Skip to main content

Myrosinase: gene family evolution and herbivore defense in Brassicaceae

  • Chapter
Plant Molecular Evolution

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  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).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  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. Blau PA, Feeney P, Contardo L, Tobson DS: Allylglucosinolate and herbivorous caterpillars: a contrast in toxicity and tolerance. Science 200: 1296–1298 (1978).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  7. Bones A, Iversen T-H: Myrosin cells and myrosinase. Isr J Bot 34: 351–375 (1985).

    CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  10. Bones AM, Visvalingam S, Thangstad OP: Sulphate can induce differential expression of thioglucoside glucohydrolases (myrosinases). Planta 193: 558–566 (1994).

    Article  CAS  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  13. Bussy A: Sur la formation de l’huile essentielle de moutarde. J Pharm 27: 464–471 (1840).

    Google Scholar 

  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).

    PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  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. 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. 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. 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).

    Article  CAS  Google Scholar 

  20. Cottaz S, Henrissat R, Driguez H: Mechanism-based inhibition and stereochemistry of glucosinolate hydrolysis by myrosinase. Biochemistry 35: 15256–15259 (1996).

    Article  PubMed  CAS  Google Scholar 

  21. Cronquist A: The Evolution and Classification of Flowering Plants, 2nd ed. New York Botanical Garden, New York (1988).

    Google Scholar 

  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. 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. Davies G, Henrissat B: Structures and mechanisms of glycosyl transferases. Curr Biol 3: 853–859 (1995).

    CAS  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  29. Durham PL, Poulton JE: Enzymatic properties of purified myrosinase from Lepidium sativum seedlings. Z Naturforsch 45: 173–178 (1990).

    CAS  Google Scholar 

  30. Ekbom B: Clutch size and larval performance of pollen beetles on different host plants. Oikos 83: 56–64 (1998).

    Article  Google Scholar 

  31. Ettlinger MG, Lundeen AJ: The structures of sinigrin and sinalbin: an enzymatic rearrangement. J Am Chem Soc 78: 4172–4173 (1956).

    Article  CAS  Google Scholar 

  32. Ettlinger MG, Kjaer A: Sulfur compounds in plants. Rec Adv Phytochem 1: 49–144 (1968).

    Google Scholar 

  33. Fagerström T, Larsson S, Tenow O: On optimal defence in plants. Funct Ecol 1: 73–81 (1987).

    Article  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  35. Falk A, Ek B, Rask L: Characterization of a new myrosinase in Brassica napus. Plant Mol Biol 27: 863–874 (1995).

    Article  PubMed  CAS  Google Scholar 

  36. Falk A, Rask L: Expression of a zeatin-O-glucoside-degrading ß-glucosidase in Brassica napus. Plant Physiol 108: 1369–1377 (1995).

    Article  PubMed  CAS  Google Scholar 

  37. Falk A, Taipalensuu J, Rask L: Characterization of myrosinase-binding protein. Planta 195: 387–395 (1995).

    Article  PubMed  CAS  Google Scholar 

  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).

    CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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. Geshi N, Andréasson E, Meijer J, Rask L, Brandt A: My-rosinase 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).

    Article  CAS  Google Scholar 

  42. Geshi N, Brandt A: Two jasmonate inducible myrosinase-binding proteins from Brassica napus L. seedlings with homology to jacalin. Planta 204: 295–304 (1998).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  44. Giamoustaris A, Mithen R: Glucosinolates and disease resistance in oilseed rape (Brassica napus ssp oleifera). Plant Pathol 46: 271–275 (1997).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  46. Grob K, Matile P: Vacuolar location of glucosinolates in horseradish root cells. Plant Sci Lett 14: 327–335 (1979).

    Article  CAS  Google Scholar 

  47. Groot Wassink JWD, Reed DW, Kolenovsky AD: Immuno-purification and immunocharacterization of the glucosinolate biosynthetic enzyme thiohydroximate S-glucosyltransferase. Plant Physiol 105: 425–433 (1994).

    CAS  Google Scholar 

  48. Halkier BA, Sibbesen O, Koch B, Møller 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).

    Article  PubMed  CAS  Google Scholar 

  49. Hartman T: Diversity and variability of plant secondary metabolism: a mechanistic view. Entomol Exp Appl 80: 177–188 (1996).

    Article  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  51. Heinricher E: Über Eiweisstoffe führende Idioblasten bei einigen Cruciferen. Ber Dtsch Bot Ges II: 463–466 (1884).

    Google Scholar 

  52. Helmlinger J, Rausch T, Hilgenberg W: Localization of newly synthesized indole-3-methylglucosinolate (= gluco-brassin) in vacuoles in horseradish (Armoracia rusticana). Physiol Plant 58: 302–310 (1983).

    Article  CAS  Google Scholar 

  53. Henrissat B: A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J 280: 309–316 (1991).

    PubMed  CAS  Google Scholar 

  54. Henrissat B, Bairoch A: Updating the sequence-based classification of glycosyl hydrolases. Biochem J 316: 695–696 (1996).

    PubMed  Google Scholar 

  55. Höglund A-S, Lenman M, Falk A, Rask L: Distribution of myrosinase in rapeseed tissues. Plant Physiol 95: 213–221 (1991).

    Article  PubMed  Google Scholar 

  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).

    Article  Google Scholar 

  57. Hölmes MRJ: Nutrition of the Oilseed Rape Crop. Applied Science Publishers, London (1980).

    Google Scholar 

  58. James DC, Rossiter JT: Development and characteristics of myrosinase in Brassica napus during early seedling growth. Physiol Plant 82: 163–170 (1991).

    Article  CAS  Google Scholar 

  59. Jensen CR, Mogensen VO, Mortensen G, Fieldsend JK, Mil-ford 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).

    Article  Google Scholar 

  60. Kater MM: Structure, function and expression of plant and bacterial enoyl-ACP reductase genes. Thesis, Vrije Universiteit, Amsterdam (1994).

    Google Scholar 

  61. Kelly PJ, Bones A, Rossiter JT: Sub-cellular immunolocalization of the glucosinolate sinigrin in seedlings of Brassica juncea. Planta 206: 370–377 (1998).

    Article  PubMed  CAS  Google Scholar 

  62. Kiddle GA, Kevin JD, Wallsgrow RM: Salicylic acid-induced accumulation of glucosinolates in oilseed rape (Brassica napus) leaves. J Exp Bot 45: 1343–1346 (1994).

    Article  CAS  Google Scholar 

  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. 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. Koch B, Nielsen VS, Halkier BA, Olsen CE, Møller BL: The biosynthesis of cyanogenic glucosides in seedlings of cassava (Manihot esculenta Crantz). Arch Biochem Biophys 292: 141–150 (1992).

    Article  PubMed  CAS  Google Scholar 

  66. Kozlowska HJ, Nowak H, Nowak J: Characterization of myrosinase in Polish varieties of rapeseed. J Sci Food Agric 34: 1171–1178 (1983).

    Article  CAS  Google Scholar 

  67. Lenman M, Rödin J, Josefsson L-G, Rask L: Immunological characterization of rapeseed myrosinase. Eur J Biochem 194: 747–753 (1990).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  70. Lönnerdal B, Janson J-C: Studies on myrosinase. II. Purification and characterization of a myrosinase from rapeseed (Brassica napus L.). Biochim Biophys Acta 315: 421–429 (1973).

    Article  Google Scholar 

  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. 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. Machlin S, Mitchell-Olds T, Bradley D: Sequence of a Brassica campestris myrosinase gene. Plant Physiol 102: 1359–1360 (1993).

    Article  PubMed  CAS  Google Scholar 

  74. Malboobi MA, Lefebvre DD: A phosphate-starvation inducible β-glucosidase gene (psr3.2) isolated from Arabidopsis thaliana is a member of a distinct subfamily of the BGA family. Plant Mol Biol 34: 57–68 (1997).

    Article  PubMed  CAS  Google Scholar 

  75. Markert CL, Möller F: Multiple forms of enzymes: tissue, ontogenetic and species specific patterns. Proc Natl Acad Sci USA 45: 753–763 (1959).

    Article  PubMed  CAS  Google Scholar 

  76. Mattiacci L, Dicke M, Posthumus MA: Induction of par-asitoid 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).

    Article  CAS  Google Scholar 

  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).

    Article  Google Scholar 

  78. Mauricio R: Costs of resistance to natural enemies in field populations of the annual plant Arabidopsis thaliana. Am Natural 151: 20–28 (1998).

    Article  CAS  Google Scholar 

  79. McGibbon DB, Allison RM: A glucosinolase system in the aphid Brevicoryne brassicae. NZ J Sci 11: 440–446 (1968).

    CAS  Google Scholar 

  80. McGregor DI: Glucosinolate content of developing rapeseed (Brassica napus L. Midas) seedlings. Can J Plant Sci 68: 367–380 (1988).

    Article  CAS  Google Scholar 

  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. 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).

    Article  CAS  Google Scholar 

  83. Mithen RF, Magrath R: Glucosinolates and resistance to Leptosphaeria maculans in wild and cultivated Brassica species. Plant Breed 108: 60–68 (1992).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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. 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. Ohtsuru M, Hata T: The interaction of L-ascorbic acid with the active center of myrosinase. Biochim Biophys Acta 567: 384–379 (1979).

    Article  PubMed  CAS  Google Scholar 

  88. Pagès RDM: TREEVIEW: an application to display phylogenetic trees on personal computers. Comp Appl Biosci 12: 357–358 (1996).

    Google Scholar 

  89. Phelan JR, Vaughan JG: Myrosinase in Sinapis alba L. J Exp Bot 31: 1425–1433 (1980).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  92. Poulton JE: Cyanogenesis in plants. Plant Physiol 94: 401–405 (1990).

    Article  PubMed  CAS  Google Scholar 

  93. Poulton JE, Müller BL: Glucosinolates. Meth Plant Biochem 9: 209–237 (1993).

    CAS  Google Scholar 

  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).

    Article  Google Scholar 

  95. Reed DW, Davin L, Jain JC, DeLuca V, Nelson L, Underhill EW: Purification and properties of UDP-glucose:thiohydroximate glucosyltransferase from Brassica napus L. seedlings. Arch Biochem Biophys 305: 526–532 (1993).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  97. Robiquet PJ, Boutron F: Sur la semence de moutarde. J Pharm Chim 17: 279–282 (1831).

    Google Scholar 

  98. Rodman J: A taxonomic analysis of glucosinolate-producing plants, Part 1. Phenetics. SystBot 16: 598–618 (1991).

    Google Scholar 

  99. Rodman J: A taxonomic analysis of glucosinolate-producing plants, Part 2. Cladistics. Syst Bot 16: 619–629 (1991).

    Google Scholar 

  100. Rodman J, Price RA, Karol K, Conti E, Sytsma KJ, Palmer JD: Nucleotide sequences of the rbcL gene indicate mono-phyly of mustard oil plants. Ann Miss Bot Gard 80: 686–699 (1993).

    Article  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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. Schnug E: Double low rapeseed in West Germany: sulphur metabolism and glucosinolate levels. Asp Appl Biol 23: 67–82 (1989).

    Google Scholar 

  107. Schnug E: Sulphur nutrition and quality of of vegetables. Sulphur Agric 14: 3–7 (1990).

    Google Scholar 

  108. Schnug E, Evans E: Monitoring the sulphur deficiency symptoms in Brassica napus. Phyton 32: 53–56 (1992).

    Google Scholar 

  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).

    Article  Google Scholar 

  110. Schoonhoven LM, Jermy T, van Loon JJA: Insect-Plant Biology. Chapman & Hall, London (1998).

    Google Scholar 

  111. Selmar D, Lieberei R, Biehl B, Voigt J: Hevea linama-rase: a nonspecific ß-glycosidase. Plant Physiol 83: 557–563 (1987).

    Article  PubMed  CAS  Google Scholar 

  112. Selmar D, Lieberei R, Biehl B: Mobilization and utilization of cyanogenic glycosides; the linustatin pathway. Plant Physiol 86: 711–716 (1988).

    Article  PubMed  CAS  Google Scholar 

  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. Sharma M: Ontogenic studies of the myrosin idioblasts in Brassica napus and Brassica montana. Bot Tidskr 66: 51–59 (1971).

    Google Scholar 

  115. Sibbesen O, Koch B, Halkier BA, Møller BL: Cytochrome P450tyr is a multifunctional heme-thiolate enzyme catalyzing the conversion of L-tyrosine to p-hydroxyphenylacetaldehyde oxime in the biosynthesis of the cyanogenic glucoside dhurrin in Sorghum bicolor (L.) Moench. J Biol Chem 270: 3506–3511 (1995).

    Article  PubMed  CAS  Google Scholar 

  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. 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).

    Article  Google Scholar 

  118. Simms EL, Rausher MD: Costs and benefits of plant resistance to herbivory. Am Natural 130: 570–581 (1987).

    Article  Google Scholar 

  119. Sinnott ML: Catalytic mechanisms of enzymic glycosyl transfer. Chem Rev 90: 1171–1202 (1990).

    Article  CAS  Google Scholar 

  120. Sørensen H: Glucosinolates: structure, properties, function. In: Shadidi F (ed.), Canola and Rapeseed, pp. 149–172. AVI Book, New York (1990).

    Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  122. Taipalensuu J, Falk A, Rask L: A wound-and methyl jasmonate-inducible transcript coding for a myrosinase-associated protein with similarities to an early nodulin. Plant Physiol 110: 483–491 (1996).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  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 wound-inducible counterpart. Eur J Biochem 250: 680–688 (1997).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  127. Thangstad OP, Iversen T-H, Slupphaug G, Bones A: Im-munocytochemical localization of myrosinase in Brassica napus L. Planta 180: 245–248 (1990).

    Article  CAS  Google Scholar 

  128. Thangstad OP, Evjen K, Bones A: Immunogold-EM localization of myrosinase in Brassicaceae. Protoplasma 161: 85–93 (1991).

    Article  CAS  Google Scholar 

  129. Thangstad OP, Winge P, Husbye H, Bones A: The myrosinase (thioglucoside glucohydrolase) gene family in Brassicaceae. Plant Mol Biol 23: 511–524 (1993).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  131. Thompson JN: The Coevolutionary Process. University of Chicago Press, Chicago, IL (1994).

    Google Scholar 

  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. 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).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  136. van Etten HD, Mansfield JW, Bailey JA, Farmer EE: Two classes of plant antibiotics: phytoalexins versus ‘phytoan-ticipins’. Plant Cell 6: 1191–1192 (1994).

    Google Scholar 

  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).

    Article  Google Scholar 

  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. 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).

    Article  CAS  Google Scholar 

  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. 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. Xue J, Lenman M, Falk A, Rask L: The glucosinolate-degrading enzyme myrosinase in Brassicaceae is encoded by a gene family. Plant Mol Biol 18: 387–398 (1992).

    Article  PubMed  CAS  Google Scholar 

  143. Xue J, Jørgensen M, Pihlgren, U, Rask L: The myrosinase gene family in Arabidopsis thaliana: gene organization, expression and evolution. Plant Mol Biol 27: 911–922 (1995).

    Article  PubMed  CAS  Google Scholar 

  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. 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).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2000 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Rask, L., Andréasson, E., Ekbom, B., Eriksson, S., Pontoppidan, B., Meijer, J. (2000). Myrosinase: gene family evolution and herbivore defense in Brassicaceae. In: Doyle, J.J., Gaut, B.S. (eds) Plant Molecular Evolution. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-4221-2_5

Download citation

  • DOI: https://doi.org/10.1007/978-94-011-4221-2_5

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-94-010-5833-9

  • Online ISBN: 978-94-011-4221-2

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics