Skip to main content

Advertisement

Springer Nature Link
Log in

Signaling in the plant cytosol: cysteine or sulfide?

  • Review Article
  • Published:
Amino Acids Aims and scope Submit manuscript

Abstract

Cysteine (Cys) is the first organic compound containing reduced sulfur that is synthesized in the last stage of plant photosynthetic assimilation of sulfate. It is a very important metabolite not only because it is crucial for the structure, function and regulation of proteins but also because it is the precursor molecule of an enormous number of sulfur-containing metabolites essential for plant health and development. The biosynthesis of Cys is accomplished by the sequential reaction of serine acetyltransferase (SAT) and O-acetylserine(thiol)synthase (OASTL). In Arabidopsis thaliana, the analysis of specific mutants of members of the SAT and OASTL families has demonstrated that the cytosol is the compartment where the bulk of Cys synthesis takes place and that the cytosolic OASTL enzyme OAS-A1 is the responsible enzyme. Another member of the OASTL family is DES1, a novel l-cysteine desulfhydrase that catalyzes the desulfuration of Cys to produce sulfide, thus acting in a manner opposite to that of OAS-A1. Detailed studies of the oas-a1 and des1 null mutants have revealed the involvement of the DES1 and OAS-A1 proteins in coordinate regulation of Cys homeostasis and the generation of sulfide in the cytosol for signaling purposes. Thus, the levels of Cys in the cytosol strongly affect plant responses to both abiotic and biotic stress conditions, while sulfide specifically generated from the degradation of Cys negatively regulates autophagy induced in different situations. In conclusion, modulation of the levels of Cys and sulfide is likely critical for plant performance.

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

Access this article

Log in via an institution

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

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

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • 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(2):656–669. doi:10.1104/pp.109.147975

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Alvarez C, Bermudez MA, Romero LC, Gotor C, Garcia I (2012a) Cysteine homeostasis plays an essential role in plant immunity. New Phytol 193(1):165–177. doi:10.1111/j.1469-8137.2011.03889.x

    Article  CAS  PubMed  Google Scholar 

  • Alvarez C, Garcia 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(11):4621–4634. doi:10.1105/tpc.112.105403

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Alvarez C, Garcia I, Romero LC, Gotor C (2012c) Mitochondrial sulfide detoxification requires a functional isoform O-acetylserine(thiol)lyase C in Arabidopsis thaliana. Mol Plant 5(6):1217–1226. doi:10.1093/mp/sss043

    Article  CAS  PubMed  Google Scholar 

  • Bassham DC (2007) Plant autophagy—more than a starvation response. Curr Opin Plant Biol 10(6):587–593. doi:10.1016/j.pbi.2007.06.006

    Article  CAS  PubMed  Google Scholar 

  • Bassham DC, Laporte M, Marty F, Moriyasu Y, Ohsumi Y, Olsen LJ, Yoshimoto K (2006) Autophagy in development and stress responses of plants. Autophagy 2(1):2–11 2092 [pii]

    Article  CAS  PubMed  Google Scholar 

  • 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(2):403–416. doi:10.1105/tpc.109.071985

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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(1):274–288. doi:10.1104/pp.112.201491

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bleecker AB, Kende H (2000) Ethylene: a gaseous signal molecule in plants. Annu Rev Cell Dev Biol 16:1–18. doi:10.1146/annurev.cellbio.16.1.1

    Article  CAS  PubMed  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(46):38803–38813

    Article  CAS  PubMed  Google Scholar 

  • Buchanan BB, Balmer Y (2005) Redox regulation: a broadening horizon. Annu Rev Plant Biol 56:187–220

    Article  CAS  PubMed  Google Scholar 

  • Buchner P, Stuiver CE, Westerman S, Wirtz M, Hell R, Hawkesford MJ, De Kok LJ (2004) Regulation of sulfate uptake and expression of sulfate transporter genes in Brassica oleracea as affected by atmospheric H(2)S and pedospheric sulfate nutrition. Plant Physiol 136(2):3396–3408

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chen J, Wu FH, Wang WH, Zheng CJ, Lin GH, Dong XJ, He JX, Pei ZM, Zheng HL (2011) Hydrogen sulphide enhances photosynthesis through promoting chloroplast biogenesis, photosynthetic enzyme expression, and thiol redox modification in Spinacia oleracea seedlings. J Exp Bot 62(13):4481–4493. doi:10.1093/jxb/err145

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cheng W, Zhang L, Jiao C, Su M, Yang T, Zhou L, Peng R, Wang R, Wang C (2013) Hydrogen sulfide alleviates hypoxia-induced root tip death in Pisum sativum. Plant Physiol Biochem 70:278–286. doi:10.1016/j.plaphy.2013.05.042

    Article  CAS  PubMed  Google Scholar 

  • Christou A, Manganaris GA, Papadopoulos I, Fotopoulos V (2013) Hydrogen sulfide induces systemic tolerance to salinity and non-ionic osmotic stress in strawberry plants through modification of reactive species biosynthesis and transcriptional regulation of multiple defence pathways. J Exp Bot 64(7):1953–1966. doi:10.1093/jxb/ert055

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chung T, Suttangkakul A, Vierstra RD (2009) The ATG autophagic conjugation system in maize: aTG transcripts and abundance of the ATG8-lipid adduct are regulated by development and nutrient availability. Plant Physiol 149(1):220–234. doi:10.1104/pp.108.126714

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Contento AL, Kim SJ, Bassham DC (2004) Transcriptome profiling of the response of Arabidopsis suspension culture cells to Suc starvation. Plant Physiol 135(4):2330–2347. doi:10.1104/pp.104.044362

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dawood M, Cao F, Jahangir MM, Zhang G, Wu F (2012) Alleviation of aluminum toxicity by hydrogen sulfide is related to elevated ATPase, and suppressed aluminum uptake and oxidative stress in barley. J Hazard Mater 209–210:121–128. doi:10.1016/j.jhazmat.2011.12.076

    Article  PubMed  Google Scholar 

  • Dixon DP, Lapthorn A, Edwards R (2002) Plant glutathione transferases. Genome Biol 3(3):REVIEWS3004

  • Droux M (2004) Sulfur assimilation and the role of sulfur in plant metabolism: a survey. Photosynth Res 79(3):331–348

    Article  CAS  PubMed  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(1):235–245

    Article  CAS  PubMed  Google Scholar 

  • Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155(1):2–18. doi:10.1104/pp.110.167569

    Article  PubMed Central  CAS  PubMed  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(12):3647–3655

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Garcia I, Castellano JM, Vioque B, Solano R, Gotor C, Romero LC (2010) Mitochondrial {beta}-cyanoalanine synthase is essential for root hair formation in Arabidopsis thaliana. Plant Cell 22(10):3268–3279. doi:10.1105/tpc.110.076828

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Garcia 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(4):2015–2027. doi:10.1104/pp.113.219436

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

  • Garcia-Mata C, Lamattina L (2010) Hydrogen sulphide, a novel gasotransmitter involved in guard cell signalling. New Phytol 188(4):977–984. doi:10.1111/j.1469-8137.2010.03465.x

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Mata C, Lamattina L (2013) Gasotransmitters are emerging as new guard cell signaling molecules and regulators of leaf gas exchange. Plant Sci 201–202:66–73. doi:10.1016/j.plantsci.2012.11.007

    Article  PubMed  Google Scholar 

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

  • Gotor C, Alvarez C, Bermudez MA, Moreno I, Garcia I, Romero LC (2010) Low abundance does not mean less importance in cysteine metabolism. Plant Signal Behav 5:1028–1030

  • Gotor C, Garcia I, Crespo JL, Romero LC (2013) Sulfide as a signaling molecule in autophagy. Autophagy 9(4):609–611. doi:10.4161/auto.23460

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gutierrez-Marcos JF, 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(23):13377–13382

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Haag AF, Kerscher B, Dall’Angelo S, Sani M, Longhi R, Baloban M, Wilson HM, Mergaert P, Zanda M, Ferguson GP (2012) Role of cysteine residues and disulfide bonds in the activity of a legume root nodule-specific, cysteine-rich peptide. J Biol Chem 287(14):10791–10798. doi:10.1074/jbc.M111.311316

    Article  PubMed Central  CAS  PubMed  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(2):1055–1067

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hatzfeld Y, Lee S, Lee M, Leustek T, Saito K (2000a) Functional characterization of a gene encoding a fourth ATP sulfurylase isoform from Arabidopsis thaliana. Gene 248(1–2):51–58

    Article  CAS  PubMed  Google Scholar 

  • Hatzfeld Y, Maruyama A, Schmidt A, Noji M, Ishizawa K, Saito K (2000b) Beta-cyanoalanine synthase is a mitochondrial cysteine synthase-like protein in spinach and Arabidopsis. Plant Physiol 123(3):1163–1171

    Article  PubMed Central  CAS  PubMed  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(1):168–185

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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(4):589–598

    Article  CAS  PubMed  Google Scholar 

  • Hu LY, Hu SL, Wu J, Li YH, Zheng JL, Wei ZJ, Liu J, Wang HL, Liu YS, Zhang H (2012) Hydrogen sulfide prolongs postharvest shelf life of strawberry and plays an antioxidative role in fruits. J Agric Food Chem 60(35):8684–8693. doi:10.1021/jf300728h

    Article  CAS  PubMed  Google Scholar 

  • Jacob C, Giles GI, Giles NM, Sies H (2003) Sulfur and selenium: the role of oxidation state in protein structure and function. Angew Chem Int Edn Engl 42(39):4742–4758

    Article  CAS  Google Scholar 

  • Jez JM, Dey S (2013) The cysteine regulatory complex from plants and microbes: what was old is new again. Curr Opin Struct Biol 23(2):302–310. doi:10.1016/j.sbi.2013.02.011

    Article  CAS  PubMed  Google Scholar 

  • Jin Z, Shen J, Qiao Z, Yang G, Wang R, Pei Y (2011) Hydrogen sulfide improves drought resistance in Arabidopsis thaliana. Biochem Biophys Res Commun 414(3):481–486. doi:10.1016/j.bbrc.2011.09.090

    Article  CAS  PubMed  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(1):220–230

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Khan MS, Haas FH, Samami AA, Gholami AM, Bauer A, Fellenberg K, Reichelt M, Hansch 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(4):1216–1231. doi:10.1105/tpc.110.074088

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kopriva S, Koprivova A (2004) Plant adenosine 5′-phosphosulphate reductase: the past, the present, and the future. J Exp Bot 55(404):1775–1783. doi:10.1093/jxb/erh185

    Article  CAS  PubMed  Google Scholar 

  • Krueger S, Niehl A, Lopez Martin MC, Steinhauser D, Donath A, Hildebrandt T, Romero LC, Hoefgen 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(4):349–367. doi:10.1111/j.1365-3040.2008.01928.x

    Article  CAS  PubMed  Google Scholar 

  • Laxman S, Sutter BM, Tu BP (2014) Methionine is a signal of amino acid sufficiency that inhibits autophagy through the methylation of PP2A. Autophagy 10(2):386–387. doi:10.4161/auto.27485

    Article  CAS  PubMed  Google Scholar 

  • Li F, Vierstra RD (2012) Autophagy: a multifaceted intracellular system for bulk and selective recycling. Trends Plant Sci 17(9):526–537. doi:10.1016/j.tplants.2012.05.006

    Article  CAS  PubMed  Google Scholar 

  • Li L, Wang Y, Shen W (2012) Roles of hydrogen sulfide and nitric oxide in the alleviation of cadmium-induced oxidative damage in alfalfa seedling roots. Biometals 25(3):617–631. doi:10.1007/s10534-012-9551-9

    Article  CAS  PubMed  Google Scholar 

  • Li ZG, Yang SZ, Long WB, Yang GX, Shen ZZ (2013) Hydrogen sulphide may be a novel downstream signal molecule in nitric oxide-induced heat tolerance of maize (Zea mays L.) seedlings. Plant Cell Environ 36(8):1564–1572. doi:10.1111/pce.12092

    Article  CAS  PubMed  Google Scholar 

  • Lisjak M, Srivastava N, Teklic T, Civale L, Lewandowski K, Wilson I, Wood ME, Whiteman M, Hancock JT (2010) A novel hydrogen sulfide donor causes stomatal opening and reduces nitric oxide accumulation. Plant Physiol Biochem 48(12):931–935. doi:10.1016/j.plaphy.2010.09.016

    Article  CAS  PubMed  Google Scholar 

  • Lisjak M, Teklic T, Wilson ID, Whiteman M, Hancock JT (2013) Hydrogen sulfide: environmental factor or signalling molecule? Plant Cell Environ 36(9):1607–1616. doi:10.1111/pce.12073

    Article  CAS  PubMed  Google Scholar 

  • Lopez-Martin MC, Becana M, Romero LC, Gotor C (2008a) Knocking out cytosolic cysteine synthesis compromises the antioxidant capacity of the cytosol to maintain discrete concentrations of hydrogen peroxide in Arabidopsis. Plant Physiol 147(2):562–572

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lopez-Martin MC, Romero LC, Gotor C (2008b) Cytosolic cysteine in redox signaling. Plant Signal Behav 3(10):880–881

    Article  PubMed Central  PubMed  Google Scholar 

  • Mendoza-Cozatl DG, Jobe TO, Hauser F, Schroeder JI (2011) Long-distance transport, vacuolar sequestration, tolerance, and transcriptional responses induced by cadmium and arsenic. Curr Opin Plant Biol 14(5):554–562. doi:10.1016/j.pbi.2011.07.004

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Noctor G, Mhamdi A, Chaouch S, Han Y, Neukermans J, Marquez-Garcia B, Queval G, Foyer CH (2012) Glutathione in plants: an integrated overview. Plant Cell Environ 35(2):454–484. doi:10.1111/j.1365-3040.2011.02400.x

    Article  CAS  PubMed  Google Scholar 

  • Park S, Imlay JA (2003) High levels of intracellular cysteine promote oxidative DNA damage by driving the fenton reaction. J Bacteriol 185(6):1942–1950

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Perez-Perez ME, Florencio FJ, Crespo JL (2010) Inhibition of target of rapamycin signaling and stress activate autophagy in Chlamydomonas reinhardtii. Plant Physiol 152(4):1874–1888. doi:10.1104/pp.109.152520

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Perez-Perez ME, Lemaire SD, Crespo JL (2012) Reactive oxygen species and autophagy in plants and algae. Plant Physiol 160(1):156–164. doi:10.1104/pp.112.199992

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Phillips AR, Suttangkakul A, Vierstra RD (2008) The ATG12-conjugating enzyme ATG10 is essential for autophagic vesicle formation in Arabidopsis thaliana. Genetics 178(3):1339–1353. doi:10.1534/genetics.107.086199

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Rea PA (2012) Phytochelatin synthase: of a protease a peptide polymerase made. Physiol Plant 145(1):154–164. doi:10.1111/j.1399-3054.2012.01571.x

    Article  CAS  PubMed  Google Scholar 

  • Richau KH, Kaschani F, Verdoes M, Pansuriya TC, Niessen S, Stuber K, Colby T, Overkleeft HS, Bogyo M, Van der Hoorn RA (2012) Subclassification and biochemical analysis of plant papain-like cysteine proteases displays subfamily-specific characteristics. Plant Physiol 158(4):1583–1599. doi:10.1104/pp.112.194001

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Romero LC, Garcia I, Gotor C (2013) l-Cysteine desulfhydrase 1 modulates the generation of the signaling molecule sulfide in plant cytosol. Plant Signal Behav 8:e24007

  • Romero LC, Aroca MA, Laureano-Marin AM, Moreno I, Garcia I, Gotor C (2014) Cysteine and cysteine-related signaling pathways in Arabidopsis thaliana. Mol Plant 7(2):264–276. doi:10.1093/mp/sst168

    Article  CAS  PubMed  Google Scholar 

  • Rose TL, Bonneau L, Der C, Marty-Mazars D, Marty F (2006) Starvation-induced expression of autophagy-related genes in Arabidopsis. Biol Cell 98(1):53–67. doi:10.1042/BC20040516

    Article  CAS  PubMed  Google Scholar 

  • Setya A, Murillo M, Leustek T (1996) Sulfate reduction in higher plants: molecular evidence for a novel 5′-adenylylsulfate reductase. Proc Natl Acad Sci USA 93(23):13383–13388

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sun J, Wang R, Zhang X, Yu Y, Zhao R, Li Z, Chen S (2013) Hydrogen sulfide alleviates cadmium toxicity through regulations of cadmium transport across the plasma and vacuolar membranes in Populus euphratica cells. Plant Physiol Biochem 65:67–74. doi:10.1016/j.plaphy.2013.01.003

    Article  CAS  PubMed  Google Scholar 

  • Sutter BM, Wu X, Laxman S, Tu BP (2013) Methionine inhibits autophagy and promotes growth by inducing the SAM-responsive methylation of PP2A. Cell 154(2):403–415. doi:10.1016/j.cell.2013.06.041

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Takahashi H (2010) Regulation of sulfate transport and assimilation in plants, Chapter 4. In: Kwang WJ (ed) International review of cell and molecular biology, vol 281. Academic Press, New York, pp 129–159. doi:10.1016/S1937-6448(10)81004-4

  • Takahashi H, Kopriva S, Giordano M, Saito K, Hell R (2011) Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes. Annu Rev Plant Biol 62:157–184. doi:10.1146/annurev-arplant-042110-103921

    Article  CAS  PubMed  Google Scholar 

  • Thompson AR, Vierstra RD (2005) Autophagic recycling: lessons from yeast help define the process in plants. Curr Opin Plant Biol 8(2):165–173. doi:10.1016/j.pbi.2005.01.013

    Article  CAS  PubMed  Google Scholar 

  • Thompson AR, Doelling JH, Suttangkakul A, Vierstra RD (2005) Autophagic nutrient recycling in Arabidopsis directed by the ATG8 and ATG12 conjugation pathways. Plant Physiol 138(4):2097–2110. doi:10.1104/pp.105.060673

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Van Hoewyk D, Pilon M, Pilon-Smits EAH (2008) The functions of NifS-like proteins in plant sulfur and selenium metabolism. Plant Sci 174(2):117–123. doi:10.1016/j.plantsci.2007.10.004

    Article  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 5′-phosphosulphate reductase is more susceptible than ATP sulphurylase to negative control by thiols. Plant J 31(6):729–740

    Article  CAS  PubMed  Google Scholar 

  • Wang R (2012) Physiological implications of hydrogen sulfide: a whiff exploration that blossomed. Physiol Rev 92(2):791–896. doi:10.1152/physrev.00017.2011

    Article  CAS  PubMed  Google Scholar 

  • Wang BL, Shi L, Li YX, Zhang WH (2010) Boron toxicity is alleviated by hydrogen sulfide in cucumber (Cucumis sativus L.) seedlings. Planta 231(6):1301–1309. doi:10.1007/s00425-010-1134-9

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Li L, Cui W, Xu S, Shen W, Wang R (2012) Hydrogen sulfide enhances alfalfa (Medicago sativa) tolerance against salinity during seed germination by nitric oxide pathway. Plant Soil 351(1–2):107–119

    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(1):310–320

    Article  PubMed Central  CAS  PubMed  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(9):2484–2496

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wirtz M, Droux M (2005) Synthesis of the sulfur amino acids: cysteine and methionine. Photosynth Res 86(3):345–362

    Article  CAS  PubMed  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(3):273–286

    Article  CAS  PubMed  Google Scholar 

  • Wirtz M, Hell R (2007) Dominant-negative modification reveals the regulatory function of the multimeric cysteine synthase protein complex in transgenic tobacco. Plant Cell 19(2):625–639

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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(404):1785–1798. doi:10.1093/jxb/erh201

    Article  CAS  PubMed  Google Scholar 

  • Xiong Y, Contento AL, Bassham DC (2005) AtATG18a is required for the formation of autophagosomes during nutrient stress and senescence in Arabidopsis thaliana. Plant J 42(4):535–546. doi:10.1111/j.1365-313X.2005.02397.x

    Article  CAS  PubMed  Google Scholar 

  • Xiong Y, Contento AL, Nguyen PQ, Bassham DC (2007) Degradation of oxidized proteins by autophagy during oxidative stress in Arabidopsis. Plant Physiol 143(1):291–299. doi:10.1104/pp.106.092106

    Article  PubMed Central  CAS  PubMed  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(4):465–476

    Article  CAS  PubMed  Google Scholar 

  • Yi H, Galant A, Ravilious GE, Preuss ML, Jez JM (2010) Sensing sulfur conditions: simple to complex protein regulatory mechanisms in plant thiol metabolism. Mol Plant 3(2):269–279. doi:10.1093/mp/ssp112

    Article  CAS  PubMed  Google Scholar 

  • Yoshimoto K (2012) Beginning to understand autophagy, an intracellular self-degradation system in plants. Plant Cell Physiol 53(8):1355–1365. doi:10.1093/pcp/pcs099

    Article  CAS  PubMed  Google Scholar 

  • Yoshimoto K, Hanaoka H, Sato S, Kato T, Tabata S, Noda T, Ohsumi Y (2004) Processing of ATG8s, ubiquitin-like proteins, and their deconjugation by ATG4s are essential for plant autophagy. Plant Cell 16(11):2967–2983. doi:10.1105/tpc.104.025395

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yoshimoto N, Inoue E, Watanabe-Takahashi A, Saito K, Takahashi H (2007) Posttranscriptional regulation of high-affinity sulfate transporters in Arabidopsis by sulfur nutrition. Plant Physiol 145(2):378–388. doi:10.1104/pp.107.105742

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yoshimoto K, Takano Y, Sakai Y (2010) Autophagy in plants and phytopathogens. FEBS Lett 584(7):1350–1358. doi:10.1016/j.febslet.2010.01.007

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Hu LY, Hu KD, He YD, Wang SH, Luo JP (2008) Hydrogen sulfide promotes wheat seed germination and alleviates oxidative damage against copper stress. J Integr Plant Biol 50(12):1518–1529. doi:10.1111/j.1744-7909.2008.00769.x

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Hu S-L, Zhang Z-J, Hu L-Y, Jiang C-X, Wei Z-J, Liu J, Wang H-L, Jiang S-T (2011) Hydrogen sulfide acts as a regulator of flower senescence in plants. Postharvest Biol Technol 60:251–257

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was funded in part by the European Regional Development Fund through the Ministerio de Economia y Competitividad (grants no. BIO2010-15201 and BIO2013-44648) and the Junta de Andalucía (grant no. CVI-7190). A.M.L-M. thanks the Ministerio de Economia y Competitividad for fellowship support through the program of Formación de Personal Investigador. A.A. thanks the Consejo Superior de Investigaciones Científicas for economic support provided by the postdoctoral program of the Junta de Ampliación de Estudios part-financed by the European Social Fund.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Instituto de Bioquímica Vegetal y Fotosíntesis, Consejo Superior de Investigaciones Científicias, Universidad de Sevilla, Avenida Américo Vespucio, 49, 41092, Seville, Spain

    Cecilia Gotor, Ana M. Laureano-Marín, Inmaculada Moreno, Ángeles Aroca, Irene García & Luis C. Romero

Authors
  1. Cecilia Gotor
    View author publications

    Search author on:PubMed Google Scholar

  2. Ana M. Laureano-Marín
    View author publications

    Search author on:PubMed Google Scholar

  3. Inmaculada Moreno
    View author publications

    Search author on:PubMed Google Scholar

  4. Ángeles Aroca
    View author publications

    Search author on:PubMed Google Scholar

  5. Irene García
    View author publications

    Search author on:PubMed Google Scholar

  6. Luis C. Romero
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Cecilia Gotor.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gotor, C., Laureano-Marín, A.M., Moreno, I. et al. Signaling in the plant cytosol: cysteine or sulfide?. Amino Acids 47, 2155–2164 (2015). https://doi.org/10.1007/s00726-014-1786-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00726-014-1786-z

Keywords