Subscribe to RSS
DOI: 10.1055/s-2007-965420
Georg Thieme Verlag Stuttgart KG · New York
Facts and Fiction about Sulfur Metabolism in Relation to Plant-Pathogen Interactions
Publication History
Received: September 20, 2006
Accepted: April 19, 2007
Publication Date:
13 September 2007 (online)
![](https://www.thieme-connect.de/media/plantbiology/200705/lookinside/thumbnails/10.1055-s-2007-965420-1.jpg)
Abstract
Sulfur deficiency developed into a widespread nutrient disorder in the 1980s because of the drastic decrease of SO2 emissions in western Europe after Clean Air Acts came into force. It was observed that not only the yield and quality of agricultural crops were negatively affected by sulfur deficiency but also their health status. Since the mid 1990s the physiological background of this latter phenomenon in the sulfur metabolism has been studied by different researchers. From 2001 until 2006, field trials with different varieties of oilseed rape were conducted in Germany, and also from 2001 until 2003 in Scotland, to investigate the underlying mechanisms of sulfur-induced resistance and to develop fertiliser strategies which increase the health status of crops and minimise the requirement for chemical fungicides. A comprehensive disease assessment was conducted and a range of different sulfur-containing metabolites and enzymes were analysed in relation to sulfur nutrition and fungal diseases. H2S emissions from field-grown crops under different sulfur nutritional status were studied for the first time and a positive relationship was observed. Besides S fertilisation, fungal infection increased H2S emissions, too. The studies deliver new insight into the complex of sulfur-induced resistance but many questions still remain open. This contribution will show different possible strategies to solve some of the open questions.
Key words
Sulfur-induced resistance (SIR) - H2S - cysteine - glutathione - fungal pathogens.
References
- 1 Almeida M. S., Cabral K. M. S., Zingali R. B., Kurtenbach E.. Characterization of two novel defense peptides from pea (Pisum sativum) seeds. Archiv für Biochemie und Biophysik. (2000); 378 278-286
- 2 Anon . www.vetpharm.unizh.ch . (2006)
-
3 Anderson J. W..
Sulfur metabolism in plants. Miflin, B. J. and Lea, P. J., eds. The Biochemistry of Plants, A Comprehensive Treatise, Vol. 16. New York; Academic Press (1990): 327-381 - 4 Balesdent M. H., Desthieux I., Gall C., Robin P., Rouxel T.. Quantification of Leptosphaeria maculans growth in cotyledons of Brassica napus using ELISA. Journal of Phytopathology. (1995); 143 65-73
- 5 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 of Toxicology. (1984); 13 25-97
- 6 Beffa T.. Inhibitory-action of elemental sulphur (S°) on fungal spores. Canadian Journal of Microbiology. (1993); 39 731-735
- 7 Bloem E., Haneklaus S., Schnug E.. Significance of sulfur compounds in the protection of plants against pests and diseases. Journal of Plant Nutrition. (2005); 28 763-784
- 8 Bloem E., Haneklaus S., Schnug E.. Comparative effects of sulfur and nitrogen fertilization and post-harvest processing parameters on the glucotropaeolin content of Tropaeolum majus L. Journal of the Science of Food and Agriculture. (2007); 87 1576-1585
- 9 Bloem E., Riemenschneider A., Volker J., Papenbrock J., Schmidt A., Salac I., Haneklaus S., Schnug E.. Sulphur supply and infection with Pyrenopeziza brassicae influence L-cysteine desulphydrase activity in Brassica napus L. Journal of Experimental Botany. (2004); 55 2305-2312
- 10 Börner H.. Pflanzenkrankheiten und Pflanzenschutz, 7th ed. Stuttgart; Eugen Ulmer (1997)
-
11 Bohlmann H..
The role of thionins in the resistance of plants. Datta, S. K. and Muthukrishnan, S., eds. Pathogenesis-Related Proteins in Plants. Boca Raton; CRC Press, Inc. (1999): 207-234 -
12 Bosma W., Kamminga G., De Kok L. J..
H2S-induced accumulation of sulfhydryl-compounds in leaves of plants under field and laboratory exposure. Rennenberg, H., Brunold, C., De Kok, L. J., and Stulen, I., eds. Sulfur Nutrition and Sulfur Assimilation in Higher Plants. The Hague, The Netherlands; SPB Academic Publishing (1990): 173-175 - 13 Bourbos V. A., Skoudridakis M. T., Barbopoulou E., Venetis K.. Ecological control of grape powdery mildew (Uncinula necator). http://www.landwirtschaft-mlr.badenwuerttemberg.de/la/lvwo/kongress/SULFUR.html. (2000)
- 14 Broekaert W. F., Cammue B. P., De Bolle M. F. C., Thevissen K., De Samblanx G. W., Osborn R. W.. Antimicrobial peptides in plants. Critical Reviews of Plant Science. (1997); 16 297-323
- 15 Broekaert W. F., Terras F. R., Cammue B. P., Osborn R. W.. Plant defensins: novel antimicrobial peptides as components of the host defense system. Plant Physiology. (1995); 108 1353-1358
- 16 Brown P. D., Morra M. J.. Control of soil-borne plant pests using glucosinolate-containing plants. Advances in Agronomy. (1997); 61 167-231
- 17 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); 41 75-86
- 18 Carlile M. J., Watkinson S. C., Gooday G. W.. The Fungi. Amsterdam; Elsevier Academic Press (2004)
- 19 Cobbett C. S.. Phytochelatines and their roles in heavy metal detoxification. Plant Physiology. (2000); 123 825-832
- 20 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
- 21 De Kok L. J., De Kan J. L., Tànczos O. G., Kuiper P. J. C.. Sulphate induced accumulation of glutathione and frost tolerance of spinach leaf tissue. Physiologia Plantarum. (1981); 53 435-438
-
22 De Kok L. J..
Sulfur metabolism in plants exposed to atmospheric sulfur. Rennenberg, H., Brunold, C., De Kok, L. J., and Stulen, I., eds. Sulphur Nutrition and Sulphur Assimilation in Higher Plants; Fundamental, Environmental and Agricultural Aspects. The Hague; SPB Academic Publishing (1990): 111-130 - 23 De Kok L. J., Stuiver C. E. E., Rubinigg M., Westerman S., Grill D.. Impact of atmospheric sulfur depositions on sulfur metabolism in plants: H2S as a sulfur source for sulfur deprived Brassica oleracea L. Botanica Acta. (1997); 110 411-419
- 24 Delapena R. C., Murray T. D.. Identifying wheat genotypes resistant to eyespot disease with a beta-glucuronidase-transformed strain of Pseudocercosporella herpotrichoides. Phytopathology. (1994); 84 972-977
- 25 Drobnica L., Zemanová M., Nemec P., Antos K., Kristián P., Stullerová S., Knoppavá V., Nemec P.. Antifungal activity of isothiocyanates and related compounds. I. Naturally occurring isothiocyanates and their analogues. Applied Microbiology. (1967); 15 701-709
- 26 Dubuis P. H., Marazzi C., Städler E., Mauch F.. Sulphur deficiency causes a reduction in antimicrobial potential and leads to increased disease susceptibility of oilseed rape. Journal of Phytopathology. (2005); 153 27-36
- 27 Edwards R., Blount J. W., Dixon R. A.. Glutathione and elicitation of the phytoalexin response in legume cultures. Planta. (1991); 184 403-409
- 28 Epple P., Apel K., Bohlmann H.. Overexpression of an endogenous thionin enhances resistance of Arabidopsis against Fusarium oxysporum. Plant Cell. (1997); 9 509-520
-
29 Filner P., Rennenberg H., Sekiya J., Bressan R. A., Wilson L. G., Le Cureux L., Shimei T..
Biosynthesis and emission of hydrogen sulfide by higher plants. Koziol, M. J. and Whatley, F. R., eds. Gaseous Air Pollutants and Plant Metabolism. London; Butterworths (1984): 291-312 - 30 ForoughiWehr B., Zuchner S., Rabenstein F.. Enzyme-linked immunosorbent assay for detection Rhynchosporium secalis (Oud) J. J. Davis in winter barley. Journal of Plant Disease and Protection. (1996); 103 267-271
- 31 Forsyth W.. A Treatise on the Culture and Management of Fruit Trees. London; Nichols and Son (1802)
-
32 Foyer C. H., Rennenberg H..
Regulation of glutathione synthesis and its role in abiotic and biotic stress defence. Brunold, C., Rennenberg, H., De Kok, L. J., Stulen, I., and Davidian, J.-C., eds. Sulfur Nutrition and Sulfur Assimilation in Higher Plants. Berne; Paul Haupt Publishers (2000): 127-153 - 33 Gerber D. B., Mancl K. M., Veenhuizen M. A., Shurson G. C.. Ammonia, Carbon Monoxide, Carbon Dioxide, Hydrogen Sulfide, and Methane in Swine Confinement Facilities. Compendium on Continuing Education for the Practicing Veterinarian. (1991); 13 1483-1488
-
34 Giovanelli J..
Regulatory aspects of cysteine and methionine biosynthesis. Rennenberg, H., Brunold, C., De Kok, L. J., and Stulen, I., eds. Sulfur Nutrition and Sulfur Assimilation in Higher Plants; Fundamental, Environmental and Agricultural Aspects. The Hague, The Netherlands; SPB Academic Publishing bv (1990): 33-48 -
35 Giovanelli J., Mudd S. H., Datko A. H..
Sulfur amino acids in plants. Miflin, B. J., ed. The Biochemistry of Plants, Vol. 5. New York; Academic Press (1980): 453-505 -
36 Gullner G., Kömives T..
The role of glutathione and glutathione-related enzymes in plant-pathogen interactions. Grill, D., Tausz, M., De Kok, L. J., eds. Significance of Glutathione in Plant Adaptation to the Environment. Dordrecht; Kluwer Academic Publishing (2001): 202-239 - 37 Hancock R. E. W., Falla T., Brown M.. Cationic bactericidal peptides. Advances in Microbiology and Physiology. (1995); 37 135-175
-
38 Haneklaus S., Bloem E., Schnug E..
Sulfur and plant disease. Datnoff, L., Elmer, W., and Huber, D., eds. Mineral Nutrition and Plant Diseases. St. Paul, MN; APS Press (2007 a): 101-118 - 39 Haneklaus S., Bloem E., DeKok L. J., Yang Z., Wang S., Schnug E.. The potential of sulfur induced resistance against plant diseases of oilseed rape. Proceedings 12th International Oilseed Rape Congress, Wuhan, China, 26 - 30 March 2007. IVI Science Press USA (2007 b): 43-46
- 40 Hassall K. A.. The Biochemistry and Uses of Pesticides. Basingstoke, UK; Macmillan Press (1990)
- 41 Haunold W., Ockelmann G., Georgii H. W.. Neuartiger Gaschromatograph zur Messung von SO2 und reduzierten Schwefelgasen in Reinluftgebieten. Staub - Reinhaltung der Luft. (1989); 49 191-196
- 42 Haunold W., Georgii H. W., Ockelmann G.. Gas chromatographic analysis of atmospheric sulfur dioxide and reduced sulfur compounds. LC GC Magazine of Separation Science. (1992); 5 28-35
- 43 Hell R.. Molecular physiology of plant sulfur metabolism. Planta. (1997); 202 138-148
- 44 Hoy M. A.. Sulfur as a control agent for pest mites in agriculture. Proceedings of the International Symposium Elemental Sulphur in Agriculture, Nice. (1987); 1 51-61
- 45 Huber B., Haunold W.. Measuring fluxes of reduced sulfur gases. FAL Agricultural Research, Special Issue. (2005); 283 61-65
- 46 Huber D.. Managing Nutrition to Control Plant Disease. FAL Agricultural Research. (2007);
- 47 Hughes P., Dennis E., Whitecross M., Llewellyn D., Gage P.. The cytotoxic plant protein, beta-purothionin, forms ion channels in liquid membranes. Journal of Biological Chemistry. (2000); 275 823-827
- 48 Jost R., Altschmied L., Bloem E., Bogs J., Gershenzon J., Hähnel U., Hänsch R., Hartmann T., Kopriva S., Mendel R. R., Papenbrock J., Reichelt M., Rennenberg H., Schnug E., Schmidt A., Textor S., Tokuhisa J., Wachter A., Rausch T., Hell R.. Expression profiling of metabolic genes in response to methyl jasmonate reveals regulation of genes of primary and secondary sulfur-related pathways in Arabidopsis thaliana. Photosynthesis Research. (2005); 86 491-508
- 49 Kassemeyer H. H.. Untersuchungen zur Entwicklung des Myzels und der Konidien von Uncinula necator und deren Einfluß auf die Epidemiologie. http://www.infodienst.bwl.de/mlr/Forschung/2000/Pflanzenschutz. (2003)
- 50 Klikocka H., Haneklaus S., Bloem E., Schnug E.. Influence of sulfur fertilization on infection of potato tubers with Rhizoctonia solani and Streptomyces scabies. Journal of Plant Nutrition. (2005); 28 819-833
- 51 Kuzniak E., Sklodowska M.. Fungal pathogen-induced changes in the antioxidant systems of leaf peroxisomes from infected tomato plants. Planta. (2005); 222 192-200
- 52 Lamb C., Dixon R. A.. The oxidative burst in plant disease resistance. Annual Review in Plant Physiology and Plant Molecular Biology. (1997); 48 251-275
- 53 Leustek T., Martin M. N., Bick J. A., Davies J. P.. Pathways and regulation of sulfur metabolism revealed through molecular studies. Annual Review of Plant Physiology and Plant Molecular Biology. (2000); 51 141-166
- 54 Lind V.. Measuring the severity of eyespot disease induced by Pseudocercosporella herpotrichoides (Fron) Deighton in wheat cultivars at different growth-stages. Plant Breeding. (1992); 108 202-209
- 55 Lorgue G., Lechenet J., Riviere A.. Clinical Veterinary Toxicology. Oxford, London, Edinburgh, Cambridge, USA, Australia; Blackwell Science Ltd. (1996): 118
-
56 Mansfield J. W..
Antimicrobial compounds and resistance: the role of phytoalexins and phytoanticipins. Slusarenko, A., Fraser, R., and van Loon, L., eds. Mechanisms of Resistance to Plant Diseases. Dordrecht; Kluwer Academic Publishers (2000): 325-370 - 57 Manici L. M., Lazzeri L., Palmieri S.. In vitro fungitoxic activity of some glucosinolates and their enzyme-derived products toward plant pathogenic fungi. Journal of Agriculture and Food Chemistry. (1997); 45 2768-2773
- 58 Miller L. P., McCallan S. E. A., Weed R. M.. Quantitative studies on the role of hydrogen sulfide formation in the toxic action of sulfur to fungus spores. Contributions from Boyce Thompson Institute. (1953); 17 151-171
- 59 Mithen R. F., Lewis B. G., Fenwick G. R.. In vitro activity of glucosinolates and their products against Leptosphaeria maculans. Transactions of the British Mycological Society. (1986); 87 433-440
- 60 Mithen R. F., Lewis B. G., Heaney R. K., Fenwick G. R.. Resistance of leaves of Brassica species to Leptosphaeria maculans. Transactions of the British Mycological Society. (1987); 88 525-531
- 61 Newton A. C., Reglinski T.. An enzyme-linked-immunosorbent-assay for quantifying mildew biomass. Journal of Plant Disease and Protection. (1993); 100 176-179
- 62 Nicolas P., Mor A.. Peptides as weapons against microorganisms in the chemical defense system of vertebrates. Annual Review of Microbiology. (1995); 49 277-304
- 63 Noctor G., Arisi A. C. M., Jouanin L., Kunert K. J., Rennenberg H., Foyer C.. Glutathione: biosynthesis, metabolism and relationship to stress tolerance explored in transformed plants. Journal of Experimental Botany. (1998); 49 623-647
- 64 O'Donoghue J. G.. Hydrogen Sulphide Poisoning in Swine. Canadian Journal of Comparative Medicine and Veterinary Science. (1961); 25 217-219
- 65 Ogawa K., Hatano-Iwasaki A., Yanagida M., Iwabuchi M.. Level of glutathione is regulated by ATP-dependent ligation of glutamate and cysteine through photosynthesis in Arabidopsis thaliana: mechanism of strong interaction of light intensity with flowering. Plant Cell Physiology. (2004); 45 1-8
- 66 Osborn R. W., De Samblanx G. W., Thevissen K., Goderis I., Torrekens S., Van Leuven F., Attenborough S., Rees S. B., Broekaert W. F.. Isolation and characterisation of plant defensins from seeds of Asteraceae, Fabaceae, Hippocastanaceae and Saxifragaceae. FEBS Letters. (1995); 368 257-262
- 67 Parisy V., Poinssot B., Owsianowski L., Buchala A., Glazebrook J., Mauch F.. Identification of PAD2 as a γ-glutamylcysteine synthetase highlights the importance of glutathione in disease resistance of Arabidopsis. The Plant Journal. (2006); 49 159-172
- 68 Pedras M. S. C., Okanga F. I., Zaharia I. L., Khan A. Q.. Phytoalexins from crucifers: synthesis, biosynthesis, and biotransformation. Phytochemistry. (2000); 53 161-176
- 69 Rausch T., Wachter A.. Sulfur metabolism: a versatile platform for launching defence operations. Trends in Plant Science. (2005); 10 503-509
- 70 Rea P. A., Li Z. S., Lu Y. P., Drozdowicz Y. M., Martinoia E.. From vacuolar GS‐X pumps to multispecific ABC transporters. Annual Review of Plant Physiology and Plant Molecular Biology. (1998); 49 727-760
- 71 Rennenberg H.. Role of O-acetylserine in hydrogen sulfide emissions from pumpkin leaves in response to sulfate. Plant Physiology. (1983); 73 560-565
- 72 Rennenberg H.. The fate of excess sulphur in higher plants. Annual Review of Plant Physiology. (1984); 35 121-153
- 73 Rennenberg H.. Synthesis and emission of hydrogen sulfide by higher plants. ACS Symposium Series - American Chemical Society (USA). (1989); 393 44-57
-
74 Rennenberg H..
Glutathione - an ancient metabolite with modern tasks. Grill, D., Tausz, M., and De Kok, L. J., eds. Significance of Glutathione in Plant Adaptation to the Environment. Dordrecht; Kluwer Academic Publishing (2001): 1-11 - 75 Rennenberg H., Filner P.. Stimulation of H2S emission from pumpkin leaves by inhibition of glutathione synthesis. Plant Physiology. (1982); 69 766-770
- 76 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
- 77 Riemenschneider A.. Isolation and characterization of cysteine-degrading and H2S-releasing proteins in higher plants. PhD Thesis, University Hannover, Germany. (2006)
- 78 Salac I.. Influence of the sulphur and nitrogen supply on S metabolites involved in Sulphur Induced Resistance (SIR) of Brassica napus L., PhD Thesis. FAL Agricultural Research, Special Issue. (2005); 277 134
- 79 Salac I., Haneklaus S., Bloem E., Booth E., Sutherland K., Walker K., Schnug E.. Influence of sulfur fertilization on sulfur metabolites, disease incidence and severity of fungal pathogens in oilseed rape in Scotland. FAL Agricultural Research. (2006); 56 1-4
- 80 Salac I., Haneklaus S., Gassner A., Bloem E., Schnug E.. Relation between Spatial Variability of Plant Physiological Parameters in Oilseed Rape and Infection with Leptosphaeria maculans. Phyton. (2004); 44 215-229
- 81 Sarwar M., Kirkegaard J. A., Wong P. T. W., Desmarchelier J. M.. Biofumigation potential of brassicas. III. In vitro toxicity of isothiocyanates to soil-borne fungal pathogens. Plant and Soil. (1998); 201 103-112
- 82 Sasaki-Sekimoto Y., Taki N., Obayashi T., Aono M., Matsumoto F., Sakurai N., Suzuki H., Hirai M. Y., Noji M., Saito K., Masuda T., Takamiya K., Shibata D., Ohta H.. Coordinated activation of metabolic pathways for antioxidants and defence compounds by jasmonates and their roles in stress tolerance in Arabidopsis. The Plant Journal. (2005); 44 653-668
-
83 Schnug E..
Glucosinolates - fundamental, environmental and agricultural aspects. Rennenberg, H., Brunold, C., De Kok, L. J., and Stulen, I., eds. Sulfur Nutrition and Sulfur Assimilation in Higher Plants. The Hague; SPB Academic Publishing (1990): 97-106 -
84 Schnug E..
Significance of sulphur for the quality of domesticated plants. Cram, W. J., De Kok, L. J., Stulen, I., Brunold, C., and Rennenberg, H., eds. Sulphur Metabolism in Higher Plants. Leiden; Backhuys Publishing (1997): 109-130 - 85 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 a): 229-231
- 86 Schnug E., Haneklaus S., Borchers A., Polle A.. Relations between sulphur supply and glutathione, ascorbate and glucosinolate concentrations in Brassica napus varieties. Journal of Plant Nutrition and Soil Science. (1995 b); 158 67-70
-
87 Schroeder P..
Plants as sources 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 (1993): 253-270 - 88 Segura A., Moreno M., Molina A., Garcia-Olmedo F.. Novel defensin subfamily from spinach (Spinacia oleracea). FEBS Letters. (1998); 435 159-162
- 89 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
- 90 Sekiya J., Schmidt A., Rennenberg H., Wilson L. G., Filner P.. Hydrogen sulfide emission by cucumber leaves in response to sulfate in light and dark. Phytochemistry. (1982 b); 21 2173-2178
- 91 Shai Y.. Mechanism of the binding, insertion and destabilization of phospholipid bilayer membranes by alpha-helical antimicrobial and cell non-selective membrane-lytic peptides. Biochimica et Biophysica Acta - Biomembranes. (1999); 1462 55-70
- 92 Smith B. J., Kirkegaard J. A.. In vitro inhibition of soil microorganisms by 2-phenylethyl isothiocyanate. Plant Pathology. (2002); 51 585-593
- 93 Smolinska U., Morra M. J., Knudsen G. R., James R. L.. Isothiocyanates produced by Brassicaceae species as inhibitors of Fusarium oxysporum. Plant Disease. (2003); 87 407-412
- 94 Strauss R., Bleiholder H., van den Boom T., Buhr L., Hack H., Hess M., Klose R., Meier U., Weber E.. Einheitliche Codierung der phaenologischen Entwicklungsstadien mono- und dikotyler Pflanzen. Basel; Ciba-Geigy AG (1994): 56pp
-
95 Tausz M..
The role of glutathione in plant response and adaptation to natural stress. Grill, D., Tausz, M., and De Kok, L. J., eds. Significance of Gutathione in Plant Adaptation to the Environment. Dordrecht; Kluwer Academic Publishing (2001): 101-122 - 96 Thomma B. P. H. J., Nelissen I., Eggermont K., Broekaert F W.. Deficiency in phytoalexin production causes enhanced susceptibility of Arabidopsis thaliana to the fungus Alternaria brassicicola. The Plant Journal. (1999); 19 163-171
- 97 Thompson C. R., Kats G.. Effects of continuous H2S fumigation on crop and forest plants. Environmental Science and Technology. (1978); 12 550-553
- 98 Tierens K. F. M. J., Thomma B. P. H. J., Brouwer M., Schmidt J., Kistner K., Porzel A., Mauch-Mani B., Cammue B. P. A., Broekaert W. F.. Study of the role of antimicrobial glucosinolates-derived isothiocyanates in resistance of Arabidopsis to microbial pathogens. Plant Physiology. (2001); 125 1688-1699
- 99 Tsuji J., Jackson E. P., Gage D. A., Hammerschmidt R., Somerville S. C.. Phytoalexin accumulation in Arabidopsis thaliana during the hypersensitive reaction to Pseudomonas syringae pv syringae. Plant Physiology. (1992); 98 1304-1309
-
100 Tweedy G. G..
Inorganic sulfur as fungicide. Gunther, F. A. and Gunther, J. D., eds. Residue Reviews, Vol. 78. New York; Springer Verlag (1981): 43-68 - 101 Vidhyasekaran P.. Fungal Pathogenesis in Plants and Crops. Boca Raton; CRC Press, Inc. (1997)
- 102 Vidhyasekaran P.. Physiology of Disease Resistance in Plants, Vol. II. Boca Raton; CRC Press, Inc. (2000)
- 103 Wang J., Zhang J., Ma Y., Wang Li Yang L., Shi S., Liu L., Schnug E.. Crop resistance to diseases as influenced by sulphur application rates. Proceedings of the 12th World Fertilizer Congress, August 3 - 9, 2001, Beijing, China. (2003): 1285-1296
- 105 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
- 106 Williams J. S., Cooper R. M.. Elemental sulphur is produced by diverse plant families as a component of defence against fungal and bacterial pathogens. Physiological and Molecular Plant Pathology. (2003); 63 3-16
- 107 Williams J. S., Cooper R. M.. The oldest fungicide and the newest phytoalexin - a reappraisal of the fungitoxicity of elemental sulphur. Plant Pathology. (2004); 53 263-279
- 108 Wilson L. G., Bressan R. A., Filner P.. Light-dependent emission of hydrogen sulfide from plants. Plant Physiology. (1978); 61 184-189
- 109 Winner W. E., Smith C. L., Koch G. W., Mooney H. A., Bewley J. D., Krouse H. R.. Rate of emission of H2S from plants and patterns of stable sulphur isotope fractionation. Nature. (1981); 289 672-673
- 110 Winterbourn C. C., Metodiewa D.. Reactivity of biologically important thiol compounds with superoxide and hydrogen peroxide. Free Radical Biology and Medicine. (1999); 27 322-328
- 111 Yang Z., Haneklaus S., DeKok L. J., Schnug E., Singh B. R.. Effect of H2S and DMS on growth and enzymatic activities of Rhizoctonia solani and its implications for sulfur-induced resistance (SIR) of agricultural crops. Phyton. (2006); 46 55-70
- 112 Zook M., Hammerschmidt R.. Origin of the thiazole ring of camalexin, a phytoalexin from Arabidopsis thaliana. Plant Physiology. (1997); 113 463-468
E. Bloem
Institute of Plant Nutrition and Soil Science
Federal Agricultural Research Centre (FAL)
Bundesallee 50
38116 Braunschweig
Germany
Email: elke.bloem@fal.de
Guest Editor: T. Rausch