Skip to main content
SpringerLink
Log in

Physiological importance and possible applications of β-substituted alanine synthase in plants

  • Review
  • Published:
Applied Biological Chemistry Submit manuscript

Abstract

Cysteine, as well as its precursors and derivatives, plays important roles in plant development and stress responses. In plants, a diverse range of reactions affecting cysteine content are catalyzed by the β-substituted alanine synthase (BSAS) enzyme family. Individual BSAS family members use similar reaction mechanisms involving pyridoxal phosphate cofactors and show catalytic preferences for biosynthesis, degradation, or modification of the cysteine amino acid. In Arabidopsis thaliana (Arabidopsis) of the Brassicaceae family, four distinct biochemical activities are characterized at the gene level, namely, O-acetylserine sulfhydrylase, β-cyanoalanine synthase, l-cysteine desulfhydrase, and S-sulfocysteine synthase activities. Reverse genetic approaches in Arabidopsis were used to elucidate the physiological roles of metabolites of cysteine metabolism (O-acetylserine, sulfide, cysteine, cyanide, and S-sulfocysteine) during the processes of root hair development, pollen tube germination, heavy metal tolerance, defense responses, stomatal closure, and autophagy. Key catalytic residues determining reaction specificities in different BSAS enzymes are being identified, along with the roles of macromolecular complexes involving BSAS. The biochemical properties of BSAS active sites are being investigated in various organisms, including plants, for possible application to the development of new biological materials and drugs. Systematic and comparative genomic studies of BSAS enzymes in Brassica plants, close relatives of Arabidopsis, requiring high cysteine production for optimum growth and disease resistance, will be useful for the future study of the diversification of BSAS and the biotechnological improvement of these important crop plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Álvarez C, Calo L, Romero LC, García I, Gotor C (2010) An O-acetylserine(thiol)lyase homolog with l-cysteine desulfhydrase activity regulates cysteine homeostasis in Arabidopsis. Plant Physiol 152:656–669

    Article  CAS  Google Scholar 

  • Álvarez C, Lozano-Juste J, Romero LC, García I, Gotor C, León J (2011) Inhibition of Arabidopsis O-acetylserine(thiol)lyase A1 by tyrosine nitration. J Biol Chem 286:578–586

    Article  CAS  Google Scholar 

  • Álvarez C, Bermúdez MÁ, Romero LC, Gotor C, García I (2012a) Cysteine homeostasis plays an essential role in plant immunity. New Phytol 193:165–177

    Article  CAS  Google Scholar 

  • Álvarez C, García I, Moreno I, Perez-Perez ME, Crespo JL, Romero LC, Gotor C (2012b) Cysteine-generated sulfide in the cytosol negatively regulates autophagy and modulates the transcriptional profile in Arabidopsis. Plant Cell 24:4621–4634

    Article  CAS  Google Scholar 

  • Álvarez C, García I, Romero LC, Gotor C (2012c) Mitochondrial sulfide detoxification requires a functional isoform O-acetylserine(thiol)lyase C in Arabidopsis thaliana. Mol Plant 5:1217–1226

    Article  CAS  Google Scholar 

  • Amtmann A, Armengaud P (2009) Effects of N, P, K, and S on metabolism. New knowledge gained from multi-level analysis. Curr Opin Plant Biol 12:275–283

    Article  CAS  Google Scholar 

  • Axup JY, Bajjuri KM, Ritland M, Hutchins BM, Kim CH, Kazane SA, Halder R, Forsyth JS, Santidrian AF, Stafin K, Lu Y, Tran H, Seller AJ, Biroc SL, SzydlikA Pinkstaff JK, Tian F, Sinha SC, Felding-Habermann B, Smider VV, Schultz PG (2012) Synthesis of site-specific antibody-drug conjugates using unnatural amino acids. Proc Natl Acad Sci USA 109:16101–16106

    Article  CAS  Google Scholar 

  • Bannai H, Tamada Y, Maruyama O, Nakai K, Miyano S (2002) Extensive feature detection of N-terminal protein sorting signals. Bioinformatics 18:298–305

    Article  CAS  Google Scholar 

  • Barroso C, Vega JM, Gotor C (1995) A new member of the cytosolic O-acetylserine(thiol)lyase gene family in Arabidopsis thaliana. FEBS Lett 363:1–5

    Article  CAS  Google Scholar 

  • Barroso C, Romero LC, Cejudo FJ, Vega JM, Gotor C (1999) Saltspecific regulation of the cytosolic O-acetylserine(thiol)lyase gene from Arabidopsis thaliana is dependent on abscisic acid. Plant Mol Biol 40:729–736

    Article  CAS  Google Scholar 

  • Bednarek P (2012) Sulfur-containing secondary metabolites from Arabidopsis thaliana and other Brassicaceae with function in plant immunity. ChemBioChem 13:1846–1859

    Article  CAS  Google Scholar 

  • Berkowitz O, Wirtz M, Wolf A, Kuhlmann J, Hell R (2002) Use of biomolecular interaction analysis to elucidate the regulatory mechanism of the cysteine synthase complex from Arabidopsis thaliana. J Biol Chem 277:30629–30634

    Article  CAS  Google Scholar 

  • Bermúdez MA, Páez-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 22:403–416

    Article  Google Scholar 

  • Bermúdez MÁ, Galmés 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 160:274–288

    Article  CAS  Google Scholar 

  • Bhave DP, Muse WB 3rd, Carroll KS (2007) Drug targets in mycobacterial sulfur metabolism. Infect Disord Drug Targets 7:140–158

    Article  CAS  Google Scholar 

  • Birke H, Haas FH, De Kok LJ, Balk J, Wirtz M, Hell R (2012a) Cysteine biosynthesis, in concert with a novel mechanism, contributes to sulfide detoxification in mitochondria of Arabidopsis thaliana. Biochem J 445:275–283

    Article  CAS  Google Scholar 

  • Birke H, Müller SJ, Rother M, Zimmer AD, Hoernstein SN, Wesenberg D, Wirtz M, Krauss GJ, Reski R, Hell R (2012b) The relevance of compartmentation for cysteine synthesis in phototrophic organisms. Protoplasma 249(Suppl 2):S147–S155

    Article  CAS  Google Scholar 

  • 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 163:959–972

    Article  CAS  Google Scholar 

  • Birke H, De Kok LJ, Wirtz M, Hell R (2015) The role of compartment-specific cysteine synthesis for sulfur homeostasis during H2S exposure in Arabidopsis. Plant Cell Physiol 56:358–367

    Article  Google Scholar 

  • Bloem E, Riemenschneider A, Volker J, Papenbrock J, Schmidt A, Salac I, Haneklaus S, Schnug E (2004) Sulphur supply and infection with Pyrenopeziza brassicae influence l-cysteine desulphydrase activity in Brassica napus L. J Exp Bot 55:2305–2312

    Article  CAS  Google Scholar 

  • Bloem E, Haneklaus S, Schnug E (2015) Milestones in plant sulfur research on sulfur-induced-resistance (SIR) in Europe. Front Plant Sci 5:779

    Article  Google Scholar 

  • Bogdanova N, Hell R (1997) Cysteine synthesis in plants: protein–protein interactions of serine acetyltransferase from Arabidopsis thaliana. Plant J 11:251–262

    Article  CAS  Google Scholar 

  • 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 280:38803–38813

    Article  CAS  Google Scholar 

  • Booth E, Walker KC, Schnug E (1991) The effect of site, foliar sulfur and nitrogen application on glucosinolate content and yield of oilseed rape. In: Proceedings of the international rapeseed congress in Saskatoon, vol 2, pp 567–572

  • Böttcher C, Westphal L, Schmotz C, Prade E, Scheel D, Glawischnig E (2009) The multifunctional enzyme CYP71B15 (PHYTOALEXIN DEFICIENT3) converts cysteine-indole-3-acetonitrile to camalexin in the indole-3-acetonitrile metabolic network of Arabidopsis thaliana. Plant Cell 21:1830–1845

    Article  CAS  Google Scholar 

  • Brunold C, Suter M (1982) Intracellular localization of serine acetyltransferase in spinach leaves. Planta 155:321–327

    Article  CAS  Google Scholar 

  • Brychkova G, Xia Z, Yang G, Yesbergenova Z, Zhang Z, Davydov O, Fluhr R, Sagi M (2007) Sulfite oxidase protects plants against sulfur dioxide toxicity. Plant J 50:696–709

    Article  CAS  Google Scholar 

  • Cahoon RE, Lutke WK, Cameron JC, Chen S, Lee SG, Rivard RS, Rea PA, Jez JM (2015) Adaptive engineering of phytochelatin-based heavy metal tolerance. J Biol Chem 290:17321–17330

    Article  CAS  Google Scholar 

  • Chalhoub B, Denoeud F, Liu S, Parkin IA, Tang H, Wang X, Chiquet J, Belcram H, Tong C, Samans B, Corréa M, Da Silva C, Just J, Falentin C, Koh CS, Le Clainche I, Bernard M, Bento P, Noel B, Labadie K, Alberti A, Charles M, Arnaud D, Guo H, Daviaud C, Alamery S, Jabbari K, Zhao M, Edger PP, Chelaifa H, Tack D, Lassalle G, Mestiri I, Schnel N, Le Paslier MC, Fan G, Renault V, Bayer PE, Golicz AA, Manoli S, Lee TH, Thi VH, Chalabi S, Hu Q, Fan C, Tollenaere R, Lu Y, Battail C, Shen J, Sidebottom CH, Wang X, Canaguier A, Chauveau A, Bérard A, Deniot G, Guan M, Liu Z, Sun F, Lim YP, Lyons E, Town CD, Bancroft I, Wang X, Meng J, Ma J, Pires JC, King GJ, Brunel D, Delourme R, Renard M, Aury JM, Adams KL, Batley J, Snowdon RJ, Tost J, Edwards D, Zhou Y, Hua W, Sharpe AG, Paterson AH, Guan C, Wincker P (2014) Plant genetics. Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science 345:950–953

    Article  CAS  Google Scholar 

  • Chivasa S, Carr JP (1998) Cyanide restores N gene-mediated resistance to tobacco mosaic virus in transgenic tobacco expressing salicylic acid hydroxylase. Plant Cell 10:1489–1498

    CAS  Google Scholar 

  • Chronis D, Krishnan HB (2003) Sulfur assimilation in soybean: molecular cloning and characterization of O-acetylserine(thiol)lyase (cysteine synthase). Crop Sci 43:1819–1827

    Article  CAS  Google Scholar 

  • Chronis D, Krishnan HB (2004) Sulfur assimilation in soybean (Glycine max [L.] Merr.): molecular cloning and characterization of a cytosolic isoform of serine acetyltransferase. Planta 218:417–426

    Article  CAS  Google Scholar 

  • Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182

    Article  CAS  Google Scholar 

  • Cooper CE, Brown GC (2008) The inhibition of mitochondrial cytochrome oxidase by the gases carbon monoxide, nitric oxide, hydrogen cyanide and hydrogen sulfide: chemical mechanism and physiological significance. J Bioenerg Biomembr 40:533–539

    Article  CAS  Google Scholar 

  • Domínguez-Solís JR, Gutierrez-Alcala G, Vega JM, Romero LC, Gotor C (2001) The cytosolic O-acetylserine(thiol)lyase gene is regulated by heavy metals and can function in cadmium tolerance. J Biol Chem 276:9297–9302

    Article  Google Scholar 

  • Droux M (2003) Plant serine acetyltransferase: new insights for regulation of sulphur metabolism in plant cells. Plant Physiol Biochem 41:619–627

    Article  CAS  Google Scholar 

  • Droux M, Martin J, Sajus P, Douce R (1992) Purification and characterization of O-acetylserine (thiol) lyase from spinach chloroplasts. Arch Biochem Biophys 295:379–390

    Article  CAS  Google Scholar 

  • 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 255:235–245

    Article  CAS  Google Scholar 

  • Emanuelsson O, Brunak S, von Hijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2:953–971

    Article  CAS  Google Scholar 

  • Feldman-Salit A, Wirtz M, Hell R, Wade RC (2009) A mechanistic model of the cysteine synthase complex. J Mol Biol 386:37–59

    Article  CAS  Google Scholar 

  • Francois JA, Kumaran S, Jez JM (2006) Structural basis for interaction of O-acetylserine sulfhydrylase and serine acetyltransferase in the Arabidopsis cysteine synthase complex. Plant Cell 18:3647–3655

    Article  CAS  Google Scholar 

  • Galant A, Preuss ML, Cameron JC, Jez JM (2011) Plant glutathione biosynthesis: diversity in biochemical regulation and reaction products. Front Plant Sci. 2:45

    Article  Google Scholar 

  • García I, Castellano JM, Vioque B, Solano R, Gotor C, Romero LC (2010) Mitochondrial β-cyanoalanine synthase is essential for root hair formation in Arabidopsis thaliana. Plant Cell 22:3268–3279

    Article  CAS  Google Scholar 

  • García I, Rosas T, Bejarano ER, Gotor C, Romero LC (2013) Transient transcriptional regulation of the CYS-C1 gene and cyanide accumulation upon pathogen infection in the plant immune response. Plant Physiol 162:2015–2027

    Article  CAS  Google Scholar 

  • García I, Gotor C, Romero LC (2014) Beyond toxicity: a regulatory role for mitochondrial cyanide. Plant Signal Behav 9:e27612

    Article  CAS  Google Scholar 

  • Gibbs DJ (2015) Emerging functions for N-terminal protein acetylation in plants. Trends Plant Sci 20:599–601

    Article  CAS  Google Scholar 

  • Gigolashvili T, Kopriva S (2014) Transporters in plant sulfur metabolism. Front Plant Sci 5:442

    Article  Google Scholar 

  • Gotor C, Romero LC (2013) S-sulfocysteine synthase function in sensing chloroplast redox status. Plant Signal Behav 8:e23313

    Article  Google Scholar 

  • Gutierrez-Marcos FJ, Roberts MA, Campbell EI, Wray JL (1996) Three members of a novel small gene-family from Arabidopsis thaliana able to complement functionally an Escherichia coli mutant defective in PAPS reductase activity encode proteins with a thioredoxin-like domain and “APS reductase” activity. Proc Natl Acad Sci USA 93:13377–13382

    Article  CAS  Google Scholar 

  • Haas FH, Heeg C, Queiroz R, Bauer A, Wirtz M, Hell R (2008) Mitochondrial serine acetyltransferase functions as a pacemaker of cysteine synthesis in plant cells. Plant Physiol 148:1055–1067

    Article  CAS  Google Scholar 

  • Han SE, Seo YS, Kim D, Sung SK, Kim WT (2007) Expression of MdCAS1 and MdCAS2, encoding apple beta-cyanoalanine synthase homologs, is concomitantly induced during ripening and implicates MdCASs in the possible role of the cyanide detoxification in Fuji apple (Malus domestica Borkh.) fruits. Plant Cell Rep 26:1321–1331

    Article  CAS  Google Scholar 

  • Haneklaus S, Walker KC, Schnug E (2005) A chronicle of sulfur research in agriculture. In: Saito K, De Kok LJ, Stulen I, Hawkesford MJ, Schnug E, Sirko A, Rennenberg H (eds) Sulfur transport and assimilation in plants in the post genome era. Backhys Publishers, Leidel, pp 249–256

    Google Scholar 

  • Haneklaus, S, Walker KC, Schnug E (2008) Hisory of sulfur deficiency in crops. In: Jez JM (ed) Sulfur: a missing bink between soils, crops, and nutrition. Agronomy Monograph 50. ASA, CSSA, and SSSA, Madison, pp 249–256

  • Hatzfeld Y, Maruyama A, Schmidt A, Noji M, Ishizawa K, Saito K (2000) β-Cyanoalanine synthase is a mitochondrial Cys synthase-like protein in spinach and Arabidopsis. Plant Physiol 123:1163–1172

    Article  CAS  Google Scholar 

  • 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 20:168–185

    Article  CAS  Google Scholar 

  • Hell R, Hillebrand H (2001) Plant concepts for mineral acquisition and allocation. Curr Opin Biotechnol 12:161–168

    Article  CAS  Google Scholar 

  • Hermsen C, Koprivova A, Matthewman C, Wesenberg D, Krauss GJ, Kopriva S (2010) Regulation of sulfate assimilation in Physcomitrella patens: mosses are different. Planta 232:461–470

    Article  CAS  Google Scholar 

  • Hesse H, Lipke J, Altmann T, Höfgen R (1999) Molecular cloning and expression analyses of mitochondrial and plastidic isoforms of cysteine synthase (O-acetylserine(thiol)lyase) from Arabidopsis thaliana. Amino Acids 16:113–131

    Article  CAS  Google Scholar 

  • Hirai MY, Fujiwara T, Awazuhara M, Kimura T, Noji M, Saito K (2003) Global expression profiling of sulfur-starved Arabidopsis by DNA macroarray reveals the role of O-acetyl-1-serine as a general regulator of gene expression in response to sulfur nutrition. Plant J 33:651–663

    Article  CAS  Google Scholar 

  • Hopkins L, Parmar S, Blaszczyk A, Hesse H, Hoefgen R, Hawkesford MJ (2005) O-acetylserine and the regulation of expression of genes encoding components for sulfate uptake and assimilation in potato. Plant Physiol 138:433–440

    Article  CAS  Google Scholar 

  • Huang B, Vetting MW, Roderick SL (2005) The active site of O-acetylserine sulfhydrylase is the anchor point for bienzyme complex formation with serine acetyltransferase. J Bacteriol 187:3201–3205

    Article  CAS  Google Scholar 

  • Hubberten HM, Klie S, Caldana C, Degenkolbe T, Willmitzer L, Hoefgen R (2012) Additional role of O-acetylserine as a sulfur status-independent regulator during plant growth. Plant J 70:666–677

    Article  CAS  Google Scholar 

  • Ikegami F, Murakoshi I (1994) Enzymatic synthesis of non-protein β-substituted alanines and some higher homologues in plants. Phytochemistry 35:1089–1104

    Article  CAS  Google Scholar 

  • Inoue K, Noji M, Saito K (1999) Determination of the sites required for the allosteric inhibition of serine acetyltransferase by l-cysteine in plants. Eur J Biochem 266:220–227

    Article  CAS  Google Scholar 

  • Jackson TL, Baker GW, Wilks FR Jr, Popov VA, Mathur Benfey PN (2015) Large cellular inclusions accumulate in Arabidopsis roots exposed to low-sulfur conditions. Plant Physiol 168:1573–1589

    Article  CAS  Google Scholar 

  • Jez JM, Fukagawa NK (2008) Plant sulfur compounds and human health. In: Jez JM (ed) Sulfur: a missing link between soils, crops, and nutrition. Agronomy Monograph 50. ASA, CSSA, and SSSA, Madison, pp 281–292

  • Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282

    CAS  Google Scholar 

  • 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 253:237–247

    Article  CAS  Google Scholar 

  • Kai Y, Kashiwagi T, Ishikawa K, Ziyatdinov MK, Redkina EI, Kiriukhin MY, Gusyatiner MM, Kobayashi S, Takagi H, Suzuki E (2006) Engineering of Escherichia coli l-serine O-acetyltransferase on the basis of crystal structure: desensitization to feedback inhibition by l-cysteine. Protein Eng Des Sel 19:163–167

    Article  CAS  Google Scholar 

  • Kawashima CG, Berkowitz O, Hell R, Noji M, Saito K (2005) Characterization and expression analysis of a serine acetyltransferase gene family involved in a key step of the sulfur assimilation pathway in Arabidopsis. Plant Physiol 137:220–230

    Article  CAS  Google Scholar 

  • Khan MS, Haas FH, Samami AA, Gholami AM, Bauer A, Fellenberg K, Reichelt M, Hänsch R, Mendel RR, Meyer AJ, Wirtz M, Hell R (2010) Sulfite reductase defines a newly discovered bottleneck for assimilatory sulfate reduction and is essential for growth and development in Arabidopsis thaliana. Plant Cell 22:1216–1231

    Article  CAS  Google Scholar 

  • Klikocka H, Haneklaus S, Bloem E, Schnug E (2005) Influence of sulfur fertilization on infection of potato tubers with Rhizoctonia solani and Streptomyces scabies. J Plant Nutr 28:819–833

    Article  CAS  Google Scholar 

  • Kopriva S (2015) Plant sulfur nutrition: from Sachs to Big Data. Plant Signal Behav 10:e1055436

    Google Scholar 

  • Kopriva S, Buchert T, Fritz G, Suter M, Weber M, Benda R, Schaller J, Feller U, Schurmann P, Schunemann V, Trautwein AX, Kroneck PM, Brunold C (2001) Plant adenosine 50-phosphosulfate reductase is a novel iron-sulfur protein. J Biol Chem 276:42881–42886

    Article  CAS  Google Scholar 

  • Kopriva S, Mugford SG, Baraniecka P, Lee BR, Matthewman CA, Koprivova A (2012) Control of sulfur partitioning between primary and secondary metabolism in Arabidopsis. Front Plant Sci. 3:163

    Article  Google Scholar 

  • Kredich NM, Becker MA, Tomkins GM (1969) Purification and characterization of cysteine synthetase, a bifunctional protein complex, from Salmonella typhimurium. J Biol Chem 244:2428–2439

    CAS  Google Scholar 

  • Krueger S, Niehl A, Lopez Martin MC, Steinhauser D, Donath A, Hildebrandt T, Romero LC, Höfgen R, Gotor C, Hesse H (2009) Analysis of cytosolic and plastidic serine acetyltransferase mutants and subcellular metabolite distributions suggests interplay of the cellular compartments for cysteine biosynthesis in Arabidopsis. Plant Cell Environ 32:349–367

    Article  CAS  Google Scholar 

  • Kumaran S, Jez JM (2007) Thermodynamics of the interaction between O-acetylserine sulfhydrylase and the C-terminus of serine acetyltransferase. Biochemistry 46:5586–5594

    Article  CAS  Google Scholar 

  • Kumaran S, Yi H, Krishnan HB, Jez JM (2009) Assembly of the cysteine synthase complex and the regulatory role of protein–protein interactions. J Biol Chem 284:10268–10275

    Article  CAS  Google Scholar 

  • 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 60:993–1008

    Article  CAS  Google Scholar 

  • Laureano-Marín AM, García I, Romero LC, Gotor C (2014) Assessing the transcriptional regulation of l-cysteine desulfhydrase 1 in Arabidopsis thaliana. Front Plant Sci 5:683

    Google Scholar 

  • Lee CP, Wirtz M, Hell R (2014) Evidence for several cysteine transport mechanisms in the mitochondrial membranes of Arabidopsis thaliana. Plant Cell Physiol 55:64–73

    Article  CAS  Google Scholar 

  • Liu F, Yoo BC, Lee JY, Pan W, Harmon AC (2006) Calcium regulated phosphorylation of soybean serine acetyltransferase in response to oxidative stress. J Biol Chem 281:27405–27415

    Article  CAS  Google Scholar 

  • Liu S, Liu Y, Yang X, Tong C, Edwards D, Parkin IA, Zhao M, Ma J, Yu J, Huang S, Wang X, Wang J, Lu K, Fang Z, Bancroft I, Yang TJ, Hu Q, Wang X, Yue Z, Li H, Yang L, Wu J, Zhou Q, Wang W, King GJ, Pires JC, Lu C, Wu Z, Sampath P, Wang Z, Guo H, Pan S, Yang L, Min J, Zhang D, Jin D, Li W, Belcram H, Tu J, Guan M, Qi C, Du D, Li J, Jiang L, Batley J, Sharpe AG, Park BS, Ruperao P, Cheng F, Waminal NE, Huang Y, Dong C, Wang L, Li J, Hu Z, Zhuang M, Huang Y, Huang J, Shi J, Mei D, Liu J, Lee TH, Wang J, Jin H, Li Z, Li X, Zhang J, Xiao L, Zhou Y, Liu Z, Liu X, Qin R, Tang X, Liu W, Wang Y, Zhang Y, Lee J, Kim HH, Denoeud F, Xu X, Liang X, Hua W, Wang X, Wang J, Chalhoub B, Paterson AH (2014) The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes. Nat Commun 5:3930

    CAS  Google Scholar 

  • López-Martín 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 147:562–572

    Article  CAS  Google Scholar 

  • Loudet O, Saliba-Colombani V, Camilleri C, Calenge F, Gaudon V, Koprivova A, North KA, Kopriva S, Daniel-Vedele F (2007) Natural variation for sulfate content in Arabidopsis thaliana is highly controlled by APR2. Nat Genet 39:896–900

    Article  CAS  Google Scholar 

  • Lunn JE, Droux M, Martin J, Douce R (1990) Localization of ATP sulfurylase and O-Acetylserine(thiol)lyase in spinach leaves. Plant Physiol 94:1345–1352

    Article  CAS  Google Scholar 

  • Maier TH (2003) Semisynthetic production of unnatural l-alpha-amino acids by metabolic engineering of the cysteine-biosynthetic pathway. Nat Biotechnol 21:422–427

    Article  CAS  Google Scholar 

  • Maruyama A, Ishizawa K, Takagi T (2000) Purification and characterization of β-cyanoalanine synthase and cysteine synthases from potato tubers: are β-cyanoalanine synthase and mitochondrial cysteine synthase same enzyme? Plant Cell Physiol 41:200–208

    Article  CAS  Google Scholar 

  • Mino K, Yamanoue T, Sakiyama T, Eisaki N, Matsuyama A, Nakanishi K (2000) Effects of bienzyme complex formation of cysteine synthetase from Escherichia coli on some properties and kinetics. Biosci Biotechnol Biochem 64:1628–1640

    Article  CAS  Google Scholar 

  • Mugford SG, Lee BR, Koprivova A, Matthewman C, Kopriva S (2011) Control of sulfur partitioning between primary and secondary metabolism. Plant J 65:96–105

    Article  CAS  Google Scholar 

  • Nakatani T, Ohtsu I, Nonaka G, Wiriyathanawudhiwong N, Morigasaki S, Takagi H (2012) Enhancement of thioredoxin/glutaredoxin-mediated l-cysteine synthesis from S-sulfocysteine increases l-cysteine production in Escherichia coli. Microb Cell Fact 11:62

    Article  CAS  Google Scholar 

  • Olsen LR, Huang B, Vetting MW, Roderick SL (2004) Structure of serine acetyltransferase in complexes with CoA and its cysteine feedback inhibitor. Biochemistry 43:6013–6019

    Article  CAS  Google Scholar 

  • Parkin IA, Koh C, Tang H, Robinson SJ, Kagale S, Clarke WE, Town CD, Nixon J, Krishnakumar V, Bidwell SL, Denoeud F, Belcram H, Links MG, Just J, Clarke C, Bender T, Huebert T, Mason AS, Pires JC, Barker G, Moore J, Walley PG, Manoli S, Batley J, Edwards D, Nelson MN, Wang X, Paterson AH, King G, Bancroft I, Chalhoub B, Sharpe AG (2014) Transcriptome and methylome profiling reveals relics of genome dominance in the mesopolyploid Brassica oleracea. Genome Biol 15:R77

    Article  CAS  Google Scholar 

  • Piotrowski M, Volmer JJ (2006) Cyanide metabolism in higher plants: cyanoalanine hydratase is a NIT4 homolog. Plant Mol Biol 61:111–122

    Article  CAS  Google Scholar 

  • Rausch T, Wachter A (2005) Sulfur metabolism: a versatile platform for launching defence operations. Trends Plant Sci 10:503–509

    Article  CAS  Google Scholar 

  • Ravilious GE, Jez JM (2012) Structural biology of plant sulfur metabolism: from assimilation to biosynthesis. Nat Prod Rep 29:1138–1152

    Article  CAS  Google Scholar 

  • Renata H, Wang ZJ, Arnold FH (2015) Expanding the enzyme universe: accessing non-natural reactions by mechanism-guided directed evolution. Angew Chem Int Ed Engl 54:3351–3367

    Article  CAS  Google Scholar 

  • Romero LC, Aroca MÁ, Laureano-Marín AM, Moreno I, García I, Gotor C (2014) Cysteine and cysteine-related signaling pathways in Arabidopsis thaliana. Mol Plant 7:264–276

    Article  CAS  Google Scholar 

  • Ruffet ML, Droux M, Douce R (1994) Purification and kinetic properties of serine acetyltransferase free of O-acetylserine(thiol)lyase from spinach chloroplasts. Plant Physiol 104(2):597–604

    CAS  Google Scholar 

  • Saito K, Yokoyama H, Noji M, Murakoshi I (1995) Molecular cloning and characterization of a plant serine acetyltransferase playing a regulatory role in cysteine biosynthesis from watermelon. J Biol Chem 270:16321–16326

    Article  CAS  Google Scholar 

  • Salbitani G, Wirtz M, Hell R, Carfagna S (2014) Affinity purification of O-acetylserine(thiol)lyase from Chlorella sorokiniana by recombinant proteins from Arabidopsis thaliana. Metabolites 4:629–639

    Article  CAS  Google Scholar 

  • Salsi E, Bayden AS, Spyrakis F, Amadasi A, Campanini B, Bettati S, Dodatko T, Cozzini P, Kellogg GE, Cook PF, Roderick SL, Mozzarelli A (2010) Design of O-acetylserine sulfhydrylase inhibitors by mimicking nature. J Med Chem 53:345–356

    Article  CAS  Google Scholar 

  • Schmidt A, Trebst A (1969) The mechanism of photosynthetic sulfate reduction by isolated chloroplasts. Biochim Biophys Acta 180:529–535

    Article  CAS  Google Scholar 

  • Schnug E, Booth E, Haneklaus S, Walker KC (1995) Sulphur supply and stress resistance in oilseed rape. In: Proceedings of the 9th international rapeseed congress, Cambridge, pp 229–231

  • Scuffi D, Álvarez C, Laspina N, Gotor C, Lamattina L, Garcia-Mata C (2014) Hydrogen sulfide generated by l-cysteine desulfhydrase acts upstream of nitric oxide to modulate ABA-dependent stomatal closure. Plant Physiol 166:2065–2076

    Article  CAS  Google Scholar 

  • Seo S, Mitsuhara I, Feng J, Iwai T, Hasegawa M, Ohashi Y (2011) Cyanide, a coproduct of plant hormone ethylene biosynthesis, contributes to the resistance of rice to blast fungus. Plant Physiol 155:502–514

    Article  CAS  Google Scholar 

  • Setya A, Murillo M, Leustek T (1996) Sulfate reduction in higher plants: molecular evidence for a novel 50-adenylylphosphosulfate (APS) reductase. Proc Natl Acad Sci USA 93:13383–13388

    Article  CAS  Google Scholar 

  • Shirzadian-Khorramabad R, Jing HC, Everts GE, Schippers JH, Hille J, Dijkwel PP (2010) A mutation in the cytosolic O-acetylserine(thiol) lyase induces a genome-dependent early leaf death phenotype in Arabidopsis. BMC Plant Biol 10:80

    Article  CAS  Google Scholar 

  • Sirko A, Blaszczyk A, Liszewska F (2004) Overproduction of SAT and/or OASTL in transgenic plants: a survey of effects. J Exp Bot 55:1881–1888

    Article  CAS  Google Scholar 

  • Spyrakis F, Felici P, Bayden AS, Salsi E, Miggiano R, Kellogg GE, Cozzini P, Cook PF, Mozzarelli A, Campanini B (2013) Fine tuning of the active site modulates specificity in the interaction of O-acetylserine sulfhydrylase isozymes with serine acetyltransferase. Biochim Biophys Acta 1834:169–181

    Article  CAS  Google Scholar 

  • Stevenazzi A, Marchini M, Sandrone G, Vergani B, Lattanzio M (2014) Amino acidic scaffolds bearing unnatural side chains: an old idea generates new and versatile tools for the life sciences. Bioorg Med Chem Lett 24:5349–5356

    Article  CAS  Google Scholar 

  • Tabe L, Wirtz M, Molvig L, Droux M, Hell R (2010) Overexpression of serine acetlytransferase produced large increases in O-acetylserine and free cysteine in developing seeds of a grain legume. J Exp Bot 61:721–733

    Article  CAS  Google Scholar 

  • Tahir J, Watanabe M, Jing HC, Hunter DA, Tohge T, Nunes-Nesi A, Brotman Y, Fernie AR, Hoefgen R, Dijkwel PP (2013) Activation of R-mediated innate immunity and disease susceptibility is affected by mutations in a cytosolic O-acetylserine(thiol) lyase in Arabidopsis. Plant J 73:118–230

    Article  CAS  Google Scholar 

  • Taiz L, Zeiger E (2010) Plant physiology, 5th edn. Sinauer Associates Inc, Sunderland

    Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis, version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  Google Scholar 

  • Tavares S, Wirtz M, Beier MP, Bogs J, Hell R, Amâncio S (2015) Characterization of the serine acetyltransferase gene family of Vitis vinifera uncovers differences in regulation of OAS synthesis in woody plants. Front Plant Sci. 6:74

    Article  Google Scholar 

  • Tsakraklides G, Martin M, Chalam R, Tarczynski MC, Schmidt A, Leustek T (2002) Sulfate reduction is increased in transgenic Arabidopsis thaliana expressing 50-adenylylsulfate reductase from Pseudomonas aeruginosa. Plant J 32:879–889

    Article  CAS  Google Scholar 

  • Turnbull AL, Surette MG (2008) l-Cysteine is required for induced antibiotic resistance in actively swarming Salmonella enterica serovar. Typhimurium. Microbiology 154:3410–3419

    Article  CAS  Google Scholar 

  • Vauclare P, Kopriva S, Fell D, Suter M, Sticher L, von Ballmoos P, Krahenbuhl U, den Camp RO, Brunold C (2002) Flux control of sulphate assimilation in Arabidopsis thaliana: adenosine 50-phosphosulphate reductase is more susceptible than ATP sulphurylase to negative control by thiols. Plant J 31:729–740

    Article  CAS  Google Scholar 

  • Wang X, Wang H, Wang J, Sun R, Wu J, Liu S, Bai Y, Mun JH, Bancroft I, Cheng F, Huang S, Li X, Hua W, Wang J, Wang X, Freeling M, Pires JC, Paterson AH, Chalhoub B, Wang B, Hayward A, Sharpe AG, Park BS, Weisshaar B, Liu B, Li B, Liu B, Tong C, Song C, Duran C, Peng C, Geng C, Koh C, Lin C, Edwards D, Mu D, Shen D, Soumpourou E, Li F, Fraser F, Conant G, Lassalle G, King GJ, Bonnema G, Tang H, Wang H, Belcram H, Zhou H, Hirakawa H, Abe H, Guo H, Wang H, Jin H, Parkin IA, Batley J, Kim JS, Just J, Li J, Xu J, Deng J, Kim JA, Li J, Yu J, Meng J, Wang J, Min J, Poulain J, Wang J, Hatakeyama K, Wu K, Wang L, Fang L, Trick M, Links MG, Zhao M, Jin M, Ramchiary N, Drou N, Berkman PJ, Cai Q, Huang Q, Li R, Tabata S, Cheng S, Zhang S, Zhang S, Huang S, Sato S, Sun S, Kwon SJ, Choi SR, Lee TH, Fan W, Zhao X, Tan X, Xu X, Wang Y, Qiu Y, Yin Y, Li Y, Du Y, Liao Y, Lim Y, Narusaka Y, Wang Y, Wang Z, Li Z, Wang Z, Xiong Z, Zhang Z, Brassica rapa Genome Sequencing Project Consortium (2011) The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43:1035–1039

  • Warrilow AG, Hawkesford MJ (2000) Cysteine synthase (O-acetylserine (thiol) lyase) substrate specificities classify the mitochondrial isoform as a cyanoalanine synthase. J Exp Bot 51:985–993

    Article  CAS  Google Scholar 

  • Watanabe M, Kusano M, Oikawa A, Fukushima A, Noji M, Saito K (2008a) Physiological roles of the beta-substituted alanine synthase gene family in Arabidopsis. Plant Physiol 146:310–320

    Article  CAS  Google Scholar 

  • Watanabe M, Mochida K, Kato T, Tabata S, Yoshimoto N, Noji M, Saito K (2008b) Comparative genomics and reverse genetics analysis reveal indispensable functions of the serine acetyltransferase gene family in Arabidopsis. Plant Cell 20:2484–2496

    Article  CAS  Google Scholar 

  • Watanabe M, Hubberten HM, Saito K, Hoefgen R (2010) General regulatory patterns of plant mineral nutrient depletion as revealed by serat quadruple mutants disturbed in cysteine synthesis. Mol Plant 3:438–466

    Article  CAS  Google Scholar 

  • Wiedemann G, Hermsen C, Melzer M, Büttner-Mainik A, Rennenberg H, Reski R, Kopriva S (2010) Targeted knock-out of a gene encoding sulfite reductase in the moss Physcomitrella patens affects gametophytic and sporophytic development. FEBS Lett 584:2271–2278

    Article  CAS  Google Scholar 

  • Winkel BS (2004) Metabolic channeling in plants. Annu Rev Plant Biol 55:85–107

    Article  CAS  Google Scholar 

  • Wirtz M, Hell R (2006) Functional analysis of the cysteine synthase protein complex from plants: structural, biochemical and regulatory properties. J Plant Physiol 163:273–286

    Article  CAS  Google Scholar 

  • Wirtz M, Berkowitz O, Droux M, Hell R (2001) The cysteine synthase complex from plants. Mitochondrial serine acetyltransferase from Arabidopsis thaliana carries a bifunctional domain for catalysis and protein-protein interaction. Eur J Biochem 268:686–693

    Article  CAS  Google Scholar 

  • Wirtz M, Droux M, Hell R (2004) O-acetylserine(thiol) lyase: anenigmatic enzyme of plant cysteine biosynthesis revisited in Arabidopsis thaliana. J Exp Bot 55:1785–1798

    Article  CAS  Google Scholar 

  • Wirtz M, Heeg C, Samami AA, Ruppert T, Hell R (2010) Enzymes of cysteine synthesis show extensive and conserved modifications patterns that include N(α)-terminal acetylation. Amino Acids 39:1077–1086

    Article  CAS  Google Scholar 

  • Wirtz M, Beard KF, Lee CP, Boltz A, Schwarzländer M, Fuchs C, Meyer AJ, Heeg C, Sweetlove LJ, Ratcliffe RG, Hell R (2012) Mitochondrial cysteine synthase complex regulates O-acetylserine biosynthesis in plants. J Biol Chem 287:27941–27947

    Article  CAS  Google Scholar 

  • Wurtele ES, Nikolau BL, Conn EE (1985) Subcellular and developmental distribution of beta-cyanoalanine synthase in barley leaves. Plant Physiol 78:285–290

    Article  CAS  Google Scholar 

  • Xie Y, Lai D, Mao Y, Zhang W, Shen W, Guan R (2013) Molecular cloning, characterization, and expression analysis of a novel gene encoding l-cysteine desulfhydrase from Brassica napus. Mol Biotechnol 54:737–746

    Article  CAS  Google Scholar 

  • 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 41:465–476

    Article  CAS  Google Scholar 

  • Yarmolinsky D, Brychkova G, Fluhr R, Sagi M (2013) Sulfite reductase protects plants against sulfite toxicity. Plant Physiol 161:725–743

    Article  CAS  Google Scholar 

  • Yi H, Jez JM (2012) Assessing functional diversity in the soybean β substituted alanine synthase enzyme family. Phytochemistry 83:15–24

    Article  CAS  Google Scholar 

  • Yi H, Galant A, Ravilious GE, Preuss ML, Jez JM (2010a) Sensing sulfur conditions: simple to complex protein regulatory mechanisms in plant thiol metabolism. Mol Plant 3:269–279

    Article  CAS  Google Scholar 

  • Yi H, Ravilious GE, Galant A, Krishnan HB, Jez JM (2010b) From sulfur to homoglutathione: thiol metabolism in soybean. Amino Acids 39:963–978

    Article  CAS  Google Scholar 

  • Yi H, Juergens M, Jez JM (2012) Structure of soybean β-cyanoalanine synthase and the molecular basis for cyanide detoxification in plants. Plant Cell 24:2696–2706

    Article  CAS  Google Scholar 

  • Yi H, Dey S, Kumaran S, Lee SG, Krishnan HB, Jez JM (2013) Structure of soybean serine acetyltransferase and formation of the cysteine regulatory complex as a molecular chaperone. J Biol Chem 288:36463–36472

    Article  CAS  Google Scholar 

  • Yip WK, Yang SF (1988) Cyanide metabolism in relation to ethylene production in plant tissues. Plant Physiol 88:473–476

    Article  CAS  Google Scholar 

  • Yonekura-Sakakibara K, Ashikari T, Tanaka Y, Kusumi T, Hase T (1998) Molecular characterization of tobacco sulfite reductase: enzyme purification, gene cloning, and gene expression analysis. J Biochem 124:615–621

    Article  CAS  Google Scholar 

  • Yonekura-Sakakibara K, Onda Y, Ashikari T, Tanaka Y, Kusumi T, Hase T (2000) Analysis of reductant supply systems for ferredoxin-dependent sulfite reductase in photosynthetic and nonphotosynthetic organs of maize. Plant Physiol 122:887–894

    Article  CAS  Google Scholar 

  • Zechmann B, Koffler BE, Russell SD (2011) Glutathione synthesis is essential for pollen germination in vitro. BMC Plant Biol 11:54–64

    Article  CAS  Google Scholar 

  • Zhu X, Yamaguchi T, Masada M (1998) Complexes of serine acetyltransferase and isozymes of cysteine synthase in spinach leaves. Biosci Biotechnol Biochem 62:947–952

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was carried out with the support of “Cooperative Research Program for Agriculture Science & Technology Development (Project No. PJ01115102),” Rural Development Administration, Republic of Korea.

Author information

Author notes

    Authors and Affiliations

    1. Department of Agricultural Biotechnology, National Academy of Agricultural Science, Jeonju, Republic of Korea

      Kyung Hee Roh

    2. Department of Biological Sciences, Chungnam National University, Daejeon, Republic of Korea

      Byung Wook Kang, Yoonkang Hur & Hankuil Yi

    3. Life Sciences Research Institute, Biomedic Co., Ltd.,, Bucheon, Republic of Korea

      Ho Bang Kim

    4. Faculty of Biotechnology, Jeju National University, Jeju, Republic of Korea

      Ho Bang Kim

    5. Division of Biomedical Engineering & Health Science Management, Mokwon University, Daejeon, Republic of Korea

      Sang Ho Lee

    Authors
    1. Kyung Hee Roh
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Byung Wook Kang
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Ho Bang Kim
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Sang Ho Lee
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Yoonkang Hur
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Hankuil Yi
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding authors

    Correspondence to Yoonkang Hur or Hankuil Yi.

    Additional information

    Yoonkang Hur and Hankuil Yi contributed equally to this work.

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Roh, K.H., Kang, B.W., Kim, H.B. et al. Physiological importance and possible applications of β-substituted alanine synthase in plants. Appl Biol Chem 59, 631–647 (2016). https://doi.org/10.1007/s13765-016-0202-7

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s13765-016-0202-7

    Keywords

    Search

    Navigation