Plant Molecular Biology

, Volume 42, Issue 1, pp 93–114 | Cite as

Myrosinase: gene family evolution and herbivore defense in Brassicaceae

  • Lars Rask
  • Erik Andréasson
  • Barbara Ekbom
  • Susanna Eriksson
  • Bo Pontoppidan
  • Johan Meijer
Article

Abstract

Glucosinolates are a category of secondary products present primarily in species of the order Capparales. When tissue is damaged, for example by herbivory, glucosinolates are degraded in a reaction catalyzed by thioglucosidases, denoted myrosinases, also present in these species. Thereby, toxic compounds such as nitriles, isothiocyanates, epithionitriles and thiocyanates are released. The glucosinolate-myrosinase system is generally believed to be part of the plant's defense against insects, and possibly also against pathogens. In this review, the evolution of the system and its impact on the interaction between plants and insects are discussed. Further, data suggesting additional functions in the defense against pathogens and in sulfur metabolism are reviewed.

cyanogenic glucosides glucosinolates myrosinase O-β-glucosidase plant–insect interaction 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Bak S, Nielsen HL, Halkier BA: The presence of CYP79 homologues in glucosinolate-producing plants shows evolutionary conservation of the enzymes in the conversion of amino acid to aldoxime in the biosynthesis of cyanogenic glucosides and glucosinolates. Plant Mol Biol 38: 725–734 (1998).Google Scholar
  2. 2.
    Barrett T, Suresh CG, Tolley SP, Dodson EJ, Hughes MA: The crystal structure of a cyanogenic β-glucosidase from white clover, a family 1 glycosyl hydrolase. Structure 3: 951–960 (1995).Google Scholar
  3. 3.
    Björkman R, Janson J-C: Studies on myrosinases. I. Purification and characterization of a myrosinase from white mustard seed (Sinapis alba L.). Biochim Biophys Acta 276: 508–518 (1972).Google Scholar
  4. 4.
    Björkman R, Lönnerdahl B: Studies on myrosinases. III. Enzymatic properties of myrosinases from Sinapis alba and Brassica napus seeds. Biochim Biophys Acta 327: 1221–1231 (1973).Google Scholar
  5. 5.
    Blau PA, Feeney P, Contardo L, Tobson DS: Allylglucosinolate and herbivorous caterpillars: a contrast in toxicity and tolerance. Science 200: 1296–1298 (1978).Google Scholar
  6. 6.
    Bodnaryk RP, Palanswamy P: Glucosinate levels in cotyledons of mustard, Brassica juncea, and rape, B. napus L., do not determine feeding rates of flea beetle, Phyllotreta cruciferae (Goeze). J Chem Ecol 16: 2735–2746 (1990).Google Scholar
  7. 7.
    Bones A, Iversen T-H: Myrosin cells and myrosinase. Isr J Bot 34: 351–375 (1985).Google Scholar
  8. 8.
    Bones A, Slupphaug G: Purification, characterization and partial amino acid sequencing of β-thioglucosidase from Brassica napus L. J Plant Physiol 134: 722–729 (1989).Google Scholar
  9. 9.
    Bones A: Distribution of β-thioglucosidase activity in intact plants, cell and tissue cultures and regenerant plants of Brassica napus L. Exp Bot 41: 737–744 (1990).Google Scholar
  10. 10.
    Bones AM, Visvalingam S, Thangstad OP: Sulphate can induce differential expression of thioglucoside glucohydrolases (myrosinases). Planta 193: 558–566 (1994).Google Scholar
  11. 11.
    Bouchereau A, Clossais-Besnard N, Bensaoud A, Leport L, Renard M: Water stress effects on rapeseed quality. Eur J Agron 5: 19–30 (1996).Google Scholar
  12. 12.
    Burmeister WP, Cottaz S, Driguez H, Iori R, Palmieri S, Henrissat B: The crystal structures of Sinapis alba myrosinase and a covalent glycosyl-enzyme intermediate provide insights into the substrate recognition and active-site machinery of an S-glycosidase. Structure 5: 663–675 (1997).Google Scholar
  13. 13.
    Bussy A: Sur la formation de l'huile essentielle de moutarde. J Pharm 27: 464–471 (1840).Google Scholar
  14. 14.
    Cavell AC, Lydiate DJ, Parkin IA, Dean C, Trick M: Collinearity between a 30-centimorgan segment of Arabidopsis thaliana chromosome 4 and duplicated regions within the Brassica napus genome. Genome 41: 62–69 (1998).Google Scholar
  15. 15.
    Chadchawan S, Bishop J, Thangstad OP, Bones AM, Mitchell-Olds T, Bradley D: Arabidopsis cDNA sequence encoding myrosinase. Plant Physiol 103: 671–672 (1993).Google Scholar
  16. 16.
    Chew FS: Biological effects of glucosinolates. In: Cutler HG, Biologically Active Natural Products for Potential Use in Agriculture, pp. 155–181. American Chemical Society, Washington (1988).Google Scholar
  17. 17.
    Chew FS: Searching for defensive chemistry in the Cruciferae, or do glucosinolates always control interactions of cruciferae with their potential herbivores and symbionts? No! In: KC Spencer (ed), Chemical Mediation of Coevolution, pp. 81–112. Academic Press, San Diego, CA (1988).Google Scholar
  18. 18.
    Chew FS, Renwick JAA: Host plant choice in Pieris butterflies. In: Cardé RT, Bell WJ (eds), Chemical Ecology of Insects 2, pp. 214–240. Chapman & Hall, New York (1995).Google Scholar
  19. 19.
    Clossais-Besnard N, Larher F: Physiological role of glucosinolates in Brassica napus. Concentration and distribution pattern of glucosinolates among plant organs during a complete life cycle. J Sci Food Agric 56: 25–38 (1991).Google Scholar
  20. 20.
    Cottaz S, Henrissat R, Driguez H: Mechanism-based inhibition and stereochemistry of glucosinolate hydrolysis by myrosinase. Biochemistry 35: 15256–15259 (1996).Google Scholar
  21. 21.
    Cronquist A: The Evolution and Classification of Flowering Plants, 2nd ed. New York Botanical Garden, New York (1988).Google Scholar
  22. 22.
    Dahlgren R: A commentary on a diagrammatic presentation of the angiosperms in relation to the distribution of character states. Plant Syst Evol, Suppl 1: 253–283 (1977).Google Scholar
  23. 23.
    Dahlgren R, Rosendal-Jensen S, Nielsen BJ: A revised classification of the angiosperms with comments on correlation between chemical and other characters. In: Young DA, Seigler DS (eds), Phytochemistry and Angiosperm Phylogeny, pp. 149–202. Praeger, New York (1981).Google Scholar
  24. 24.
    Davies G, Henrissat B: Structures and mechanisms of glycosyl transferases. Curr Biol 3: 853–859 (1995).Google Scholar
  25. 25.
    Dawson GW, Griffiths DC, Pickett JA, Wadhams LJ, Woodcock CM: Plant-derived synergists of alarm pheromone from turnip aphid Lipaphis (Hyadaphis) erysimi (Homoptera, Aphididae). J Chem Ecol 13: 166–1671 (1987).Google Scholar
  26. 26.
    Doughty KJ, Porter AJR, Morton AM, Kiddle G, Bock CH, Wallsgrove R: Variation in the glucosinolate content of oilseed rape (Brassica napus L.) leaves. II. Response to infection by Alternaria brassicae (Berk.). Sacc. Ann Appl Biol 118: 469–477 (1991).Google Scholar
  27. 27.
    Doughty KJ, Kiddle GA, Morton AM, Pye BJ, Wallsgrove RM, Pickett JA: Selective induction of glucosinolates in oilseed rape leaves by methyl jasmonate. Phytochemistry 38: 347–350 (1995).Google Scholar
  28. 28.
    Doughty KJ, Blight MM, Bock CH, Fieldsend JK, Pickett JA: Release of alkenyl isothiocyanates and other volatiles from Brassica rapa seedlings during infection by Alternaria brassicae. Phytochemistry 43: 371–374 (1996).Google Scholar
  29. 29.
    Durham PL, Poulton JE: Enzymatic properties of purified myrosinase from Lepidium sativum seedlings. Z Naturforsch 45: 173–178 (1990).Google Scholar
  30. 30.
    Ekbom B: Clutch size and larval performance of pollen beetles on different host plants. Oikos 83: 56–64 (1998).Google Scholar
  31. 31.
    Ettlinger MG, Lundeen AJ: The structures of sinigrin and sinalbin: an enzymatic rearrangement. J Am Chem Soc 78: 4172–4173 (1956).Google Scholar
  32. 32.
    Ettlinger MG, Kjaer A: Sulfur compounds in plants. Rec Adv Phytochem 1: 49–144 (1968).Google Scholar
  33. 33.
    Fagerström T, Larsson S, Tenow O: On optimal defence in plants. Funct Ecol 1:73–81 (1987).Google Scholar
  34. 34.
    Falk A, Xue J, Lenman M, Rask L: Sequence of a cDNA clone encoding the enzyme myrosinase and expression of myrosinase in different tissues of Brassica napus. Plant Sci 83: 181–186 (1992).Google Scholar
  35. 35.
    Falk A, Ek B, Rask L: Characterization of a new myrosinase in Brassica napus. Plant Mol Biol 27: 863–874 (1995).Google Scholar
  36. 36.
    Falk A, Rask L: Expression of a zeatin-O-glucosidedegrading β-glucosidase in Brassica napus. Plant Physiol 108: 1369–1377 (1995).Google Scholar
  37. 37.
    Falk A, Taipalensuu J, Rask L: Characterization of myrosinase-binding protein. Planta 195: 387–395 (1995).Google Scholar
  38. 38.
    Fenwick R, Heaney RK, Mullin WJ: Glucosinolates and their breakdown products in food and food plants. CRC Crit Rev Food Sci Nutr 18: 123–201 (1983).Google Scholar
  39. 39.
    Fieldsend J, Milford GFJ: Changes in glucosinolates during crop development in single-and double-low genotypes of winter oilseed rape (Brassica napus). I. Production and distribution in vegetative tissue and developing pods during development and potential role in recycling of sulphur within the crop. Ann Appl Biol 124: 531–542 (1994).Google Scholar
  40. 40.
    Gershenzon J: The cost of plant chemical defense against herbivory: a biochemical perspective. In: Bernays E (ed), Insect-Plant Interactions, vol. 5, pp. 105–173. CRC Press, Boca Raton, FL (1994).Google Scholar
  41. 41.
    Geshi N, Andréasson E, Meijer J, Rask L, Brandt A: Myrosinase and myrosinase-binding proteins are co-localized in grains of myrosin cells in cotyledon of Brassica napus L. seedlings. Plant Phys Biochem 36: 583–590 (1998).Google Scholar
  42. 42.
    Geshi N, Brandt A: Two jasmonate inducible myrosinasebinding proteins from Brassica napus L. seedlings with homology to jacalin. Planta 204: 295–304 (1998).Google Scholar
  43. 43.
    Giamoustaris A, Mithen R: The effect of modifying the glucosinolate content of leaves on oilseed rape (Brassica napus ssp. oleifera) on its interaction with specialist and generalist pests. Ann Appl Biol 126: 347–363 (1995).Google Scholar
  44. 44.
    Giamoustaris A, Mithen R: Glucosinolates and disease resistance in oilseed rape (Brassica napus ssp oleifera). Plant Pathol 46: 271–275 (1997).Google Scholar
  45. 45.
    Greenhalgh JG, Mithel N: The involvement of flavour volatile in the resistance to downy mildew of wild and cultivated form of Brassica oleracea. New Phytol 77: 391–398 (1976).Google Scholar
  46. 46.
    Grob K, Matile P: Vacuolar location of glucosinolates in horseradish root cells. Plant Sci Lett 14: 327–335 (1979).Google Scholar
  47. 47.
    Groot Wassink JWD, Reed DW, Kolenovsky AD: Immunopurification and immunocharacterization of the glucosinolate biosynthetic enzyme thiohydroximate S-glucosyltransferase. Plant Physiol 105: 425–433 (1994).Google Scholar
  48. 48.
    Halkier BA, Sibbesen O, Koch B, Mø ller BL: Characterization of cytochrome P450tyr, a multifunctional haemthiolate N-hydroxylase involved in the biosynthesis of the cyanogenic glucoside dhurrin. Drug Metabol Drug Interact 12: 285–297 (1995).Google Scholar
  49. 49.
    Hartman T: Diversity and variability of plant secondary metabolism: a mechanistic view. Entomol Exp Appl 80: 177–188 (1996).Google Scholar
  50. 50.
    Haughn GW, Davin L, Giblin M, Underhill EW: Biochemical genetics of plant secondary metabolites in Arabidopsis thaliana. The glucosinolates. Plant Physiol 97: 217–226 (1991).Google Scholar
  51. 51.
    Heinricher E: Ñber Eiweisstoffe führende Idioblasten bei einigen Cruciferen. Ber Dtsch Bot Ges II: 463–466 (1884).Google Scholar
  52. 52.
    Helmlinger J, Rausch T, Hilgenberg W: Localization of newly synthesized indole-3-methylglucosinolate (= glucobrassin) in vacuoles in horseradish (Armoracia rusticana). Physiol Plant 58: 302–310 (1983).Google Scholar
  53. 53.
    Henrissat B: A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J 280: 309–316 (1991).Google Scholar
  54. 54.
    Henrissat B, Bairoch A: Updating the sequence-based classification of glycosyl hydrolases. Biochem J 316: 695–696 (1996).Google Scholar
  55. 55.
    Höglund A-S, Lenman M, Falk A, Rask L: Distribution of myrosinase in rapeseed tissues. Plant Physiol 95: 213–221 (1991).Google Scholar
  56. 56.
    Höglund A-S, Lenman M, Rask L: Myrosinase is localized to the interior of myrosin grains and is not associated to the surrounding tonoplast membrane. Plant Sci 85: 165–170 (1992).Google Scholar
  57. 57.
    Holmes MRJ: Nutrition of the Oilseed Rape Crop. Applied Science Publishers, London (1980).Google Scholar
  58. 58.
    James DC, Rossiter JT: Development and characteristics of myrosinase in Brassica napus during early seedling growth. Physiol Plant 82: 163–170 (1991).Google Scholar
  59. 59.
    Jensen CR, Mogensen VO, Mortensen G, Fieldsend JK, Milford GFJ, Andersen MN, Thage JH: Seed glucosinolate, oil and protein contents of field-grown rape (Brassica napus L.) affected by soil drying and evaporative demand. Field Crop Res 47: 93–105 (1996).Google Scholar
  60. 60.
    Kater MM: Structure, function and expression of plant and bacterial enoyl-ACP reductase genes. Thesis, Vrije Universiteit, Amsterdam (1994).Google Scholar
  61. 61.
    Kelly PJ, Bones A, Rossiter JT: Sub-cellular immunolocalization of the glucosinolate sinigrin in seedlings of Brassica juncea. Planta 206: 370–377 (1998).Google Scholar
  62. 62.
    Kiddle GA, Kevin JD, Wallsgrow RM: Salicylic acidinduced accumulation of glucosinolates in oilseed rape (Brassica napus) leaves. J Exp Bot 45: 1343–1346 (1994).Google Scholar
  63. 63.
    Kjaer A: The natural distribution of glucosinolates: a uniform group of sulfur-containing glucosides. In: Bendz G, Santesson J (eds), Chemistry in Botanical Classification, pp. 229–234. Academic Press, New York (1973).Google Scholar
  64. 64.
    Kjaer A: Glucosinolates in the Cruciferae. In: Vaughan JG, MacLeod AJ, Jones BMG (eds), The Biology and Chemistry of the Cruciferae, pp. 207–219. Academic Press, London (1976).Google Scholar
  65. 65.
    Koch B, Nielsen VS, Halkier BA, Olsen CE, Mø ller BL: The biosynthesis of cyanogenic glucosides in seedlings of cassava (Manihot esculenta Crantz). Arch Biochem Biophys 292: 141–150 (1992).Google Scholar
  66. 66.
    Kozlowska HJ, Nowak H, Nowak J: Characterization of myrosinase in Polish varieties of rapeseed. J Sci Food Agric 34: 1171–1178 (1983).Google Scholar
  67. 67.
    Lenman M, Rödin J, Josefsson L-G, Rask L: Immunological characterization of rapeseed myrosinase. Eur J Biochem 194: 747–753 (1990).Google Scholar
  68. 68.
    Lenman M, Falk A, Rödin J, Höglund A-S, Ek B, Rask L: Differential expression of myrosinase gene families. Plant Physiol 103: 703–711 (1993).Google Scholar
  69. 69.
    Lenman M, Falk A, Xue J, Rask L: Characterization of a Brassica napus pseudogene: myrosinases are members of the BGA family of β-glycosidases. Plant Mol Biol 21: 463–474 (1993).Google Scholar
  70. 70.
    Lönnerdal B, Janson J-C: Studies on myrosinase. II. Purifi-cation and characterization of a myrosinase from rapeseed (Brassica napus L.). Biochim Biophys Acta 315: 421–429 (1973).Google Scholar
  71. 71.
    Louda S. Mole S: Glucosinolates, chemistry and ecology. In: Rosenthal GA, Berenbaum MR (eds), Herbivores. Their Interactions with Secondary Plant Metabolites, 2nd ed., vol. 1, pp. 123–164. Academic Press, San Diego, CA (1991).Google Scholar
  72. 72.
    Lüthy B, Matile P: The mustard oil bomb: rectified analysis of the subcellular organisation of the myrosinase system. Biochem Physiol Pflanzen 179: 5–12 (1984).Google Scholar
  73. 73.
    Machlin S, Mitchell-Olds T, Bradley D: Sequence of a Brassica campestris myrosinase gene. Plant Physiol 102: 1359–1360 (1993).Google Scholar
  74. 74.
    Malboobi MA, Lefebvre DD: A phosphate-starvation inducible β-glucosidase gene (psr3.2) isolated from Arabidop sis thaliana is a member of a distinct subfamily of the BGA family. Plant Mol Biol 34: 57–68 (1997).Google Scholar
  75. 75.
    Markert CL, Möller F: Multiple forms of enzymes: tissue, ontogenetic and species specific patterns. Proc Natl Acad Sci USA 45: 753–763 (1959).Google Scholar
  76. 76.
    Mattiacci L, Dicke M, Posthumus MA: Induction of parasitoid attracting synomone in brussels sprouts plants by feeding of Pieris brassicae larvae: role of mechanical damage and herbivore elicitor. J Chem Ecol 20: 2229–2247 (1994).Google Scholar
  77. 77.
    Mauricio R, Rausher MD: Experimental manipulation of putative selective agents provides evidence for the role of natural enemies in the evolution of plant defense. Evolution 51: 1435–1444 (1997).Google Scholar
  78. 78.
    Mauricio R: Costs of resistance to natural enemies in field populations of the annual plant Arabidopsis thaliana. Am Natural 151: 20–28 (1998).Google Scholar
  79. 79.
    McGibbon DB, Allison RM: A glucosinolase system in the aphid Brevicoryne brassicae. NZ J Sci 11: 440–446 (1968).Google Scholar
  80. 80.
    McGregor DI: Glucosinolate content of developing rapeseed (Brassica napus L. Midas) seedlings. Can J Plant Sci 68: 367–380 (1988).Google Scholar
  81. 81.
    Milford GFJ, Fieldsend JK, Porter AJR, Rawlinson CJ, Evans EJ, Bilsborrow P: Changes in glucosinolate concentrations during the vegetative growth of single and double low cultivars of winter oilseed rape. Asp Appl Biol 23: 83–90 (1989).Google Scholar
  82. 82.
    Mithen RF, Lewis BG, Fenwick GR: In vitro activity of glucosinates and their products against Leptoshaeria maculans. Trans Br Mycol Soc 87: 433–440 (1986).Google Scholar
  83. 83.
    Mithen RF, Magrath R: Glucosinolates and resistance to Leptosphaeria maculans in wild and cultivated Brassica species. Plant Breed 108: 60–68 (1992).Google Scholar
  84. 84.
    Mithen R, Raybould AF, Giamoustaris A: Divergent selection for secondary metabolites between wild populations of Brassica oleracea and its implication for plant-herbivore interactions. Heredity 75: 472–484 (1995).Google Scholar
  85. 85.
    Nicholas KB, Nicholas HB Jr: GeneDoc: a tool for editing and annotating multiple sequence alignments. Distributed by the authors. http://www.cris.com/ketchup/genedoc.shtml (1997).Google Scholar
  86. 86.
    Nielsen JK: Crucifer-feeding Chrysomelidae: mechanisms of host plant finding and acceptance. In: Jolivet P, Petitpierre E, Hsiao TH (eds), Biology of Chrysomelidae, pp. 25–40. Kluwer Academic Publishers, Dordrecht, Netherlands (1988).Google Scholar
  87. 87.
    Ohtsuru M, Hata T: The interaction of L-ascorbic acid with the active center of myrosinase. Biochim Biophys Acta 567: 384–379 (1979).Google Scholar
  88. 88.
    Pagè s RDM: TREEVIEW: an application to display phylogenetic trees on personal computers. Comp Appl Biosci 12: 357–358 (1996).Google Scholar
  89. 89.
    Phelan JR, Vaughan JG: Myrosinase in Sinapis alba L. J Exp Bot 31: 1425–1433 (1980).Google Scholar
  90. 90.
    Pihakaski K, Pihakaski S: Myrosinase in Brassicaceae (Cruciferae). II. Myrosinase activity in different organs of Sinapis alba. J Exp Bot 29: 335–345 (1978).Google Scholar
  91. 91.
    Porter AJR, Morton AM, Kiddle G, Doughty KJ, Wallsgrove RM: Variation in the glucosinolate content of oilseed rape (Brassica napus L.). I. Effects of leaf age and position. Ann Appl Biol 118: 461–467 (1991).Google Scholar
  92. 92.
    Poulton JE: Cyanogenesis in plants. Plant Physiol 94: 401–405 (1990).Google Scholar
  93. 93.
    Poulton JE, Mø ller BL: Glucosinolates. Meth Plant Biochem 9: 209–237 (1993).Google Scholar
  94. 94.
    Read DP, Feeny PP, Root RB: Habitat selection by the aphid parasite Diaeretiella rapae (Hymenoptera: Braconidae) and hyperparasite Charips brassicae (Hymenoptera: Cynipidae). Can Entomol 102: 1567–1578 (1970).Google Scholar
  95. 95.
    Reed DW, Davin L, Jain JC, DeLuca V, Nelson L, Underhill EW: Purification and properties of UDPglucose: thiohydroximate glucosyltransferase from Brassica napus L. seedlings. Arch Biochem Biophys 305: 526–532 (1993).Google Scholar
  96. 96.
    Renwick JAA, Radke CD, Saqchdev-Gupta K, Städler E: Leaf surface chemical stimulating oviposition by Pieris rapae (Lepidoptera: Pieridae). Chemoecology 3: 33–38 (1992).Google Scholar
  97. 97.
    Robiquet PJ, Boutron F: Sur la semence de moutarde. J Pharm Chim 17: 279–282 (1831).Google Scholar
  98. 98.
    Rodman J: A taxonomic analysis of glucosinolate-producing plants, Part 1. Phenetics. Syst Bot 16: 598–618 (1991).Google Scholar
  99. 99.
    Rodman J: A taxonomic analysis of glucosinolate-producing plants, Part 2. Cladistics. Syst Bot 16: 619–629 (1991).Google Scholar
  100. 100.
    Rodman J, Price RA, Karol K, Conti E, Sytsma KJ, Palmer JD: Nucleotide sequences of the rbcL gene indicate monophyly of mustard oil plants. Ann Miss Bot Gard 80: 686–699 (1993).Google Scholar
  101. 101.
    Rodman JE, Soltis PS, Soltis DE, Sytsma KJ, Karol KG: Parallel evolution of glucosinolate biosynthesis inferred from congruent nuclear and plastid gene phylogenies. Am J Bot 85: 997–1006 (1998).Google Scholar
  102. 102.
    Roessingh P, Städler E, Fenwick GR, Lewis JA, Nielsen JK, Hurter J, Ramp T: Oviposition and tarsal chemoreceptors of the cabbage root fly are stimulated by glucosinolates and host plant extracts. Entomol Exp Appl 65: 267–282 (1994).Google Scholar
  103. 103.
    Rouxel T, Kollman A, Boulidard L, Mithen R: Abiotic elicitation of indole phytoalexins and resistance to Leptosphaeria maculans within Brassicaceae. Planta 184: 271–278 (1991).Google Scholar
  104. 104.
    Sarwar M, Kirkegaard, JA, Wong, PTW, Desmarchelier JM: Biofumigation potential of brassicas. III. In vitro toxicity of isothiocyanates to soil-borne fungal pathogens. Plant Soil 201: 103–112 (1998).Google Scholar
  105. 105.
    Saupe SG: Cyanogenic compounds and angiosperm phylogeny. In: Young DA, Seigler DS (eds), Phytochemistry and Angiosperm Phylogeny, pp. 80–116. Praeger, New York (1981).Google Scholar
  106. 106.
    Schnug E: Double low rapeseed in West Germany: sulphur metabolism and glucosinolate levels. Asp Appl Biol 23: 67–82 (1989).Google Scholar
  107. 107.
    Schnug E: Sulphur nutrition and quality of of vegetables. Sulphur Agric 14: 3–7 (1990).Google Scholar
  108. 108.
    Schnug E, Evans E:Monitoring the sulphur deficiency symptoms in Brassica napus. Phyton 32: 53–56 (1992).Google Scholar
  109. 109.
    Schnug E, Haneklaus S, Borchers A, Polle A: Relations between sulphur supply and glutathione and ascorbate concentrations in Brassica napus. Z Pflanzenernähr Bodenk 158: 7–69 (1995).Google Scholar
  110. 110.
    Schoonhoven LM, Jermy T, van Loon JJA: Insect-Plant Biology. Chapman & Hall, London (1998).Google Scholar
  111. 111.
    Selmar D, Lieberei R, Biehl B, Voigt J: Hevea linamarase: a nonspecific β-glycosidase. Plant Physiol 83: 557–563 (1987).Google Scholar
  112. 112.
    Selmar D, Lieberei R, Biehl B: Mobilization and utilization of cyanogenic glycosides; the linustatin pathway. Plant Physiol 86: 711–716 (1988).Google Scholar
  113. 113.
    Sexton AC, Howlett BJ: Characterization of a gene encoding cyanide hydratase in Leptosphaeria maculans, the causal agent of blackleg disease of oilseed Brassicas. 7th International Congress of Plant Pathology, Edinburgh, UK, Abstract 1.8.45 (1998).Google Scholar
  114. 114.
    Sharma M: Ontogenic studies of the myrosin idioblasts in Brassica napus and Brassica montana. Bot Tidskr 66: 51–59 (1971).Google Scholar
  115. 115.
    Sibbesen O, Koch B, Halkier BA, Mø ller BL: Cytochrome P450tyr is a multifunctional heme-thiolate enzyme catalyzing the conversion of L-tyrosine to phydroxyphenylacetaldehyde oxime in the biosynthesis of the cyanogenic glucoside dhurrin in Sorghum bicolor (L.) Moench. J Biol Chem 270: 3506–3511 (1995).Google Scholar
  116. 116.
    Siemens DH, Mitchell-Olds T: Evolution of pest-induced defenses in Brassica plants: tests of theory. Ecology 79: 632–646 (1998).Google Scholar
  117. 117.
    Simmonds MSJ, Blaney WM, Mithen R, Birch ANE, Lewis J: Behavioural and chemosensory responses of the turnip root fly (Delia floralis) to glucosinolates. Entomol Exp Appl 71: 41–57 (1995).Google Scholar
  118. 118.
    Simms EL, Rausher MD: Costs and benefits of plant resistance to herbivory. Am Natural 130: 570–581 (1987).Google Scholar
  119. 119.
    Sinnott ML: Catalytic mechanisms of enzymic glycosyl transfer. Chem Rev 90: 1171–1202 (1990).Google Scholar
  120. 120.
    Sø rensen H: Glucosinolates: structure, properties, function. In: Shadidi F (ed.), Canola and Rapeseed, pp. 149–172. AVI Book, New York (1990).Google Scholar
  121. 121.
    Taipalensuu J, Lundgren S, Rask L: No evidence for the ascorbic activation site of myrosinase being encoded by end of exon 9, beginning of exon 10. Hereditas 122: 95–98 (1995).Google Scholar
  122. 122.
    Taipalensuu J, Falk A, Rask L: A wound-and methyl jasmonate-inducible transcript coding for a myrosinaseassociated protein with similarities to an early nodulin. Plant Physiol 110: 483–491 (1996).Google Scholar
  123. 123.
    Taipalensuu J, Andréasson E, Eriksson S, Rask L: Regulation of the wound-induced myrosinase-associated protein transcript in Brassica napus plants. Eur J Biochem 247: 963–971 (1997).Google Scholar
  124. 124.
    Taipalensuu J, Eriksson S, Rask L: The myrosinase-binding protein from Brassica napus seeds possesses lectin activity and has a highly similar vegetatively expressed woundinducible counterpart. Eur J Biochem 250: 680–688 (1997).Google Scholar
  125. 125.
    Taipalensuu J, Falk A, Ek B, Rask L: Myrosinase-binding proteins are derived from a large wound-inducible and repetitive transcript. Eur J Biochem 243: 605–611 (1997).Google Scholar
  126. 126.
    Tani N, Ohtsuru M, Hata T: Purification and general characteristics of bacterial myrosinase produced by Enterobacter cloacae. Agric Biol Chem 38: 1623–1630 (1974).Google Scholar
  127. 127.
    Thangstad OP, Iversen T-H, Slupphaug G, Bones A: Immunocytochemical localization of myrosinase in Brassica napus L. Planta 180: 245–248 (1990).Google Scholar
  128. 128.
    Thangstad OP, Evjen K, Bones A: Immunogold-EMlocalization of myrosinase in Brassicaceae. Protoplasma 161: 85–93 (1991).Google Scholar
  129. 129.
    Thangstad OP, Winge P, Husbye H, Bones A: The myrosinase (thioglucoside glucohydrolase) gene family in Brassicaceae. Plant Mol Biol 23: 511–524 (1993).Google Scholar
  130. 130.
    Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG: The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res 25: 4876–4882 (1997).Google Scholar
  131. 131.
    Thompson JN: The Coevolutionary Process. University of Chicago Press, Chicago, IL (1994).Google Scholar
  132. 132.
    Tookey HL, VanEtten CH, Daxenbichler ME: Glucosinolates. In: Liner IE (ed), Toxic Constitutents of Plant Foodstuffs, 2nd ed., pp. 103–142. Academic Press, New York (1980).Google Scholar
  133. 133.
    Troelstra C, Hesen W, Bootsma D, Hoeijmakers JHJ: Structure and expression of the excision repair gene ERCC6 involved in the human disorder Cockayne's syndrome group B. Nucl Acids Res 21: 419–426 (1993).Google Scholar
  134. 134.
    van der Kooij TAW, de Kok LJ, Haneklaus S, Schnug E: Uptake and metabolism of sulphur dioxide by Arabidopsis thaliana. New Phytol 135: 101–107 (1997).Google Scholar
  135. 135.
    van der Meijden E: Plant defence, an evolutionary dilemma: contrasting effects of (specialist and generalist) herbivores and natural enemies. Entomol Exp Appl 80: 307–310 (1996).Google Scholar
  136. 136.
    van Etten HD, Mansfield JW, Bailey JA, Farmer EE: Two classes of plant antibiotics: phytoalexins versus 'phytoanticipins'. Plant Cell 6: 1191–1192 (1994).Google Scholar
  137. 137.
    van Loon JJ, Blaakmeer A, Griepink FC, van Beek TA, Schoonhoven LM, de Groot A: Leaf surface compound from Brassica oleracea (Cruciferae) induces oviposition by Pieris brassicae (Lepidoptera: Pieridae). Chemoecology 3: 39–44 (1992).Google Scholar
  138. 138.
    Verschaffelt E: The cause determining the selection of food in some herbivorous insects. Proc Royal Acad Amsterdam 13: 536–542 (1910).Google Scholar
  139. 139.
    Vincent C, Stewart RK: Effect of allyl isothiocyanate on field behavior of crucifer- feeding flea beetles (Colepotera: Chrysomelidae). J Chem Ecol 10: 33–39 (1984).Google Scholar
  140. 140.
    Wallsgrove RM, Bennet RN, Doughty KJ, Schrijvers S, Kiddle G: Glucosinolate metabolism in diseased plants. Asp Appl Biol 42: 251–256 (1995).Google Scholar
  141. 141.
    Werker E, Vaughan JG: Ontogeny and distribution of myrosin cells in the shoot of Sinapis alba L. A light-and electron microscope study. Isr J Bot 25: 140–151 (1976).Google Scholar
  142. 142.
    Xue J, Lenman M, Falk A, Rask L: The glucosinolatedegrading enzyme myrosinase in Brassicaceae is encoded by a gene family. Plant Mol Biol 18: 387–398 (1992).Google Scholar
  143. 143.
    Xue J, Jø rgensen M, Pihlgren, U, Rask L: The myrosinase gene family in Arabidopsis thaliana: gene organization, expression and evolution. Plant Mol Biol 27: 911–922 (1995).Google Scholar
  144. 144.
    Xue J, Pihlgren U, Rask L: Temporal, cell-specific, and tissue-preferential expression of myrosinase genes during embryo and seedling development in Sinapis alba. Planta 191: 95–101 (1995).Google Scholar
  145. 145.
    Xue J, Rask L: The unusual 5' splicing border GC is used in myrosinase genes of the Brassicaceae. Plant Mol Biol 29: 167–171 (1995).Google Scholar
  146. 146.
    Zhao F, Evans E, Bilsborrow PE, Syers JK: Influence of nitrogen and sulphur on the glucosinolate profile of rapeseed (Brassica napus L). J Sci Food Agric 64: 295–304 (1994).Google Scholar

Copyright information

© Kluwer Academic Publishers 2000

Authors and Affiliations

  • Lars Rask
    • 1
  • Erik Andréasson
    • 2
  • Barbara Ekbom
    • 3
  • Susanna Eriksson
    • 2
  • Bo Pontoppidan
    • 2
  • Johan Meijer
    • 2
  1. 1.Dept. of Medical Biochemistry and MicrobiologyUppsala UniversityUppsalaSweden
  2. 2.Dept. of Plant BiologySwedish University of Agricultural SciencesUppsalaSweden
  3. 3.Dept. of EntomologySwedish University of Agricultural SciencesUppsalaSweden

Personalised recommendations