JXB Advance Access originally published online on June 4, 2004
Journal of Experimental Botany 2004 55(404):1947-1953; doi:10.1093/jxb/erh179
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RESEARCH PAPER |
Elemental sulphur as an induced antifungal substance in plant defence
Department of Biology and Biochemistry, University of Bath, Bath BA2 7AY, UK
* To whom correspondence should be addressed. Fax +44 (0)1225 386779. E-mail: bssrmc{at}bath.ac.uk
Received 12 February 2004; Accepted 6 April 2004
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Abstract |
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Top
Abstract
IntroductionMan's oldest fungicide has probably long functioned in this role in plants, as a natural component of induced antifungal defence. Elemental sulphur (S0) is the only inorganic phytoalexin and the only phytoalexin produced by so many different taxa. S0 (detected by GC-MS as 32S8) is produced in representative species of Sterculiaceae (cocoa), Solanaceae (tomato, tobacco), Malvaceae (cotton), and Leguminosae (French bean) in response to xylem-invading fungal and bacterial pathogens. Production was more rapid and intensive in disease-resistant genotypes. Gene expression for S0 production may be xylem-specific as S0 was not present in leaves of six species undergoing hypersensitivity to Pseudomonas syringae. Anomalously, high constitutive S0 levels occurred in leaves of Arabidopsis and Brassica oleracea. S0 was highly toxic (ED50 1–3 µg ml–1) to many fungal pathogens representing ascomycetes, basidiomycetes, and deuteromycetes, but not to an oomycete, Phytophthora, or to bacteria. Levels in cocoa and tomato xylem and Arabidopsis leaves were potentially inhibitory, but in other interactions were below theoretically toxic concentrations. However, S0 accumulation is highly localized, suggesting that the element is produced in sufficient amounts, at the right time and place to be effective. SEM-EDX revealed S in tomato and cocoa xylem walls, xylem parenchyma, and vascular gels and tyloses, all sites appropriate to counter vascular pathogenic Verticillium dahliae. Transient increases in sulphate, glutathione and cysteine occurred in tomato xylem. The sulphate may reflect the over-expression of sulphate transporters, but the thiols might be possible precursors. Analysis of differential gene expression should reveal what may be a novel biosynthetic pathway of S0 formation in eukaryotes.
Key words: Arabidopsis, defence, fungicide, hypersensitivity, pathogens, phytoalexin, sulphur, thiols, tomato, xylem
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Introduction |
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There are many S-containing compounds, which have been linked, directly or indirectly, with the defence of plants against microbial pathogens; these include thionins, defensins, glucosinolates, crucifer phytoalexins, alliin, and glutathione (Hell, 1997
). Before the recent discovery, to be outlined in this chapter, elemental sulphur (S0) was not considered as a component of disease resistance. This is partly because the element had never been detected in the numerous investigations of antimicrobial compounds in diverse plants. S0 may have been overlooked in thin layer chromatography (TLC) plate bioassays, the most common basis of discovery of new compounds. Because S0 is highly hydrophobic and often runs with or close to the solvent front, antifungal bands there are often dismissed as artefacts resulting from contamination from solvents or silica gel. Another likely reason for it remaining undetected for so long, is that S0 formation, although well known in certain specialized prokaryotes (Visser et al., 1997; Reinartz et al., 1998), has rarely been detected in eukaryotes (Kraus et al., 1984; Pezet and Pont, 1977) and only three times in plants (Cooper et al., 1996; Joyard et al., 1988; Kylin et al., 1994). The element is best known to Man as his oldest pesticide.
S0 was first recommended for disease control by Forsyth (1802). By the early 20th century it was the most important fungicide, especially for fruit diseases, until organic S-fungicides such as maneb and captan were developed in the 1950s (Tweedy, 1981). Nevertheless, in the early 1970s, the use of S0 in the USA exceeded by 2.5 times that of any other fungicide (Hassall, 1990). Now, systemic fungicides with diverse but site-specific modes of action predominate, yet S0 is still used, often in combination with them; this is to increase their spectrum but also to increase their lifespan, because of the development of pathogen resistance to compounds with single site action (Jolivet, 1993). Field resistance to S0 has not been reported, no doubt because it has multiple sites of action, although the precise mode(s) of action is still not known (Beffa et al., 1987).
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Plant defences: a key role for phytoalexins |
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Plants possess a myriad of defences. Constitutive resistance includes physical barriers such as the cuticle and cell walls, and antimicrobial compounds (phytoanticipins) such as saponins and phenolics (Cooper, 1981
; Kuhn and Hargreaves, 1987). Active defences in response to pathogen invasion include the formation of reaction oxygen species, localized cell wall reinforcement (by lignin, suberin, structural proteins, silicon, calcium), antimicrobial or lytic proteins, and antimicrobial compounds (phytoalexins). Many of these changes are linked to a rapid, apoptotic response, resulting in the death of one or a few invaded plant cells, known as the hypersensitive response (HR) (Hammond-Kosack and Jones, 1996).
Most plant families produce organic phytoalexins of diverse chemistry; these groups are often associated with a family, for example, sesquiterpenoids of Solanaceae, isoflavanoids of Leguminosae. Typically, there is a multiple response involving several related derivatives, such as up to nine wyerone (furanoacetylenic derivatives) forms in Vicia faba, and several forms of phaseollin in Phaseolus vulgaris and Glycine max (Keen and Kennedy, 1974; Mansfield, 2000). The compounds are formed de novo in living cells and accumulate to high levels, especially in HR cells. HR cells have lost the metabolic capacity to degrade them, unlike the producing cells in which there is a high turnover, perhaps because some phytoalexins are also toxic to plant cells. Pathogens are inhibited in or adjacent to HR cells and the accumulation of phytoalexins is one key component of creating an antimicrobial environment (Mansfield, 2000).
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Discovery of elemental sulphur as a phytoalexin in five plant families |
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An investigation (initially using a TLC bioassay) of chemical defences in resistant lines of Theobroma cacao (Sterculiaceae) against the xylem-invading fungal pathogen Verticillium dahliae, revealed a typical multiple phytoalexin response comprising four antifungal compounds (Cooper et al., 1996
; Resende et al., 1996). Extracted xylem contained a terpenoid (arjunolic acid) and two phenolics (acetophenones). The most hydrophobic and fungitoxic compound unexpectedly proved to be elemental sulphur. This was confirmed by TLC co-chromatograhy, GC-MS (S8 breaking down successively to S2), and X-ray crystallography. It was initially suspected to be artefactual, as a breakdown product of a S-rich organic compound. However, there was a lack of 1H or 13C NMR signals that would result from an organic S compound that undergoes thermolysis on GC-MS to give free S (Cooper et al., 1996).
Subsequently S0 production has been reported to be linked with active defence in another three important plant families, and potentially with preformed defence in another family: Leguminosae, Malvaceae, Solanaceae, and Cruciferae (Williams et al., 2002; Williams and Cooper, 2003). Accurate quantitative analysis was facilitated by the development of novel methods involving GC-MS using dilution analysis with an added 34S8 standard (Williams et al., 2002).
S0 was detected from xylem excised from plants inoculated with fungal vascular pathogens: cotton and tomato to V. dahliae, French bean and tobacco to Fusarium oxysporum formae speciales, and tomato to the bacterial vascular pathogen Ralstonia solanacearum (Fig. 1) (Williams and Cooper, 2003). The pattern and kinetics of S0 formation mirror that of many organic phytoalexins, with a faster and greater production in disease-resistant genotypes than in susceptible lines, and with no or negligible amounts in control tissue (Mansfield, 2000; Kuhn and Hargreaves, 1987). In view of this trend it was unexpected to find S0 in high constitutive amounts in leaves of Arabidopsis and in cotyledons of Brassica oleracea; in the latter hybrid, inoculation with an HR-inducing, incompatible race of the obligate downy mildew Peronospora parasitica did not increase S0 levels.
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With the exception of members of the Cruciferae, the response may be specific to xylem. S0 was absent from leaves of six species showing hypersensitivity to incompatible isolates of Pseudomonas syringae pathovars. Other than lettuce, barley, and cabbage, these included species which had produced S0 in xylem challenged by vascular pathogens, i.e. tomato, tobacco, and French bean. Genes expressed specifically in xylem are well documented and those of possible relevance include group 1 and group 2 sulphate transporters, the former in response to Verticillium (Howarth et al., 2003
; Smith et al., 1995; Takahashi et al., 2000) and the I-2 gene in tomato for resistance to F. oxysporum (Mes et al., 2000). S0 was not detected in xylem of strawberry challenged with V. dahliae or in maize leaves inoculated with Erwinia stewartii. A wider survey of S0 production is needed to confirm tissue specificity and occurrence in different taxa. However, the current methodology for accurate and unequivocal detection of S0 restricts the rate at which samples can be processed.
Because of its elemental nature, the likelihood of detection at the cellular level was possible. Few antimicrobial compounds in plants have been visualized at this level (Cooper et al., 1996; Mansfield, 2000). Scanning electron microscopy combined with X-ray microanalysis (SEM-EDX) revealed that in T. cacao and in tomato, localized accumulations of S were present in locations relevant to inhibit a xylem-invading pathogen. i.e. in scattered xylem parenchyma cells, xylem vessel walls, and vascular occluding gels and tyloses (Fig. 2). The latter structures are probably produced as a defence response to occlude vessels and prevent systemic movement of the pathogen (Cooper, 2000). SEM-EDX also confirmed the absence of significant S levels in adjacent stem pith tissue in these two species (Cooper et al., 1996; Williams and Cooper, 2003). The accumulation of S in xylem parenchyma cells could reflect accumulation in hypersensitive cells; the death of a proportion of these cells is typical for vascular diseases (Cooper, 1981). Other phytoalexins such as wyerone and phaseollin accumulate to high concentrations in necrotic areas (Mansfield, 2000).
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SEM-EDX showed S in A. thaliana leaves was present in all cell types, but the technique does not distinguish elemental from bound S and may merely reflect the many S compounds which characterize crucifers, such as glucosinolates and S-containing phytoalexins (Pedras et al., 1997
; Fahey et al., 2001). |
Toxicity and pathogen spectrum of elemental sulphur |
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From previously published work, of which much was from the early 20th century, it is difficult to ascribe level and range of toxicity of S0 to pathogens. Different formulations were used by investigators, such as sulphur flowers (sublimed S0), sulphur flour (ground S0), milk of sulphur (precipitated S0), colloidal S0 (wettable form of the previous types), lime sulphur (sulphide of lime containing S0), and liver of sulphur (potash containing S0) (Thatcher and Streeter, 1925
; Sharvelle, 1961). Also different bioassays were used, but much data were derived from observations of disease control under field conditions (Williams and Cooper, 2004). Although minimum inhibitory concentrations and modes of action were not clear from these many studies, it is apparent that S0-sensitive pathogens include powdery mildews (against which S0 is best known (Jolivet, 1993)), certain smut and rust fungi, anamorphic fungi with no described sexual stage such as Verticillium and Fusarium, and some fungi with known ascomycete stages such as Stagonospora nodorum and Venturia inaequalis. Therefore, the toxicity of S0 was reinvestigated using the pathogens from the host–pathogen survey and representatives of the major fungal groups, with a variety of bioassays designed to test effects in the short and long term, and to all relevant fungal stages. This was partly to relate the S0 levels detected in planta with a possible role in defence. Susceptibility of Gram-negative and -positive bacteria was also tested because of lack of information and because R. solanacearum triggered S0 formation in tomato.
In summary, all fungal species were highly sensitive to S0. Spore germination (on glass) of most species was inhibited at c. 3 µg ml–1 and the TLC bioassay (on silica gel), which reflects growth of spores and hyphae, showed inhibition at c. 6–12 µg ml–1. Some fungi appeared highly sensitive, such as Blumeria graminis (cereal powdery mildew) and Ustilago maydis (maize smut), which were inhibited at <1 µg ml–1. Verticillium and Fusarium species with a vascular mode of parasitism or with alternative pathogenic strategies (e.g. insect or nematode pathogens, or rot-inducing plant necrotrophs), were compared for S0 sensitivity. This was to test if xylem-invading species had acquired tolerance to S0 as a component of pathogenicity; tolerance to or detoxification of phytoalexins is often a prerequisite to pathogenicity (Morrissey and Osbourn, 1999; Van Etten et al., 2001). However, there was no adaptation by vascular pathogenic forms, and this would agree with the absence of reports on pathogens developing resistance in the field to S0 following its use as a commercial fungicide.
There was no inhibition of the Oomycete Phytophthora palmivora even at 8 mg ml–1. Oomycetes resemble fungi in the form of their thalli, ecology, and the plant parasitic ability of some species and are traditionally studied by mycologists (Berbee and Taylor, 1999). However, they are not close relatives of fungi (according to flagella structure and small subunit rRNA). Nevertheless Phytophthora species are sensitive to certain antifungal phytoalexins, such as from soybean, sweet pepper, and potato (Williams and Cooper, 2004). The insensitivity of P. parasitica to S0 may explain the lack of data in the literature on the effects of S0 on this group.
Bacteria were also not inhibited by S0 concentrations up to 8 mg ml–1. This may reflect that S0 is produced by many specialized bacterial species: purple and green sulphur bacteria accumulate S0 globules when reduced S compounds are used as electron donors for anoxygenic photosynthesis, whereas, sulphur-oxidizing bacteria produce S0 aerobically (Hazeu et al., 1988; Izac et al., 1982; Prange et al., 1999). The elicitation of S0 in tomato by R. solanacearum may therefore seem paradoxical, however, it shows that plants produce multiple defences, which are not entirely specific to the elicitation event, but part of a broad response.
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Levels of elemental sulphur, its location and form in planta |
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S0 appeared in T. cacao and tomato in a relevant tissue and cellular location, at the right time and in sufficient amounts to be implicated in a defence role, mediated by inhibition of the pathogen V. dahliae. Maximum amounts in T. cacao were >110 µg g–1 and in tomato >10 µg g–1. In other interactions, in which sulphur was induced in resistant varieties to significant levels by fungal xylem-invading pathogens, the concentrations (max 100–250 ng g–1) were below the theoretical levels for fungitoxicity (c. 1–12 µg ml–1). Nevertheless, from many studies on organic phytoalexins, it is accepted that extracts from whole tissues can give substantial underestimates of phytoalexin levels present in localized areas of infection, such as HR cells (Mansfield, 2000
). SEM-EDX analysis suggests that S0 can also be concentrated in this way. Levels of S0 (1.5–6 µg g–1) in Arabidopsis leaves were also potentially inhibitory to fungi, but there is no evidence at this stage of cellular localization.
The inevitable anomaly exists as to how pathogens invade plants containing potentially toxic levels of constitutive antifungal compounds. The biotrophic pathogens of Arabidopsis, Erysiphe orontii (powdery mildew), and Peronospora parasitica (downy mildew) may not contact or release S0 because of their subtle mode of invasion of living cells, but necrotrophs are potentially vulnerable to preformed compounds because these aggressive pathogens release and encounter them following cellular decompartmentalization and degradation (Morrissey and Osbourn, 1999). It may be coincidental, but to the authors' knowledge there are relatively few necrotrophs of Arabidopsis. It would be valuable to investigate those that do, such as Botrytis cinerea and Alternaria brassicicola (Thomma et al., 1999), in terms of their sensitivity to S0 and cellular location with respect to sites of S0 accumulation.
As with other non-polar phytoalexins, the question must be considered, in what form does this hydrophobic element exist in the largely hydrophilic environment of the cell? This aspect has been studied in sulphur-producing bacteria in which sulphur globules are liquid and amorphous (Steudel et al., 1990), whereas S0 is solid and usually crystalline at 20 °C. Proteins may act as surfactants, enveloping the sulphur droplets with their hydrophilic components interacting with the aqueous cytosol and the hydrophobic moieties directed to the globule surface, preventing crytallization (Brune, 1995; Steudel, 1989). However, sulphur globules have not been visualized in plant cells and S0 accumulations were also detected extracellularly (within xylem walls, gels, and tyloses). Other phytoalexins such as wyerone can also become extracellular, probably by secretion rather than passive diffusion (Kuhn and Hargreaves, 1987). Clearly much work remains as to the actual form in planta of S0 that is encountered by plant pathogens.
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Biogenesis of elemental sulphur |
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Sulphate, the major source of sulphur for plants, is reduced in a multistep pathway, predominantly in the chloroplasts, to sulphide. It then combines to form cysteine, of which some is converted to methionine or glutathione; the latter is the major stored and transportable form of non-protein reduced sulphur (Schmidt and Jäger, 1992
; Hell, 1997; Leustek and Saito, 1999; Hawkesford and Wray, 2000). The production of elemental sulphur in eukaryotes is by an uncharacterized pathway. The origin of the S0 production in plants may be from glutathione or cysteine degradation or from oxidation of sulphide as a by-product. Therefore, these components were analysed in a model plant–pathogen system, in which S0 is produced in the resistant interaction, in order to provide possible clues for the biosynthetic route of S0. Transient but significant increases of 2–3-fold were detected in concentrations of sulphate, glutathione, and cysteine in inoculated vascular tissues from stems of resistant but not susceptible lines of tomato after infection by V. dahliae (Williams et al., 2002). Sulphate levels were also higher in root xylem and in leaves, and glutathione also increased in leaves. These changes in thiols and sulphate only occurred in plants supplied with a high sulphate regime (1.0 mM 
). Later comments on the frequency of sulphur deficiency in crops should be noted in the context of the capacity of stressed plants to produce defence-related compounds.
The increased sulphate levels may reflect the over-expression of sulphate transporters in response to the burden on metabolism to produce S0. The transient peaks of cysteine and glutathione preceded or coincided with that of S0 and might implicate these S-containing compounds in the biogenesis of S0. Leaves are the major site of S reduction, and glutathione would be involved in its transport in the xylem. The pool size of glutathione can also be elevated in response to the oxidative burst that typically accompanies defence to pathogens, because of the protective effect of reduced glutathione (Kömives et al., 1998; May et al., 1996). Localized glutathione accumulation and its subsequent degradation, together with chemical oxidation (Steudel et al., 1986), could result in the observed depositions of S0. An alternative route may involve sulphide oxidase postulated to result in S0 production in spinach chloroplasts (Joyard et al., 1988), and oxidation by cytochromes has been suggested in the green alga Chlorella fusca (Kraus et al., 1984). Both of these enzymes have been implicated in the production of bacterial S0 (Moriarty and Nicholas, 1970; Gray and Knaff, 1982; Pattaragulwanit et al., 1998). It is possible that sulphide is a by-product of the degradation of these thiols and it is this sulphide that is oxidized to form S0 in a non-enzymic reaction (Steudel et al., 1986). Cysteine degradation pathways are another possibility, for example, by a putative cysteine desulphydrase (Schmidt, 1987). Recently, a cysteine desulphurylase, targeted to plastids has been cloned from Arabidopsis, with the capacity to form L-alanine and elemental sulphur from cysteine as the substrate (Léon et al., 2002). The cellular locations and regulation of different forms of this enzyme in plants which form S0 in response to pathogen attack would be of interest to evaluate the possible role of this gene family in S0 formation, as would the effect of gene disruption.
Novel components of a pathway leading to S0 accumulation, up-regulated following pathogen infection, may be identified by employing gene screening procedures relying on differential expression, such as differential display. These approaches are currently being applied to the tomato–Verticillium interaction. Biogenesis of constitutive S0 in crucifers may be by a different route, such as from the degradation of glucosinolates (Bones and Rossiter, 1996; Foo et al., 2000). It is intended to deploy a mutant screen approach (to identify by chemical analysis S0-deficient lines) as the first step to investigate S0 formation in Arabidopsis.
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Implications and applications |
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There is an irony that the discovery of this highly fungitoxic element in diverse plant species, coincides with sulphur deficiency as a major current nutrient disorder in Europe and other parts of the world (Schnug and Haneklaus, 1998
). The application of sulphur in various forms to crops is now advocated in order to compensate for this deficiency (Riley et al., 2000). Treatment with elemental sulphur, such as in the micronized form (Jolivet, 1993) may provide the added bonuses of fungicidal action and enhancement of innate host defences based on S-containing compounds and, in some species, S0 itself. S nutrition has been claimed to influence the resistance of Brassica napus and grapevine to fungal pathogens (Burandt et al., 2001). Genes for S0 biosynthesis are not only likely to be novel, but may be transferable to S0 non-producing species or, within a species able to accumulate S0, transferred to tissues other than xylem. S0 formation should be a valuable addition to the defence armoury of plants, because it is toxic to most fungal pathogens and a trait that pathogens are unlikely to overcome.
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Acknowledgements |
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Part of this work was funded by BBSRC and the initial discovery of S0 by the Brazilian Research Council (CNPq). We thank all collaborators, who are named as co-authors on our cited papers, and the many suppliers worldwide of microbial cultures, plant cultivars and infected material. The work was performed under DEFRA licence no. PHL 16/3694.
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References |
|---|
Beffa T, Pezet R, Turian G. 1987. Multiple-site inhibition by colloidal elemental sulfur (S0) of respiration by mitochondria from young dormant
spores of Phomopsis viticola. Physiologia Plantarum 69, 443–450.Berbee ML, Taylor JW. 1999. Fungal phylogeny. In: Oliver R, Schweizer M, eds. Molecular fungal biology. Cambridge, UK: Cambridge University Press, 21–77.
Bones AM, Rossiter JT. 1996. The myrosinase–glucosinolate system, its organization and biochemistry. Physiologia Plantarum 97, 194–208.[CrossRef]
Brune DC. 1995. Isolation and characterization of sulfur globule proteins from Chromatium vinosum and Thiocapsa roseopersicina. Archives of Microbiology 163, 391–399.[Web of Science][Medline]
Burandt P, Papenbrock J, Schmidt A, Bloem E, Haneklaus S, Schnug E. 2001. Genotypical differences in total sulfur contents and cysteine desulfhydrase activities in Brassica napus L. Phyton 41, 75–86.
Cooper RM. 1981. Pathogen-induced changes in host ultrastructure. In: Staples R, Toenniesen G, eds. Plant disease control: resistance and susceptibility. Chichester, UK: John Wiley & Sons, 105–142.
Cooper RM. 2000. Verticillium-host interactions: past achievements and future molecular prospects-an overview. In: Tjamos E, Rowe R, Heale J, Fravel D, eds. Advances in Verticillium research and disease management. St Paul, Minnesota: APS Press, 144–150.
Cooper RM, Resende MLV, Flood J, Rowan MG, Beale MH, Potter U. 1996. Detection and cellular localization of elemental sulphur in disease-resistant genotypes of Theobroma cacao. Nature 379, 159–162.[CrossRef]
Fahey JW, Zaleman AT, Talaly P. 2001. The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry 56, 50–51.
Foo HL, Grønning LM, Goodenough L, Bones AM, Danielsen BE, Whiting DA, Rossiter JT. 2000. Purification and characterization of epithiospecifier protein from Brassica napus: enzymic intramolecular sulphur addition within alkenyl thiohydroximates derived from alkenyl glucosinolate hydrolysis. FEBS Letters 468, 243–246.[CrossRef][Web of Science][Medline]
Forsyth W. 1802. A treatise on the culture and management of fruit trees. London, UK: Nichols and Son.
Gray GO, Knaff DB. 1982. The role of a cytochrome c-552 in the oxidation of sulfide in Chromatium vinosum. Biochimica et Biophysica Acta 680, 290–296.[CrossRef]
Hammond-Kosack KM, Jones JDG. 1996. Resistance gene-dependent plant defence responses. The Plant Cell 8, 1773–1791.[CrossRef][Web of Science][Medline]
Hassall KA. 1990. The biochemistry and uses of pesticides. Basingstoke, UK: Macmillan Press Ltd.
Hawkesford MJ, Wray JL. 2000. Molecular genetics of sulphur assimilation. Advances in Botanical Research 33, 159–223.[CrossRef]
Hazeu W, Batenburg-Van der Vegte WH, Bos P, Van der Pas RK, Kuenen JG. 1988. The production and utilization of intermediary elemental sulfur during the oxidation of reduced sulfur compounds by Thiobacillus ferrooxidans. Archives of Microbiology 150, 574–579.[CrossRef]
Hell R. 1997. Molecular physiology of plant sulfur metabolism. Planta 202, 138–148.[CrossRef][Web of Science][Medline]
Howarth JR, Fourcroy P, Davidian J-C, Smith FW, Hawkesford MJ. 2003. Cloning of two contrasting high-affinity sulfate transporters from tomato induced by low sulfate and infection by the vascular pathogen Verticillium dahliae. Planta 218, 58–64.[CrossRef][Web of Science][Medline]
Izac RR, Stierle DB, Sims JJ. 1982. Sulfur and N-methylformamide from the marine red alga Erythrophyllum delesserioides. Phytochemistry 21, 229.
Jolivet P. 1993. Elemental sulfur in agriculture. In: De Kok L, Stulen I, Rennenberg H, Brunold C, Rauser W, eds. Sulfur nutrition and assimilation in higher plants. The Hague, The Netherlands: SPB Academic Publishing, 193–206.
Joyard J, Fores E, Blée E, Douce R. 1988. Characterization of elemental sulfur in isolated intact spinach chloroplasts. Plant Physiology 88, 961–964.
Keen NT, Kennedy BW. 1974. Hydroxyphaseollin and related isoflavonoids in the hypersensitive resistance reaction of soybeans to Pseudomonas glycinea. Physiological Plant Pathology 4, 173–185.
Kömives T, Gullner G, Király Z. 1998. Role of glutathione and glutathione-related enzymes in response of plants to environmental stress. Annals of the New York Academy of Science 851, 251–258.[CrossRef][Web of Science]
Kraus F, Schäfer W, Schmidt A. 1984. Formation of elemental sulfur by Chlorella fusca during growth on L-cysteine ethylester. Plant Physiology 74, 176–182.
Kuhn PJ, Hargreaves JA. 1987. Antifungal substances from herbaceous plants. In: Pegg GF, Ayres PG, eds. Fungal infection of plants. Cambridge, UK: Cambridge University Press, 193–218.
Kylin H, Atuma S, Hovander L, Jensen S. 1994. Elemental sulphur (S8) in higher plants—biogenic or anthropogenic origin? Experientia 50, 80–85.[CrossRef]
Léon S, Touraine B, Briat J-F, Lobréaux S. 2002. The AtNFS2 gene from Arabidopsis thaliana encode a NifS-like plastidial desulphurase. Biochemical Journal 366, 557–564.[CrossRef][Web of Science][Medline]
Leustek T, Saito K. 1999. Sulfate transport and assimilation in plants. Plant Physiology 120, 637–643.
Mansfield JW. 2000. Antimicrobial compounds and resistance. The role of phytoalexins and phytoanticipins. In: Slusarenko A, Fraser R, van Loon L, eds. Mechanisms of resistance to plant diseases, Netherlands: Kluwer Academic Publishers, 325–370.
May MJ, Hammond-Kosack KE, Jones JDG. 1996. Involvement of reactive oxygen species, glutathione metabolism, and lipid peroxidation in the Cf-gene-dependent defense response of tomato cotyledons induced by race-specific elicitors of Cladosporium fulvum. Plant Physiology 110, 1367–1379.[Abstract]
Moriarty DJW, Nicholas DJD. 1970. Products of sulphide oxidation in extracts of Thiobacillus concretivorus. Biochimica et Biophysica Acta 197, 143–151.[Medline]
Mes JJ, Van Doorn AA, Wijbrandi J, Simons G, Cornelissen BJC, Haring MA. 2000. Expression of the Fusarium resistance gene I-2 colocalizes with the site of fungal containment. The Plant Journal 23, 183–193.[CrossRef][Web of Science][Medline]
Morrissey JP, Osbourn AE. 1999. Fungal resistance to plant antibiotics as a mechanism of pathogenesis. Microbiology and Molecular Biology Reviews 63, 708–724.
Pattaragulwanit K, Brune DC, Trüper HG, Dahl C. 1998. Molecular genetic evidence for extracytoplasmic localization of sulfur globules in Chromatium vinosum. Archives of Microbiology 169, 434–444.[CrossRef][Web of Science][Medline]
Pedras MSC, Khan AQ, Taylor JL. 1997. Phytoalexins from Brassicas: overcoming plants' defenses. In: Hedin P, Hollingworth R, Masler E, Miyamoto J, Thompson D, eds. Phytochemicals for pest control. ACS Symposium Series 658. Washington, USA: American Chemical Society, 155–166.
Pezet R, Pont V. 1977. Elemental sulfur: accumulation in different species of fungi. Science 196, 428–429.
Prange A, Arzberger I, Engemann C, Modrow H, Schumann O, Trüper HG, Steudel R, Dahl C, Hormes J. 1999. In situ analysis of sulfur in the sulfur globules of phototrophic sulfur bacteria by X-ray absorption near edge spectroscopy. Biochimica et Biophysica Acta 1428, 446–454.[Medline]
Reinartz M, Tschäpe J, Brüser T, Trüper HG, Dahl C. 1998. Sulfide oxidation in the phototrophic sulfur bacterium Chromatium vinosum. Archives of Microbiology 170, 59–68.[CrossRef][Web of Science][Medline]
Resende MLV, Flood J, Ramsden JD, Rowan MG, Beale MH, Cooper RM. 1996. Novel phytoalexins including elemental sulphur in the resistance of cocoa (Theobroma cacao L.) to Verticillium wilt (Verticillium dahliae Kleb.). Physiological and Molecular Plant Pathology 48, 347–359.[CrossRef]
Riley NG, Zhao FJ, McGrath SP. 2000. Availability of different forms of sulphur fertilizers to wheat and oilseed rape. Plant and Soil 222, 139–147.[CrossRef]
Schmidt A. 1987. D-cysteine desulfhydrase from spinach. Methods in Enzymology 143, 449–453.
Schmidt A, Jäger K. 1992. Open questions about sulfur metabolism in plants. Plant Molecular Biology 43, 325–349.
Schnug E, Haneklaus S. 1998. Diagnosis of sulfur nutrition. In: Schnug E, ed. Sulfur in agroecosystems. Dordrecht, The Netherlands: Kluwer Academic Publishers, 1–38.
Sharvelle EG. 1961. The nature and uses of modern fungicides. Minneapolis, Minnesota, USA: Burgess.
Smith FW, Ealing PM, Hawkesford MJ, Clarkson DT. 1995. Plant members of a family of sulfate transporters reveal functional subtypes. Proceedings of the National Academy of Sciences, USA 92, 9373–9377.
Steudel R. 1989. On the nature of the elemental sulfur produced by sulfur-oxidizing bacteria. In: Schlegel H, Bowien B, eds. Biology of autotrophic bacteria. Madison, Wisconsin, USA: Science Technology Publications, 289–303.
Steudel R, Holdt G, Nagorka R. 1986. On the autoxidation of aqueous sodium polysulfide. Z. Naturforsch 41b, 1519–1522.
Steudel R, Holdt G, Visscher PT, Van Gemerden H. 1990. Search for polythionates in cultures of Chromatium vinosum after sulfide incubation. Archives of Microbiology 153, 432–437.[CrossRef]
Takahashi H, Watanabe-Takahashi A, Smith FW, Blake-Kalff M, Hawkesford MJ, Saito K. 2000. The roles of three functional sulphate transporters involved in uptake and translocation of sulphate in Arabidopsis thaliana. The Plant Journal 23, 171–182.[CrossRef][Web of Science][Medline]
Thatcher RW, Streeter LR. 1925. The adherence to foliage of sulfur in fungicidal dusts and sprays. New York State Agricultural Experiment Station, Geneva, New York Technical Bulletin 116, 3–18.
Thomma BP, Nelissen I, Eggermont K, Broekaert WF. 1999. Deficiency in phytoalexin production causes enhanced susceptibility of Arabidopsis thaliana to the fungus Alternaria brassicicola. The Plant Journal 19, 163–171.[CrossRef][Web of Science][Medline]
Tweedy BG. 1981. Inorganic sulfur as a fungicide. Residue Reviews 78, 43–68.
Van Etten H, Temporini E, Wasmann C. 2001. Phytoalexin (and phytoanticipin) tolerance as a virulence trait: why is it not required by all pathogens? Physiological and Molecular Plant Pathology 59, 83–93.[CrossRef]
Visser JM, Robertson LA, Van Verseveld HW, Gijs Kuenen J. 1997. Sulfur production by obligately chemolithoautotrophic Thiobacillus species. Applied and Environmental Microbiology 63, 2300–2305.[Abstract]
Williams JS, Cooper RM. 2003. Elemental sulphur is produced by diverse plant families as a component of defence against fungal and bacterial pathogens. Physiological and Molecular Plant Pathology 63, 3–16.[CrossRef]
Williams JS, Cooper RM. 2004. The oldest fungicide and newest phytoalexin- reappraisal of the fungitoxicity of elemental sulphur. Plant Pathology (in press).
Williams JS, Hall SA, Hawkesford MJ, Beale MH, Cooper RM. 2002. Elemental sulfur and thiol accumulation in tomato and defense against a fungal vascular pathogen. Plant Physiology 128, 150–159.
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