Subscribe to RSS
DOI: 10.1055/s-2007-965424
Georg Thieme Verlag Stuttgart KG · New York
Characterization of Cysteine-Degrading and H2S-Releasing Enzymes of Higher Plants - From the Field to the Test Tube and Back
Publication History
Received: September 8, 2006
Accepted: April 19, 2007
Publication Date:
13 September 2007 (online)
![](https://www.thieme-connect.de/media/plantbiology/200705/lookinside/thumbnails/10.1055-s-2007-965424-1.jpg)
Abstract
Due to the clean air acts and subsequent reduction of emission of gaseous sulfur compounds sulfur deficiency became one of the major nutrient disorders in Northern Europe. Typical sulfur deficiency symptoms can be diagnosed. Especially plants of the Cruciferae family are more susceptible against pathogen attack. Sulfur fertilization can in part recover or even increase resistance against pathogens in comparison to sulfur-deficient plants. The term sulfur-induced resistance (SIR) was introduced, however, the molecular basis for SIR is largely unknown. There are several sulfur-containing compounds in plants which might be involved in SIR, such as high levels of thiols, glucosinolates, cysteine-rich proteins, phytoalexins, elemental sulfur, or H2S. Probably more than one strategy is used by plants. Species- or even variety-dependent differences in the development of SIR are probably used. Our research focussed mainly on the release of H2S as defence strategy. In field experiments using different Brassica napus genotypes it was shown that the genetic differences among Brassica genotypes lead to differences in sulfur content and L-cysteine desulfhydrase activity. Another field experiment demonstrated that sulfur supply and infection with Pyrenopeziza brassica influenced L-cysteine desulfhydrase activity in Brassica napus. Cysteine-degrading enzymes such as cysteine desulfhydrases are hypothesized to be involved in H2S release. Several L- and D-cysteine-specific desulfhydrase candidates have been isolated and partially analyzed from the model plant Arabidopsis thaliana. However, it cannot be excluded that H2S is also released in a partial back reaction of O-acetyl-L-serine(thiol)lyase or enzymes not yet characterized. For the exact determination of the H2S concentration in the cell a H2S-specific microsensor was used the first time for plant cells. The transfer of the results obtained for application back on Brassica was initiated.
Key words
Arabidopsis thaliana - Brassica napus - cysteine - desulfhydrase - H2S
References
- 1 Bates T. S., Lamb B. K., Guenther A., Dignon J., Stoiber R. E.. Sulfur emissions to the atmosphere from natural sources. Journal of Atmospheric Chemistry. (1992); 14 315-337
- 2 Beauchamp R. O., Bus J. S., Popp J. A., Boreiko C. J., Andjelkovich D. A.. A critical review of the literature on hydrogen sulfide toxicity. Critical Reviews in Toxicology. (1984); 13 25-48
- 3 Bloem E., Riemenschneider A., Volker J., Papenbrock J., Schmidt A., Salac I., Haneklaus S., Schnug E.. Sulphur supply and infection with Pyrenopeziza brassica influence L-cysteine desulfhydrase activity in Brassica napus L. Journal of Experimental Botany. (2004); 55 2305-2312
- 52 Bloem E., Haneklaus S., Salac I., Wickenhäuser P., Schnug E.. Facts and fiction about sulfur metabolism in relation to plant-pathogen interactions. Plant Biology. (2007); 9 596-607
- 4 Bohlmann H., Apel K.. Thionins. Annual Review of Plant Physiology and Plant Molecular Biology. (1991); 42 227-240
- 5 Burandt P., Papenbrock J., Schmidt A., Bloem E., Haneklaus S., Schnug E.. Genotypical differences in total sulfur contents and cysteine desulfhydrase activities in Brassica napus L. Phyton. (2001 a); 41 75-86
-
6 Burandt P., Papenbrock J., Schmidt A., Bloem E., Haneklaus S., Schnug E..
Characterization of Brassica napus L. lines showing differences in total sulfur contents and cysteine desulfhydrase activities on the molecular level. Horst, W. J. et al., eds. Plant Nutrition - Food Security and Sustainability of Agro-Ecosystems. Dordrecht; Kluwer Academic Publishers (2001 b): 172-173 - 7 Burandt P., Schmidt A., Papenbrock J.. Three OAS‐TL isoenzymes from Arabidopsis catalyze cysteine synthesis and cysteine desulfuration at different pH values. Journal of Plant Physiology. (2002); 159 111-119
- 8 Cooper R. M., Resende M. L. V., Flood J., Rowan M. G., Beale M. H., Potter U.. Detection and cellular localization of elemental sulphur in disease-resistant genotypes of Theobroma cacao. Nature. (1996); 379 159-162
- 9 De Kok L. J., Castro A., Durenkamp M., Stuiver C. E. E., Westerman S., Yang L., Stulen I.. Sulphur in plant physiology. Proceedings No. 500, The International Fertiliser Society, York. (2000): 1-26
- 10 Giamoustaris A., Mithen R.. Glucosinolates and disease resistance in oilseed rape (Brassica napus ssp. oleifera). Plant Pathology. (1997); 46 271-275
- 11 Harrington H. M., Smith I. K.. Cysteine metabolism in cultured tobacco cells. Plant Physiology. (1980); 65 151-155
- 12 Hirai M. Y., Klein M., Fujikawa Y., Yano M., Goodenowe D. B., Yamazaki Y., Kanaya S., Nakamura Y., Kitayama M., Suzuki H., Sakurai N., Shibata D., Tokuhisa J., Reichelt M., Gershenzon J., Papenbrock J., Saito K.. Elucidation of gene-to-gene networks in Arabidopsis by integration of metabolomics and transcriptomics. Journal of Biological Chemistry. (2005); 280 25590-25595
- 13 Kliebenstein D. J.. Secondary metabolites and plant/environment interactions: a view through Arabidopsis thaliana tinged glasses. Plant, Cell and Environment. (2004); 27 732-738
- 14 Kushnir S., Babiychuk E., Storozhenko S., Davey M. W., Papenbrock J., De Rycke R., Engler G., Stephan U. W., Lange H., Kispal G., Lill R., van Montagu M.. Mutation of the mitochondrial ABC transporter Sta1 leads to dwarfism and chlorosis in the Arabidopsis mutant starik. Plant Cell. (2001); 13 89-100
- 15 Leon S., Tournaine B., Briat J. F., Lobreaux S.. The AtNFS2 gene from Arabidopsis thaliana encodes a NifS-like plastidial cysteine desulphurase. Biochemical Journal. (2002); 366 557-564
-
16 Leustek T..
Sulfate metabolism. Somerville, C. R. and Meyerowitz, E. M., eds. The Arabidopsis Book , Rockville, MD, USA: American Society of Plant Biologists, April 4, 2002. DOI: 10.1199/tab.0017 http://www.aspb.org/publications/arabidopsis/ (2002) -
17 Mazelis M..
Catabolism of sulfur-containing amino acids. De Kok, L. J., Stulen, I., Rennenberg, H., Brunold, C., and Rauser, W. E., eds. Sulfur Ntrition and Assimilation in Higher Plants. The Hague; SPB Academic Publishing bv (1993): 95-108 - 18 McEwan M., MacFarlane Smith W. H.. Identification of volatile organic compounds emitted in the field by oilseed rape (Brassica napus ssp. oleifera) over the growing season. Clinical and Experimental Allergy. (1998); 28 332-338
- 19 Mueller E. G.. Trafficking in persulfides: delivering sulfur in biosynthetic pathways. Nature Chemical Biology. (2006); 2 185-194
- 20 Nagasawa T., Ishii T., Kumagai H., Yamada H.. D-cysteine desulfhydrase of Escherichia coli. Purification and characterization. European Journal of Biochemistry. (1985); 153 541-551
- 21 Nagasawa T., Ishii T., Yamada H.. Physiological comparison of D-cysteine desulfhydrase of Escherichia coli with 3-chloro-D-alanine dehydrochlorinase of Pseudomonas putida CR 1-1. Archives of Microbiology. (1988); 149 413-416
- 22 Pilon-Smits E. A., Garifullina G. F., Abdel-Ghany S., Kato S., Mihara H., Hale K. L., Burkhead J. L., Esaki N., Kurihara T., Pilon M.. Characterization of a NifS-like chloroplast protein from Arabidopsis. Implications for its role in sulfur and selenium metabolism. Plant Physiology. (2002); 130 1309-1318
- 23 Rausch T., Wachter A.. Sulfur metabolism: a versatile platform for launching defence operations. Trends in Plant Science. (2005); 10 503-509
- 24 Rennenberg H.. Cysteine desulfhydrase activity in cucurbit plants: simulation by preincubation with L- and D-cysteine. Phytochemistry. (1983); 22 1557-1560
- 25 Rennenberg H.. Synthesis and emission of hydrogen sulfide by higher plants. ACS Symposium Series - American Chemical Society (USA). (1989); 393 44-57
- 26 Rennenberg H., Filner P.. Developmental changes in the potential for H2S emission in cucurbit plants. Plant Physiology. (1983); 71 269-275
- 27 Rennenberg H., Arabatzis N., Grundel I.. Cysteine desulphydrase activity in higher plants: evidence for the action of L- and D-cysteine specific enzymes. Phytochemistry. (1987); 26 1583-1589
- 28 Rennenberg H., Huber B., Schroder P., Stahl K., Haunold W., Georgii H. W., Slovik S., Pfanz H.. Emission of volatile sulfur compounds from spruce trees. Plant Physiology. (1990); 92 560-564
- 29 Resende M. L. V., Flood J., Ramsden J. D., Rowan M. G., Beale M. H., Cooper R. M.. Novel phytoalexins including elemental sulphur in the resistance of cocoa (Theobroma cacao L.) to Verticillium wilt (Verticillium dahliae Kleb.). Physiological and Molecular Plant Pathology. (1996); 48 347-359
- 30 Riemenschneider A.. Isolation and characterization of cysteine-degrading and H2S-releasing enzymes of higher plants. PhD Thesis, University of Hannover. (2006)
-
31 Riemenschneider A., Bonacina E., Schmidt A., Papenbrock J..
Isolation and characterization of a second D-cysteine desulfhydrase-like protein from Arabidopsis. . Saito, K., De Kok, L. J., Stulen, I., Hawkesford, M. J., Schnug, E., Sirko, A., and Rennenberg, H., eds. Sulfur Transport and Assimilation in Plants in the Post Genomic Era. Leiden; Backhuys Publishers (2005 a): 103-106 - 32 Riemenschneider A., Nikiforova V., Hoefgen R., De Kok L. J., Papenbrock J.. Impact of elevated H2S on metabolite levels, activity of enzymes and expression of genes involved in cysteine metabolism. Plant Physiology and Biochemistry. (2005 b); 43 473-483
- 33 Riemenschneider A., Riedel K., Hoefgen R., Papenbrock J., Hesse H.. Impact of reduced O-acetylserine(thiol)lyase isoform contents on potato (Solanum tuberosum L.) plant metabolism. Plant Physiology. (2005 c); 137 892-900
- 34 Riemenschneider A., Wegele R., Schmidt A., Papenbrock J.. Isolation and characterization of a D-cysteine desulfhydrase protein from Arabidopsis thaliana. FEBS Journal. (2005 d); 272 1291-1304
- 35 Schmidt A.. A cysteine desulfhydrase from spinach leaves specific for D-cysteine. Zeitschrift für Pflanzenphysiologie. (1982); 107 301-312
-
36 Schmidt A..
Metabolic background of H2S release from plants. De Kok, L. J. and Schnug, E., eds. Proceedings of the 1st Sino-German Workshop on Aspects of Sulfur Nutrition of Plants. Landbauforschung Völkenrode (2005): 121-129 - 37 Schmidt A., Erdle I.. A cysteine desulfhydrase specific for D-cysteine from the green alga Chlorella fusca. Zeitschrift für Naturforschung C. (1983); 38 428-435
- 38 Schnug E., Booth E., Haneklaus S., Walker K. C.. Sulphur supply and stress resistance in oilseed rape. Proceedings of the 9th International Rapeseed Congress, Cambridge. (1995): 229-231
-
39 Schröder P..
Plants as a source of atmospheric sulfur. De Kok, L. J., Stulen, I., Rennenberg, H., Brunold, C., and Rauser, W. E., eds. Sulfur Nutrition and Sulfur Assimilation in Higher Plants. The Hague; SPB Academic Publishing bv (1993): 253-270 - 40 Schulz H. N., Jørgensen B. B.. Big bacteria. Annual Review of Microbiology. (2001); 55 105-137
- 41 Schulz H. N., de Beer D.. Uptake rates of oxygen and sulfide measured with individual Thiomargarita namibiensis cells by using microelectrodes. Applied and Environmental Microbiology. (2002); 68 5746-5749
- 42 Schütz B., De Kok L. J., Rennenberg H.. Thiol accumulation and cysteine desulfhydrase activity in H2S-fumigated leaves and leaf homogenates of cucurbit plants. Plant Cell Physiology. (1991); 32 733-736
- 43 Searcy D. G.. HS-:O2 oxidoreductase activity of Cu,Zn superoxide dismutase. Archives of Biochemistry and Biophysics. (1996); 334 50-58
- 44 Sekiya J., Schmidt A., Wilson L. G., Filner P.. Emission of hydrogen sulfide by leaf tissue in response to L-cysteine. Plant Physiology. (1982 a); 70 430-436
- 45 Sekiya J., Wilson L. G., Filner P.. Resistance to injury by sulfur dioxide: correlation with its reduction to, and emission of, hydrogen sulfide in Cucurbitaceae. Plant Physiology. (1982 b); 70 437-441
- 46 Soutourina J., Blanquet S., Plateau P.. Metabolism of D-aminoacyl-tRNAs in Escherichia coli and Saccharomyces cerevisiae cells. Journal of Biological Chemistry. (2000); 275 32535-32542
- 47 Soutourina J., Blanquet S., Plateau P.. Role of D-cysteine desulfhydrase in the adaptation of Escherichia coli to D-cysteine. Journal of Biological Chemistry. (2001); 276 40864-40872
- 48 Staton A. L., Mazelis M.. The C-S lyases of higher plants: homogeneous beta-cystathionase of spinach leaves. Archives of Biochemistry and Biophysics. (1991); 290 46-50
- 49 Williams J. S., Cooper R. M.. The oldest fungicide and newest phytoalexin - a reappraisal of the fungitoxicity of elemental sulphur. Plant Pathology. (2004); 53 263-279
- 50 Williams J. S., Hall S. A., Hawkesford M. J., Beale M. H., Cooper R. M.. Elemental sulfur and thiol accumulation in tomato and defense against a fungal vascular pathogen. Plant Physiology. (2002); 128 150-159
- 51 Wirtz M., Droux M., Hell R.. O-acetylserine (thiol) lyase: an enigmatic enzyme of plant cysteine biosynthesis revisited in Arabidopsis thaliana. Journal of Experimental Botany. (2004); 55 1785-1798
J. Papenbrock
Institut für Botanik
Universität Hannover
Herrenhäuser Straße 2
30419 Hannover
Germany
Email: jutta.papenbrock@botanik.uni-hannover.de
Guest Editor: T. Rausch