyase gene family in Solanum lycopersicum L.

  • Danmei Liu
  • Juanjuan Lu
  • Hui Li
  • Juanjuan Wang
  • Yanxi PeiEmail author
Article
  • 473 Downloads

Abstract

Key message

This research demonstrated the conservation and diversification of the functions of the O-acetylserine-(thiol) lyase gene family genes in Solanum lycopersicum L.

Abstract

Cysteine is the first sulfur-containing organic molecule generated by plants and is the precursor of many important biomolecules and defense compounds. Cysteine and its derivatives are also essential in various redox signaling-related processes. O-acetylserine(thiol)lyase (OASTL) proteins catalyze the last step of cysteine biosynthesis. Previously, researches focused mainly on OASTL proteins which were the most abundant or possessed the authentic OASTL activity, whereas few studies have ever given a comprehensive view of the functions of all the OASTL members in one specific species. Here, we characterized 8 genes belonging to the OASTL gene family from tomato genome (SlOAS2 to SlOAS9), including the sequence analyses, subcellular localization, enzymatic activity assays, expression patterns, as well as the interaction property with SATs. Apart from SlOAS3, all the other genes encoded OASTL-like proteins. Tomato OASTLs were differentially expressed during the development of tomato plants, and their encoded proteins had diverse compartmental distributions and functions. SlOAS5 and SlOAS6 catalyzed the biogenesis of cysteine in chloroplasts and in the cytosol, respectively, and this was in consistent with their interaction abilities with SlSATs. SlOAS4 catalyzed the generation of hydrogen sulfide, similar to its Arabidopsis ortholog, DES1. SlOAS2 also functioned as an L-cysteine desulfhydrase, but its expression pattern was very different from that of SlOAS4. Additionally, SlOAS8 might be a β-cyanoalanine synthase in mitochondria, and the S-sulfocysteine synthase activity appeared lost in tomato plants. SlOAS7 exhibited a transactivational ability in yeast; while the subcellular localization of SlOAS9 was in the peroxisome and correlated with the process of leaf senescence, indicating that these two genes might have novel roles.

Keywords

Tomato OASTL SAT Enzymatic activity Subcellular localization Expression pattern 

Notes

Acknowledgements

This work is funded by the National Natural Science Foundation of China (31501772) and Shanxi Province Science Foundation for Youths (201601D021097). We thank Dr. Yongfu Fu for tomato seeds of cv. MicroTom and the vector pGWB555. We thank Drs. Lifang Niu, Zhengrui Qin and Liyu Huang for providing the subcellular localization vectors. We thank International Science Editing (http://www.internationalscienceediting.com) for editing this manuscript.

Author contribution

DL and YP conceived the project and designed experiments; DL, JL, HL, JW performed experiments; DL and YP analysed experiment data and wrote the manuscript.

Supplementary material

11103_2018_807_MOESM1_ESM.pdf (838 kb)
Supplementary material 1 (PDF 837 KB)

References

  1. Alvarez C, Calo L, Romero LC, Garcia I, Gotor C (2010) An O-acetylserine(thiol)lyase homolog with l-cysteine desulfhydrase activity regulates cysteine homeostasis in Arabidopsis. Plant Physiol 152:656–669CrossRefPubMedPubMedCentralGoogle Scholar
  2. Alvarez C, Bermudez MA, Romero LC, Gotor C, Garcia I (2012) Cysteine homeostasis plays an essential role in plant immunity. New Phytol 193:165–177CrossRefPubMedGoogle Scholar
  3. Barroso C, Vega JM, Gotor C (1995) A new member of the cytosolic O-acetylserine(thiol)lyase gene family in Arabidopsis thaliana. FEBS Lett 363:1–5CrossRefPubMedGoogle Scholar
  4. Bermudez MA, Paez-Ochoa MA, Gotor C, Romero LC (2010) Arabidopsis S-sulfocysteine synthase activity is essential for chloroplast function and long-day light-dependent redox control. Plant Cell 22:403–416CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bermudez MA, Galmes J, Moreno I, Mullineaux PM, Gotor C, Romero LC (2012) Photosynthetic adaptation to length of day is dependent on S-sulfocysteine synthase activity in the thylakoid lumen. Plant Physiol 160:274–288CrossRefPubMedPubMedCentralGoogle Scholar
  6. Birke H, Haas FH, De Kok LJ, Balk J, Wirtz M, Hell R (2012) Cysteine biosynthesis, in concert with a novel mechanism, contributes to sulfide detoxification in mitochondria of Arabidopsis thaliana. Biochem J 445:275–283CrossRefPubMedGoogle Scholar
  7. Birke H, Heeg C, Wirtz M, Hell R (2013) Successful fertilization requires the presence of at least one major O-acetylserine(thiol)lyase for cysteine synthesis in pollen of Arabidopsis. Plant Physiol 163:959–972CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bonner ER, Cahoon RE, Knapke SM, Jez JM (2005) Molecular basis of cysteine biosynthesis in plants: structural and functional analysis of O-acetylserine sulfhydrylase from Arabidopsis thaliana. J Biol Chem 280:38803–38813CrossRefPubMedGoogle Scholar
  9. Campanini B, Benoni R, Bettati S, Beck CM, Hayes CS, Mozzarelli A (2015) Moonlighting O-acetylserine sulfhydrylase: new functions for an old protein. Biochim Biophys Acta 1854:1184–1193CrossRefPubMedPubMedCentralGoogle Scholar
  10. Chattopadhyay A et al (2007) Structure, mechanism, and conformational dynamics of O-acetylserine sulfhydrylase from Salmonella typhimurium: comparison of A and B isozymes. Biochemistry 46:8315–8330CrossRefPubMedGoogle Scholar
  11. Droux M, Ruffet ML, Douce R, Job D (1998) Interactions between serine acetyltransferase and O-acetylserine (thiol) lyase in higher plants–structural and kinetic properties of the free and bound enzymes. Eur J Biochem 255:235–245CrossRefPubMedGoogle Scholar
  12. Exposito-Rodriguez M, Borges AA, Borges-Perez A, Perez JA (2008) Selection of internal control genes for quantitative real-time RT-PCR studies during tomato development process. BMC Plant Biol 8:131CrossRefPubMedPubMedCentralGoogle Scholar
  13. Feldman-Salit A, Wirtz M, Hell R, Wade RC (2009) A mechanistic model of the cysteine synthase complex. J Mol Biol 386:37–59CrossRefPubMedGoogle Scholar
  14. Heeg C, Kruse C, Jost R, Gutensohn M, Ruppert T, Wirtz M, Hell R (2008) Analysis of the Arabidopsis O-acetylserine(thiol)lyase gene family demonstrates compartment-specific differences in the regulation of cysteine synthesis. Plant Cell 20:168–185CrossRefPubMedPubMedCentralGoogle Scholar
  15. Hell R, Bork C, Bogdanova N, Frolov I, Hauschild R (1994) Isolation and characterization of two cDNAs encoding for compartment specific isoforms of O-acetylserine (thiol) lyase from Arabidopsis thaliana. FEBS Lett 351:257–262CrossRefPubMedGoogle Scholar
  16. Hesse H, Lipke J, Altmann T, Hofgen R (1999) Molecular cloning and expression analyses of mitochondrial and plastidic isoforms of cysteine synthase (O-acetylserine(thiol)lyase) from Arabidopsis thaliana. Amino Acids 16:113–131CrossRefPubMedGoogle Scholar
  17. Howarth JR, Dominguez-Solis JR, Gutierrez-Alcala G, Wray JL, Romero LC, Gotor C (2003) The serine acetyltransferase gene family in Arabidopsis thaliana and the regulation of its expression by cadmium. Plant Mol Biol 51:589–598CrossRefPubMedGoogle Scholar
  18. Jin ZP et al (2017) Hydrogen sulfide mediates ion fluxes inducing stomatal closure in response to drought stress in Arabidopsis thaliana. Plant Soil 419:141–152CrossRefGoogle Scholar
  19. Jost R, Berkowitz O, Wirtz M, Hopkins L, Hawkesford MJ, Hell R (2000) Genomic and functional characterization of the oas gene family encoding O-acetylserine (thiol) lyases, enzymes catalyzing the final step in cysteine biosynthesis in Arabidopsis thaliana. Gene 253:237–247CrossRefPubMedGoogle Scholar
  20. Khare R, Kumar S, Shukla T, Ranjan A, Trivedi PK (2017) Differential sulphur assimilation mechanism regulates response of Arabidopsis thaliana natural variation towards arsenic stress under limiting sulphur condition. J Hazard Mater 337:198–207CrossRefPubMedGoogle Scholar
  21. Koprivova A, Kopriva S (2016) Hormonal control of sulfate uptake and assimilation. Plant Mol Biol 91:617–627CrossRefPubMedGoogle Scholar
  22. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRefGoogle Scholar
  23. Lai KW, Yau CP, Tse YC, Jiang L, Yip WK (2009) Heterologous expression analyses of rice OsCAS in Arabidopsis and in yeast provide evidence for its roles in cyanide detoxification rather than in cysteine synthesis in vivo. J Exp Bot 60:993–1008CrossRefPubMedPubMedCentralGoogle Scholar
  24. Lee J, Lee H, Kim J, Lee S, Kim DH, Kim S, Hwang I (2011) Both the hydrophobicity and a positively charged region flanking the C-terminal region of the transmembrane domain of signal-anchored proteins play critical roles in determining their targeting specificity to the endoplasmic reticulum or endosymbiotic organelles in Arabidopsis cells. Plant Cell 23:1588–1607CrossRefPubMedPubMedCentralGoogle Scholar
  25. Liu D et al (2014) The SEPALLATA MADS-box protein SLMBP21 forms protein complexes with JOINTLESS and MACROCALYX as a transcription activator for development of the tomato flower abscission zone. Plant J 77:284–296CrossRefPubMedGoogle Scholar
  26. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25:402–408CrossRefGoogle Scholar
  27. Lopez-Martin MC, Becana M, Romero LC, Gotor C (2008) Knocking out cytosolic cysteine synthesis compromises the antioxidant capacity of the cytosol to maintain discrete concentrations of hydrogen peroxide in Arabidopsis. Plant Physiol 147:562–572CrossRefPubMedPubMedCentralGoogle Scholar
  28. Marino SM, Gladyshev VN (2010) Cysteine function governs its conservation and degeneration and restricts its utilization on protein surfaces. J Mol Biol 404:902–916CrossRefPubMedPubMedCentralGoogle Scholar
  29. Nelson BK, Cai X, Nebenfuhr A (2007) A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J 51:1126–1136CrossRefPubMedGoogle Scholar
  30. Palmer E, Freeman T (2004) Investigation into the use of C- and N-terminal GFP fusion proteins for subcellular localization studies using reverse transfection microarrays. Comp Funct Genom 5:342–353CrossRefGoogle Scholar
  31. Rabeh WM, Cook PF (2004) Structure and mechanism of O-acetylserine sulfhydrylase. J Biol Chem 279:26803–26806CrossRefPubMedGoogle Scholar
  32. Riemenschneider A, Nikiforova V, Hoefgen R, De Kok LJ, Papenbrock J (2005a) Impact of elevated H(2)S on metabolite levels, activity of enzymes and expression of genes involved in cysteine metabolism. Plant Physiol Biochem 43:473–483CrossRefPubMedGoogle Scholar
  33. Riemenschneider A, Riedel K, Hoefgen R, Papenbrock J, Hesse H (2005b) Impact of reduced O-acetylserine(thiol)lyase isoform contents on potato plant metabolism. Plant Physiol 137:892–900CrossRefPubMedPubMedCentralGoogle Scholar
  34. Romero LC, Aroca MA, Laureano-Marin AM, Moreno I, Garcia I, Gotor C (2014) Cysteine and cysteine-related signaling pathways in Arabidopsis thaliana. Molecular plant 7:264–276CrossRefPubMedGoogle Scholar
  35. Singh VK, Mangalam AK, Dwivedi S, Naik S (1998) Primer premier: program for design of degenerate primers from a protein sequence. Biotechniques 24:318–319CrossRefPubMedGoogle Scholar
  36. Spiegelhauer O, Mende S, Dickert F, Knauer SH, Ullmann GM, Dobbek H (2010) Cysteine as a modulator residue in the active site of xenobiotic reductase A: a structural, thermodynamic and kinetic study. J Mol Biol 398:66–82CrossRefPubMedGoogle Scholar
  37. Thompson JD, Gibson TJ, Higgins DG (2002) Multiple sequence alignment using ClustalW and ClustalX. Curr Protocols Bioinform 2:3Google Scholar
  38. Wang P, Richardson C, Hawes C, Hussey PJ (2016) Arabidopsis NAP1 regulates the formation of autophagosomes. Curr Biol 26:2060–2069CrossRefPubMedGoogle Scholar
  39. Wirtz M, Hell R (2006) Functional analysis of the cysteine synthase protein complex from plants: structural, biochemical and regulatory properties. J Plant Physiol 163:273–286CrossRefPubMedGoogle Scholar
  40. Wirtz M, Droux M, Hell R (2004) O-acetylserine (thiol) lyase: an enigmatic enzyme of plant cysteine biosynthesis revisited in Arabidopsis thaliana. J Exp Bot 55:1785–1798CrossRefPubMedGoogle Scholar
  41. Xiao C, Chen F, Yu X, Lin C, Fu YF (2009) Over-expression of an AT-hook gene, AHL22, delays flowering and inhibits the elongation of the hypocotyl in Arabidopsis thaliana. Plant Mol Biol 71:39–50CrossRefPubMedGoogle Scholar
  42. Xu M, Marsh HM, Sevier CS (2016) A conserved cysteine within the ATPase domain of the endoplasmic reticulum chaperone BiP is necessary for a complete complement of BiP activities. J Mol Biol 428:4168–4184CrossRefPubMedPubMedCentralGoogle Scholar
  43. Yamaguchi Y, Nakamura T, Kusano T, Sano H (2000) Three Arabidopsis genes encoding proteins with differential activities for cysteine synthase and beta-cyanoalanine synthase. Plant Cell Physiol 41:465–476CrossRefPubMedGoogle Scholar
  44. Youssefian S, Nakamura M, Sano H (1993) Tobacco plants transformed with the O-acetylserine (thiol) lyase gene of wheat are resistant to toxic levels of hydrogen sulphide gas. Plant J 4:759–769CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.College of Life ScienceShanxi UniversityTaiyuanChina
  2. 2.Scientific Instrument CenterShanxi UniversityTaiyuanChina

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