The multiplicity of chemical structures of sulfur containing compounds, influenced in part by the element's several oxidation states, directly results in diverse modes of action for sulfur-containing natural products synthesized as secondary metabolites in plants. Sulfur-containing natural products constitute a formidable wall of defence against a wide range of pathogens and pests. Steady progress in the development of new technologies have advanced research in this area, helping to uncover the role of such important plant defence molecules like endogenously-released elemental sulphur, but also deepening current understanding of other better-studied compounds like the glucosinolates. As studies continue in this area, it is becoming increasingly evident that sulfur and sulfur compounds play far more important roles in plant defence than perhaps previously suspected.
TomlinCDS. (Ed.). (2000) The latest pesticide manual contains 812 chemicals as main entries, 236 (29%) of them are organic or inorganic sulfur compounds, The Pesticide Manual (British Crop Protection Council, Farnham, 12th ed. Cited in Lamberth C. (2004) Sulphur chemistry in crop protection. Journal of Sulfur Chemistry, 25, 39–62.
2.
GreweF. (1970) In Chemie der Pflanzenschutz- und Schädlingsbekämpfungsmittel, WeglerR. (Ed.). Springer, Berlin, Vol. 2, p. 3. Cited in LamberthC. (2004) Sulphur chemistry in crop protection. Journal of Sulfur Chemistry, 25, 39–62.
3.
TweedyBG. (1981) Inorganic sulfur as a fungicide. Residue Reviews, 78, 43–68.
4.
MansfieldJW. (2000) Antimicrobial compounds and resistance, the role of phytoalexins and phytoanticipins. In Mechanisms of Resistance to Plant Diseases. SlusarenkoAJ, FraserRSS, van LoonLC (Eds). Kluwer Academic Publishers, Dordrecht, The Netherlands. 325–370.
5.
BurowM, WittstockU, GershenzonJ. (2008) Sulfur-containing secondary metabolites and their role in plant defense. In Sulfur metabolism in phototrophic organisms, advances in photosynthesis and respiration. HellR, DahlC, KnaffD, LeustekT. (Eds). Springer, The Netherlands. Vol 27, 201–222.
6.
van EttenHD, MansfieldJW, BaileyJA, FarmerEE. (1994) Two classes of plant antibiotics: phytoalexins versus “phytoanticipins”. Plant Cell, 6, 1191–1192.
7.
AnkriS, MirelmanD. (1999) Antimicrobial properties of allicin from garlic. Microbes and Infection, 1, 125–129.
8.
DavisSR. (2005) An overview of the antifungal properties of allicin and its breakdown products; the possibility of a safe and effective antifungal prophylactic. Mycoses, 48, 95–100.
9.
WillsED. (1956) Enzyme inhibition by allicin, the active principle of garlic. Biochemical Journal, 63, 514–520.
10.
MironT, RabinkovA, MirelmanD, WilchekM, WeinerL. (2000) The mode of action of allicin: its ready permeability through phospholipid membranes may contribute to its biological activity. Biochemica et Biophysica Acta, 1463, 20–30.
11.
GruhlkeMCH, PortzD, StitzM, AnwarA, SchneiderT, JacobC, SchlaichNL, SlusarenkoAJ. (2010) Allicin disrupts the cell's electrochemical potential and induces apoptosis in yeast. Free Radical Biology & Medicine, 49, 1916–1924.
12.
HirschK, DanilenkoM, GiatJ, MironT, RabinkovA, WilchekM, MirelmanD, LevyJ, SharoniY. (2000) Effect of purified allicin, the major ingredient of freshly crushed garlic, on cancer cell proliferation. Nutrition and Cancer, 38, 245–254.
13.
OommenS, AntoRJ, SrinivasG, KarunagaranD. (2004) Allicin (from garlic) induces caspase-mediated apoptosis in cancer cells. European Journal of. Pharmacology, 485, 97–103.
14.
ParkSY, ChoSJ, KwonHC, LeeKR, RheeDK, PyoS. (2005) Caspase-independent cell death by allicin in human epithelial carcinoma cells: involvement of PKA. Cancer Letters, 224, 123–132.
15.
Bat-ChenW, GolanT, PeriI, LudmerZ, SchwartzB. (2010) Allicin purified from fresh garlic cloves induces apoptosis in colon cancer cells via Nrf2. Nutrition and Cancer, 62, 947–957.
16.
ZhangW, HaM, GongY, XuY, DongN, YuanY. (2010) Allicin induces apoptosis in gastric cancer cells through activation of both extrinsic and intrinsic pathways. Oncology Reports, 24, 1585–1592.
17.
MusahRA, HeQ, KubecR. (2009) Discovery and characterization of a novel lachrymatory factor synthase in Petiveria alliacea and its influence on alliinase-mediated formation of biologically active organosulfur compounds. Plant Physiology, 151, 1294–1303.
18.
MusahRA, HeQ, KubecR, JadhavA. (2009) Studies of a novel cysteine sulfoxide lyase from Petiveria alliacea: the first heteromeric alliinase. Plant Physiology, 151, 1304–1316.
19.
BenevidesPJ, YoungMC, GiesbrechtAM, RoqueNF, BolzaniVS. (2001) Antifungal polysulphides from Petiveria alliacea L. Phytochemistry, 57, 743–747.
KubecR, KimS, MusahRA. (2002) S-substituted cysteine derivatives and thiosulfinate formation in Petiveria alliacea–part II. Phytochemistry, 61, 675–680.
23.
KimS, KubecR, MusahRA. (2006) Antibacterial and antifungal activity of sulfur-containing compounds from Petiveria alliacea. Journal of Ethnopharmacology, 104, 188–192.
24.
DickeM. (1999) Are herbivore-induced plant volatiles reliable indicators of herbivore identity to foraging carnivorous arthropods?Entomologia Experimentalis et Applicata, 91, 131–142.
25.
KupieckiFP, VirtanenAI. (1960) Cleavage of alkyl cysteine sulphoxides by an enzyme in onion (Allium cepa). Acta Chemica Scandinavica, 14, 1913–1918.
26.
BlockE, WangS, ZhangZ, SheridanR. (2009) Unpublished results. In BlockE. (2010) Garlic and Other Alliums: The Lore and the Science. Royal Society of Chemistry, Cambridge, UK.
27.
ImaiS, TsugeN, TomotakeM, NagatomeY, SawadaH, NagataT, KumagaiH. (2002) An onion enzyme that makes the eyes to water. Nature, 419, 685.
28.
StotzHU, SawadaY, ShimadaY, HiraiMY, SasakiE, KrischkeM, BrownPD, SaitoK, KamiyaY. (2011) Role of camalexin, indole glucosinolates, and side chain modification of glucosinolate-derived isothiocyanates in defense of Arabidopsis against Sclerotinia sclerotiorum. The Plant Journal, 67, 81–93.
29.
TierensKFMJ, ThommaBPHJ, BrouwerM, SchmidtJr., KistnerK, PorzelA, Mauch-ManiB, CammueBPA, BroekaertWF. (2001) Study of the role of antimicrobial glucosinolate-derived isothiocyanates in resistance of arabidopsis to microbial pathogens. Plant Physiology, 125, 1688–1699.
30.
BonesAM, JohnTR. (1996) The myrosinase-glucosinolate system, its organisation and biochemistry. Physiologia Plantarum, 97, 194–208.
31.
KellyPJ, BonesA, RossiterJT. (1998) Sub-cellular immunolocalization of the glucosinolate sinigrin in seedlings of Brassica juncea. Planta, 206, 370–377.
32.
KruegerS, GiavaliscoP, KrallL, SteinhauserM-C, BüssisD, UsadelB, FlüggeU-I, FernieAR, WillmitzerL, SteinhauserD. (2011) A topological map of the compartmentalized Arabidopsis thaliana leaf metabolome. PLoS ONE, 6, e17806.
33.
FaheyJW, ZalcmannAT, TalalayP. (2001) The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry, 56, 5–51.
34.
von ReussSH, KönigWA. (2005) Olefinic isothiocyanates and iminodithiocarbonates from the liverwort Corsinia coriandrina. European Journal of Organic Chemistry, 1184–1188.
35.
SellamA, DongoA, GuillemetteT, HudhommeP, SimoneauP. (2007) Transcriptional responses to exposure to the brassicaceous defence metabolites camalexin and allyl-isothiocyanate in the necrotrophic fungus Alternaria brassicicola. Molecular Plant Pathology, 8, 195–208.
36.
MorrisseyJP, OsbournAE. (1999) Fungal resistance to plant antibiotics as a mechanism of pathogenesis. Microbiology and Molecular Biology Reviews, 63, 708–724.
37.
SellamA, PoupardP, SimoneauP. (2006) Molecular cloning of AbGst1 encoding a glutathione transferase differentially expressed during exposure of Alternaria brassicicola to isothiocyanates. FEMS Microbiology Letters, 258, 241–249.
HalkierBA, GershenzonJ. (2006) Biology and biochemistry of glucosinolates. Annual Review of Plant Biology, 57, 303–333.
40.
KawakishiS, KanekoT. (1987) Interaction of proteins with allyl isothiocyanate. Journal of Agricultural and Food Chemistry, 35, 85–88.
41.
MewisIZ, UlrichC, SchnitzlerWH. (2002) The role of glucosinolates and their hydrolysis products in oviposition and host-plant finding by cabbage webworm, Hellula undalis. Entomologia Experimentalis et Applicata, 105, 129–139.
42.
MilesCI, CampoMLd, RenwickJAA. (2005) Behavioral and chemosensory responses to a host recognition cue by larvae of Pieris rapae. Journal of Comparative Physiology. A, Neuroethology, sensory, neural, and behavioral physiology, 191, 147–155.
43.
WittstockU, AgerbirkN, StauberEJ, OlsenCE, HipplerM, Mitchell-OldsT, GershenzonJ, VogelH. (2004) Successful herbivore attack due to metabolic diversion of a plant chemical defense. Proceedings of the National Academy of Sciences of the U. S.A., 101, 4859–4864.
44.
SlootwegAFG. (1956) Rootrot of bulbs caused by Pratylenchus and Hoplolaimus spp. Nematologica, 1, 192–201.
45.
MarottiI, MarottiM, PiccagliaR, NastriA, GrandiS, DinelliG. (2010) Thiophene occurrence in different Tagetes species: agricultural biomasses as sources of biocidal substances. Journal of the Science of Food and Agriculture, 90, 1210–1217.
46.
HudsonJB, GrahamEA, RossiR, CarpitaA, NeriD, TowersGHN. (1993) Biological activities of terthiophenes and polyynes from the Asteraceae. Planta Medica, 59, 447–450.
47.
RomagnoliC, MaresD, FasuloMP, BruniA. (1994) Antifungal effects of α-terthienyl from Tagetes patula on five dermatophytes. Phytotherapy Research, 8, 332–336.
48.
ChampagneDE, ArnasonJT, PhilogeneBJR, MorandP, LamJ. (1986) Light-mediated allelochemical effects of naturally-occurring polyacetylenes and thiophenes from Asteraceae on herbivorous insects. Journal of Chemical Ecology, 12, 836–858.
49.
BakkerJ, GommersFJ, NieuwenhuisI, WynberglH. (297) Photoactivation of the nematicidal compound α-terthienyl from roots of marigolds (Tagetes species) Journal of Biological Chemistry, 254, 1841–1844.
50.
SteudelR. (297) The chemistry of organic polysulfanes R-Sn-R (n > 2). Chemical Reviews, 102, 3905–3945.
51.
DoeringM, BaLA, LilienthalN, NiccoC, SchererC, AbbasM, ZadaAAP, CoriatR, BurkholzT, WessjohannL, DiederichM, BatteuxF, HerlingM, Claus JacobC. (2010) Synthesis and selective anticancer activity of organochalcogen based redox catalysts. Journal of Medicinal Chemistry, 53, 6954–6963
52.
SchneiderT, BaLA, KhairanK, ZwergelC, BachND, BernhardtI, BrandtW, WessjohannL, DiederichM, JacobC. (2011) Interactions of polysulfanes with components of red blood cells. MedChemComm, 2, 196–200.
53.
MünchbergU, AnwarA, MecklenburgS, JacobC. (2007) Polysulfides as biologically active ingredients of garlic. Organic and Biomolecular Chemistry, 5, 1505–1518.
54.
BowmanGT, ClementJC, DavidsonDE, EswarakrishnanV, FieldL, HochJM, MusallamHA, PickRO, RavichandranR, SrivastavaPR. (1986) Potential antiradiation drugs containing no nitrogen, and related compounds. Chemico-Biological Interactions, 57, 161–174.
55.
HuangY, ChenSX, HoSH. (2000) Bioactivities of methyl allyl disulfide and diallyl trisulfide from essential oil of garlic to two species of stored-product pests, Sitophilus zeamais (Coleoptera: Curculionidae) and Tribolium castaneum (Coleoptera: Tenebrionidae). Journal of Economic Entomology, 93, 537–543.
56.
LiuP, GuoJ, LiuH, ChengY, WangB, LongC, DengB. (2009) Diallyl trisulfide (DATS) effectively induced apoptosis of postharvest disease Penicillium expansum of citrus. Annals of Microbiology, 59, 675–679.
57.
O'GaraEA, HillDJ, MaslinDJ. (2000) Activities of garlic oil, garlic powder, and their diallyl constituents against Helicobacter pylori. Applied and Environmental Microbiology, 66, 2269–2273.
58.
KyungKH, KimMH, ParkMS, KimYS. (2002) Alliinase-independent inhibition of Staphylococcus aureus B33 by heated garlic. Journal of Food Science, 67, 780–785.
59.
PaxtonJD. (1981) Phytoalexins- a working redefinition. Phytopathologische Zeitschrift, 101, 106–109.
60.
JolivetP. (1993) Elemental sulfur in agriculture. In Sulfur nutrition and assimilation in higher plants. De KokL, StulenI, RennenbergH, BrunoldC, RauserW. (Eds). SPB Academic Publishing, The Hague, The Netherlands, 193–206.
61.
WilliamsJS, CooperRM. (2004) The oldest fungicide and newest phytoalexin – a reappraisal of the fungitoxicity of elemental sulphur. Plant Pathology, 53, 263–279.
62.
CooperRM, WilliamsJS. (2004) Elemental sulphur as an induced antifungal substance in plant defence. Journal of Experimental Botany, 55, 1947–1953.
63.
CooperRM, ResendeMLV, FloodJ, RowanMG, BealeMH, PotterU. (1996) Detection and cellular localization of elemental sulphur in disease-resistant genotypes of Theobroma cacao. Nature, 379, 159–162
SharvelleEG. (1961) The Nature and Uses of Modern Fungicides. Burgess, Minneapolis, MN, USA.
66.
ReinartzM, TschäpeJ, BrüserT, TrüperHG, DahlC. (1998) Sulfide oxidation in the phototrophic sulfur bacterium Chromatium vinosum. Archives of Microbiology, 170, 59–68
67.
SchmidtTM, ArieliB, CohenY, PadanE, StrohlWR. (1987) Sulfur metabolism in Beggiatoa alba. Journal of Bacteriology, 169, 5466–5472.
68.
VisserJM, RobertsonLA, Van VerseveldHW, Gijs KuenenJ. (1997) Sulfur production by obligately chemolithoautotrophic Thiobacillus species. Applied and Environmental Microbiology, 63, 2300–2305
69.
CooperRM, WilliamsJS. (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.
70.
BeffaT. (1993) Inhibitory action of elemental sulphur (S°) on fungal spores. Canadian Journal of Microbiology, 39, 731–735.
71.
MillerLP, McCallanSEA, WeedRM. (1953) Quantitative studies on the role of hydrogen sulfide formation in the toxic action of sulfur to fungus spores. Contributions from Boyce Thompson Institute, 17, 151–171.
72.
McCallanSEA, WilcoxonF. (1931) The fungicidal action of sulphur. II. The production of hydrogen sulphide by sulphured leaves and spores and its toxicity to spores. Contributions from Boyce Thompson Institute, 3, 13–38.
BrowneLM, ConnKL, AyertWA, TewariJP. (1991) The camalexins: new phytoalexins produced in the leaves of Camelina sativa (Cruciferae). Tetrahedron, 47, 3909–3914.
77.
TsujiJ, HammerschmidtR, SomervilleSC. (1991) Purification and characterization of arabilexin a phytoalexin from Arabidopsis thaliana. Phytopathology, 81, 1224–1225.
78.
SlusarenkoAJ, Mauch-ManiB. (1991) Downy mildew of Arabidopsis thaliana caused by Peronospora parasitica: A model system for the investigation of the molecular biology of host-parasite interactions. In Advances in molecular genetics of plant-microbe interactions. HenneckeH, VermaDPS (Eds), Vol. 1, Kluwer Academic Publishers, Dordrecht, The Netherlands, 280–283.
79.
GlawischnigE, HansenBG, OlsenCE, HalkierBA. (2004) Camalexin is synthesized from indole-3-acetaldoxime, a key branching point between primary and secondary metabolism in Arabidopsis. Proceedings of the National Academy of Sciences of the U.S.A., 101, 8245–8250.
80.
TsujiJ, ZookM, SomervilleSC, LastRL, HammerschmidtR. (1993) Evidence that tryptophan is not a direct biosynthetic intermediate of camalexin in Arabidopsis thaliana. Physiological and Molecular Plant Pathology, 43, 221–229.
81.
ZookM, HammerschmidtR. (1997) Origin of the thiazole ring of camalexin, a phytoalexin from Arabidopsis thaliana. Plant Physiology, 113, 463–468.
82.
BurowM, WittstockU, GershenzonJ. (1998) Sulfur-containing secondary metabolites and their role in plant defense. In Advances in photosynthesis and respiration, Vol 27, Sulfur metabolism in phototrophic organisms. HellR, DahlC, KnaffDB, LeustekT (Eds). Springer, Dordrecht, The Netherlands, 211–212.
