Myrosinase

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Thioglucosidase (Myrosinase)
1e4m.png
Myrosinase from Sinapis alba. PDB 1e4m [1]
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EC no. 3.2.1.147
CAS no. 9025-38-1
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Myrosinase (EC 3.2.1.147, thioglucoside glucohydrolase, sinigrinase, and sinigrase) is a family of enzymes involved in plant defense against herbivores, specifically the mustard oil bomb. The three-dimensional structure has been elucidated and is available in the PDB (see links in the infobox).

Contents

A member of the glycoside hydrolase family, myrosinase possesses several similarities with the more ubiquitous O-glycosidases. [2] [3] However, myrosinase is the only known enzyme found in nature that can cleave a thio-linked glucose. Its known biological function is to catalyze the hydrolysis of a class of compounds called glucosinolates. [4]

Myrosinase activity

Myrosinase is regarded as a defense-related enzyme and is capable of hydrolyzing glucosinolates into various compounds, some of which are toxic. [5]

Mechanism

Myrosinase catalyzes the chemical reaction

a thioglucoside + H2O a sugar + a thiol

Thus, the two substrates of this enzyme are thioglucoside and H2O, whereas its two products are sugar and thiol.

In the presence of water, myrosinase cleaves off the glucose group from a glucosinolate. The remaining molecule then quickly converts to a thiocyanate, an isothiocyanate, or a nitrile; these are the active substances that serve as defense for the plant. The hydrolysis of glucosinolates by myrosinase can yield a variety of products, depending on various physiological conditions such as pH and the presence of certain cofactors. All known reactions have been observed to share the same initial steps. (See Figure 2.) First, the β-thioglucoside linkage is cleaved by myrosinase, releasing D-glucose. The resulting aglycone undergoes a spontaneous Lossen-like rearrangement, releasing a sulfate. The last step in the mechanism is subject to the greatest variety depending on the physiological conditions under which the reaction takes place. At neutral pH, the primary product is the isothiocyanate. Under acidic conditions (pH < 3), and in the presence of ferrous ions or epithiospecifer proteins, the formation of nitriles is favored instead. [2] [6]

Figure 2: Mechanism of glucosinolate hydrolysis by myrosinase. Myrosinase general mechanism.png
Figure 2: Mechanism of glucosinolate hydrolysis by myrosinase.

Cofactors and inhibitors

Ascorbate is a known cofactor of myrosinase, serving as a base catalyst in glucosinolate hydrolysis. [1] [7] For example, myrosinase isolated from daikon (Raphanus sativus) demonstrated an increase in V max from 2.06 μmol/min per mg of protein to 280 μmol/min per mg of protein on the substrate, allyl glucosinolate (sinigrin) when in the presence of 500 μM ascorbate. [4] Sulfate, a byproduct of glucosinolate hydrolysis, has been identified as a competitive inhibitor of myrosinase. [4] In addition, 2-F-2-deoxybenzylglucosinolate, which was synthesized specifically to study the mechanism of myrosinase, inhibits the enzyme by trapping one of the glutamic acid residues in the active site, Glu 409. [3] [8]

Structure

Myrosinase exists as a dimer with subunits of 60-70 kDa each. [9] [10] X-ray crystallography of myrosinase isolated from Sinapis alba revealed the two subunits are linked by a zinc atom. [7] The prominence of salt bridges, disulfide bridges, hydrogen bonding, and glycosylation are thought to contribute to the enzyme’s stability, especially when the plant is under attack and experiences severe tissue damage. [2] A feature of many β-glucosidases are catalytic glutamate residues at their active sites, but two of these have been replaced by a single glutamine residue in myrosinase. [3] [11] Ascorbate has been shown to substitute for the activity of the glutamate residues. [1] (See Figure 3 for mechanism.)

Figure 3: Active site of myrosinase during the first step of glucosinolate hydrolysis. Here, ascorbate is used as a cofactor to substitute for the missing second catalytic glutamate in order to cleave the thio-linked glucose. Glucosinolate hydrolysis with ascorbate cofactor at active site of myrosinase.png
Figure 3: Active site of myrosinase during the first step of glucosinolate hydrolysis. Here, ascorbate is used as a cofactor to substitute for the missing second catalytic glutamate in order to cleave the thio-linked glucose.

Biological function

Myrosinase and its natural substrate, glucosinolate, are known to be part of the plant’s defense response. When the plant is attacked by pathogens, insects, or other herbivores, the plant uses myrosinase to convert glucosinolates, which are otherwise-benign, into toxic products like isothiocyanates, thiocyanates, and nitriles. [2]

Compartmentalization in plants

The glucosinolate-myrosinase defensive system is packaged in the plant in a unique manner. Plants store myrosinase glucosinolates by compartmentalization, such that the latter is released and activated only when the plant is under attack. Myrosinase is stored largely as myrosin grains in the vacuoles of particular idioblasts called myrosin cells, but have also been reported in protein bodies or vacuoles, and as cytosolic enzymes that tend to bind to membranes. [12] [13] Glucosinolates are stored in adjacent but separate "S-cells." [14] When the plant experiences tissue damage, the myrosinase comes into contact with glucosinolates, quickly activating them into their potent, antibacterial form. [2] The most potent of such products are isothiocyanates, followed by thiocyanates and nitriles. [15]

Evolution

Plants known to have evolved a myrosinase-glucosinolate defense system include: white mustard (Sinapis alba), [9] garden cress (Lepidium sativum), [16] wasabi (Wasabia japonica), [17] and daikon (Raphanus sativus), [18] [19] as well as several members of the family Brassicaceae, including yellow mustard (Brassica juncea), [20] rape seed (Brassica napus), [21] and common dietary brassicas like broccoli, cauliflower, cabbage, bok choy, and kale. [2] The bitter aftertaste of many of these vegetables can often be attributed to the hydrolysis of glucosinolates upon tissue damage during food preparation or when consuming these vegetables raw. [2] Papaya seeds use this method of defense, but not the fruit pulp itself. [22]

Myrosinase has also been isolated from the cabbage aphid. [23] This suggests coevolution of the cabbage aphid with its main food source. The aphid employs a similar defense strategy to plants. Like its main food source, the cabbage aphid compartmentalizes its native myrosinase and the glucosinolates it ingests. When the cabbage aphid is attacked and its tissues are damaged, its stored glucosinolates are activated, producing isothiocyanates and deterring predators from attacking other aphids. [24]

Historical relevance and modern applications

Agriculture

Historically, crops like rapeseed that contained the glucosinolate-myrosinase system were deliberately bred to minimize glucosinolate content, since rapeseed in animal feed was proving toxic to livestock. [25] The glucosinolate-myrosinase system has been investigated as a possible biofumigant to protect crops against pests. The potent glucosinolate hydrolysis products (GHPs) could be sprayed onto crops to deter herbivory. Another option would be to use techniques in genetic engineering to introduce the glucosinolate-myrosinase system in crops as a means of fortifying their resistance against pests. [15]

Health effects

Isothiocyanates, the primary product of glucosinolate hydrolysis, have been known to prevent iodine uptake in the thyroid, causing goiters. [26] Isothiocyanates in high concentrations may cause hepatotoxicity. [4] There is insufficient scientific evidence that consuming cruciferous vegetables with increased intake of isothiocyanates affects the risk of human diseases. [27]

Related Research Articles

<span class="mw-page-title-main">Brassicaceae</span> Family of flowering plants

Brassicaceae or Cruciferae is a medium-sized and economically important family of flowering plants commonly known as the mustards, the crucifers, or the cabbage family. Most are herbaceous plants, while some are shrubs. The leaves are simple, lack stipules, and appear alternately on stems or in rosettes. The inflorescences are terminal and lack bracts. The flowers have four free sepals, four free alternating petals, two shorter free stamens and four longer free stamens. The fruit has seeds in rows, divided by a thin wall.

<span class="mw-page-title-main">Horseradish</span> Species of flowering plants in the cabbage family Brassicaceae

Horseradish is a perennial plant of the family Brassicaceae. It is a root vegetable, cultivated and used worldwide as a spice and as a condiment. The species is probably native to Southeastern Europe and Western Asia.

<span class="mw-page-title-main">Broccoli</span> Edible green plant in the cabbage family

Broccoli is an edible green plant in the cabbage family whose large flowering head, stalk and small associated leaves are eaten as a vegetable. Broccoli is classified in the Italica cultivar group of the species Brassica oleracea. Broccoli has large flower heads, or florets, usually dark green, arranged in a tree-like structure branching out from a thick stalk which is usually light green. The mass of flower heads is surrounded by leaves. Broccoli resembles cauliflower, which is a different but closely related cultivar group of the same Brassica species.

<i>Brassica</i> Genus of flowering plants in the cabbage family Brassicaceae

Brassica is a genus of plants in the cabbage and mustard family (Brassicaceae). The members of the genus are informally known as cruciferous vegetables, cabbages, mustard plants, or simply brassicas. Crops from this genus are sometimes called cole crops—derived from the Latin caulis, denoting the stem or stalk of a plant.

<span class="mw-page-title-main">Isothiocyanate</span> Chemical group (–N=C=S)

In organic chemistry, isothiocyanate is the functional group −N=C=S, formed by substituting the oxygen in the isocyanate group with a sulfur. Many natural isothiocyanates from plants are produced by enzymatic conversion of metabolites called glucosinolates. These natural isothiocyanates, such as allyl isothiocyanate, are also known as mustard oils. An artificial isothiocyanate, phenyl isothiocyanate, is used for amino acid sequencing in the Edman degradation.

<span class="mw-page-title-main">Mustard oil</span> Oil derived from mustard plants

Mustard oil can mean either the pressed oil used for cooking, or a pungent essential oil also known as volatile oil of mustard. The essential oil results from grinding mustard seed, mixing the grounds with water, and isolating the resulting volatile oil by distillation. It can also be produced by dry distillation of the seed. Pressed mustard oil is used as cooking oil in some cultures, but sale is restricted in some countries due to high levels of erucic acid. Varieties of mustard seed also exist that are low in erucic acid.

<span class="mw-page-title-main">Allyl isothiocyanate</span> Chemical compound

Allyl isothiocyanate (AITC) is a naturally occurring unsaturated isothiocyanate. The colorless oil is responsible for the pungent taste of Cruciferous vegetables such as mustard, radish, horseradish, and wasabi. This pungency and the lachrymatory effect of AITC are mediated through the TRPA1 and TRPV1 ion channels. It is slightly soluble in water, but more soluble in most organic solvents.

<span class="mw-page-title-main">Nitrilase</span> Class of enzymes

Nitrilase enzymes catalyse the hydrolysis of nitriles to carboxylic acids and ammonia, without the formation of "free" amide intermediates. Nitrilases are involved in natural product biosynthesis and post translational modifications in plants, animals, fungi and certain prokaryotes. Nitrilases can also be used as catalysts in preparative organic chemistry. Among others, nitrilases have been used for the resolution of racemic mixtures. Nitrilase should not be confused with nitrile hydratase which hydrolyses nitriles to amides. Nitrile hydratases are almost invariably co-expressed with an amidase, which converts the amide to the carboxylic acid. Consequently, it can sometimes be difficult to distinguish nitrilase activity from nitrile hydratase plus amidase activity.

<span class="mw-page-title-main">Sulforaphane</span> Chemical compound

Sulforaphane is a compound within the isothiocyanate group of organosulfur compounds. It is produced when the enzyme myrosinase transforms glucoraphanin, a glucosinolate, into sulforaphane upon damage to the plant, which allows the two compounds to mix and react.

<span class="mw-page-title-main">Glucoraphanin</span> Chemical compound

Glucoraphanin is a glucosinolate found in broccoli, mustard and other cruciferous vegetables.

<span class="mw-page-title-main">Glucosinolate</span> Class of chemical compounds

Glucosinolates are natural components of many pungent plants such as mustard, cabbage, and horseradish. The pungency of those plants is due to mustard oils produced from glucosinolates when the plant material is chewed, cut, or otherwise damaged. These natural chemicals most likely contribute to plant defence against pests and diseases, and impart a characteristic bitter flavor property to cruciferous vegetables.

<span class="mw-page-title-main">Sinigrin</span> Chemical compound

Sinigrin or allyl glucosinolate is a glucosinolate that belongs to the family of glucosides found in some plants of the family Brassicaceae such as Brussels sprouts, broccoli, and the seeds of black mustard. Whenever sinigrin-containing plant tissue is crushed or otherwise damaged, the enzyme myrosinase degrades sinigrin to a mustard oil, which is responsible for the pungent taste of mustard and horseradish. Seeds of white mustard, Sinapis alba, give a less pungent mustard because this species contains a different glucosinolate, sinalbin.

<span class="mw-page-title-main">Cruciferous vegetables</span> Vegetables of the family Brassicaceae

Cruciferous vegetables are vegetables of the family Brassicaceae with many genera, species, and cultivars being raised for food production such as cauliflower, cabbage, kale, garden cress, bok choy, broccoli, Brussels sprouts, mustard plant and similar green leaf vegetables. The family takes its alternative name from the shape of their flowers, whose four petals resemble a cross.

<span class="mw-page-title-main">Glucobrassicin</span> Chemical compound

Glucobrassicin is a type of glucosinolate that can be found in almost all cruciferous plants, such as cabbages, broccoli, mustards, and woad. As for other glucosinolates, degradation by the enzyme myrosinase is expected to produce an isothiocyanate, indol-3-ylmethylisothiocyanate. However, this specific isothiocyanate is expected to be highly unstable, and has indeed never been detected. The observed hydrolysis products when isolated glucobrassicin is degraded by myrosinase are indole-3-carbinol and thiocyanate ion, which are envisioned to result from a rapid reaction of the unstable isothiocyanate with water. However, a large number of other reaction products are known, and indole-3-carbinol is not the dominant degradation product when glucosinolate degradation takes place in crushed plant tissue or in intact plants.

<i>Rhamphospermum arvense</i> Species of plant

Rhamphospermum arvense, the charlock mustard, field mustard, wild mustard, or just charlock, is an annual or winter annual plant in the family Brassicaceae. It is found in the fields of North Africa, Asia, Europe, and some other areas where it has been transported and naturalized. Pieris rapae, the small white butterfly, and Pieris napi, the green veined white butterfly, are significant consumers of charlock during their larval stages.

<span class="mw-page-title-main">Sinalbin</span> Chemical compound

Sinalbin is a glucosinolate found in the seeds of white mustard, Sinapis alba, and in many wild plant species. In contrast to mustard from black mustard seeds which contain sinigrin, mustard from white mustard seeds has only a weakly pungent taste.

<span class="mw-page-title-main">Gluconasturtiin</span> Chemical compound

Gluconasturtiin or phenethyl glucosinolate is one of the most widely distributed glucosinolates in the cruciferous vegetables, mainly in the roots, and is probably one of the plant compounds responsible for the natural pest-inhibiting properties of growing crucifers, such as cabbage, mustard or rape, in rotation with other crops. This effect of gluconasturtiin is due to its degradation by the plant enzyme myrosinase into phenethyl isothiocyanate, which is toxic to many organisms.

<i>Brevicoryne brassicae</i> Species of true bug

Brevicoryne brassicae, commonly known as the cabbage aphid or cabbage aphis, is a destructive aphid native to Europe that is now found in many other areas of the world. The aphids feed on many varieties of produce, including cabbage, broccoli (especially), Brussels sprouts, cauliflower and many other members of the genus Brassica, but do not feed on plants outside of the family Brassicaceae. The insects entirely avoid plants other than those of Brassicaceae; even though thousands may be eating broccoli near strawberries, the strawberries will be left untouched.

The mustard oil bomb, formerly known as the glucosinolate–myrosinase complex, is a chemical herbivory defense system found in members of the Brassicaceae. The mustard oil bomb requires the activation of a common plant secondary metabolite, glucosinolate, by an enzyme, myrosinase. The defense complex is typical among plant defenses to herbivory in that the two molecules are stored in different compartments in the leaves of plants until the leaf is torn by an herbivore. The glucosinolate has a β-glucose and a sulfated oxime. The myrosinase removes the β-glucose to form mustard oils that are toxic to herbivores. The defense system was named a "bomb" by Matile, because it like a real bomb is waiting to detonate upon disturbance of the plant tissue.

<span class="mw-page-title-main">Glucotropaeolin</span> Chemical compound

Glucotropaeolin or benzyl glucosinolate is a glucosinolate found in cruciferous vegetables, particularly garden cress. Upon enzymatic activity, it is transformed into benzyl isothiocyanate, which contributes to the characteristic flavor of these brassicas.

References

  1. 1 2 3 Burmeister WP, Cottaz S, Rollin P, Vasella A, Henrissat B (December 2000). "High resolution X-ray crystallography shows that ascorbate is a cofactor for myrosinase and substitutes for the function of the catalytic base". The Journal of Biological Chemistry. 275 (50): 39385–39393. doi: 10.1074/jbc.M006796200 . PMID   10978344.
  2. 1 2 3 4 5 6 7 8 Halkier BA, Gershenzon J (2006). "Biology and biochemistry of glucosinolates". Annual Review of Plant Biology. 57: 303–333. doi:10.1146/annurev.arplant.57.032905.105228. PMID   16669764.
  3. 1 2 3 4 Bones AM, Rossiter JT (June 2006). "The enzymic and chemically induced decomposition of glucosinolates". Phytochemistry. 67 (11): 1053–1067. doi:10.1016/j.phytochem.2006.02.024. PMID   16624350.
  4. 1 2 3 4 Shikita M, Fahey JW, Golden TR, Holtzclaw WD, Talalay P (August 1999). "An unusual case of 'uncompetitive activation' by ascorbic acid: purification and kinetic properties of a myrosinase from Raphanus sativus seedlings". The Biochemical Journal. 341 ( Pt 3) (3): 725–732. doi:10.1042/0264-6021:3410725. PMC   1220411 . PMID   10417337.
  5. ↑ A wound- and methyl jasmonate-inducible transcript coding for a myrosinase-associated protein with similarities to an early nodulin
  6. ↑ Lambrix V, Reichelt M, Mitchell-Olds T, Kliebenstein DJ, Gershenzon J (December 2001). "The Arabidopsis epithiospecifier protein promotes the hydrolysis of glucosinolates to nitriles and influences Trichoplusia ni herbivory". The Plant Cell. 13 (12): 2793–2807. doi:10.1105/tpc.010261. PMC   139489 . PMID   11752388.
  7. 1 2 Burmeister WP, Cottaz S, Driguez H, Iori R, Palmieri S, Henrissat B (May 1997). "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 (5): 663–675. doi: 10.1016/s0969-2126(97)00221-9 . PMID   9195886.
  8. ↑ Cottaz S, Rollin P, Driguez H (1997). "Synthesis of 2-deoxy-2-fluoroglucotropaeolin, a thioglucosidase inhibitor". Carbohydrate Research. 298 (1–2): 127–130. doi:10.1016/s0008-6215(96)00294-7.
  9. 1 2 Björkman R, Janson JC (August 1972). "Studies on myrosinases. I. Purification and characterization of a myrosinase from white mustard seed (Sinapis alba, L.)". Biochimica et Biophysica Acta (BBA) - Enzymology. 276 (2): 508–518. doi:10.1016/0005-2744(72)91011-X. PMID   5068825.
  10. ↑ Pessina A, Thomas RM, Palmieri S, Luisi PL (August 1990). "An improved method for the purification of myrosinase and its physicochemical characterization". Archives of Biochemistry and Biophysics. 280 (2): 383–389. doi:10.1016/0003-9861(90)90346-Z. PMID   2369130.
  11. ↑ Henrissat B, Davies GJ (December 2000). "Glycoside hydrolases and glycosyltransferases. Families, modules, and implications for genomics". Plant Physiology. 124 (4): 1515–1519. doi:10.1104/pp.124.4.1515. PMC   1539306 . PMID   11115868.
  12. ↑ Lüthy B, Matile P (1984). "The mustard oil bomb: Rectified analysis of the subcellular organisation of the myrosinase system". Biochemie und Physiologie der Pflanzen. 179 (1–2): 5–12. doi:10.1016/s0015-3796(84)80059-1.
  13. ↑ Andréasson E, Bolt Jørgensen L, Höglund AS, Rask L, Meijer J (December 2001). "Different myrosinase and idioblast distribution in Arabidopsis and Brassica napus". Plant Physiology. 127 (4): 1750–1763. doi:10.1104/pp.010334. PMC   133578 . PMID   11743118.
  14. ↑ Koroleva OA, Davies A, Deeken R, Thorpe MR, Tomos AD, Hedrich R (October 2000). "Identification of a new glucosinolate-rich cell type in Arabidopsis flower stalk". Plant Physiology. 124 (2): 599–608. doi:10.1104/pp.124.2.599. PMC   59166 . PMID   11027710.
  15. 1 2 Gimsing AL, Kirkegaard JA (2009). "Glucosinolates and biofumigation: fate of glucosinolates and their hydrolysis products in soil". Phytochemistry Reviews. 8: 299–310. doi:10.1007/s11101-008-9105-5. S2CID   30626061.
  16. ↑ Durham PL, Poulton JE (May 1989). "Effect of Castanospermine and Related Polyhydroxyalkaloids on Purified Myrosinase from Lepidium sativum Seedlings". Plant Physiology. 90 (1): 48–52. doi:10.1104/pp.90.1.48. PMC   1061675 . PMID   16666767.
  17. ↑ Ohtsuru M, Kawatani H (1979). "Studies on the myrosinase from Wasabia japonica: Purification and some properties of wasabi myrosinase". Agricultural and Biological Chemistry. 43 (11): 2249–2255. doi: 10.1271/bbb1961.43.2249 .
  18. ↑ Iversen TH, Baggerud C (1980). "Myrosinase activity in differentiated and undifferentiated plants of Brassiaceae Z.". Zeitschrift für Pflanzenphysiologie. 97 (5): 399–407. doi:10.1016/s0044-328x(80)80014-6.
  19. ↑ El-Sayed ST, Jwanny EW, Rashad MM, Mahmoud AE, Abdallah NM (1995). "Glycosidases in plant tissues of some brassicaceae screening of different cruciferous plants for glycosidases production". Applied Biochemistry and Biotechnology. 55 (3): 219–230. doi:10.1007/BF02786861. ISSN   0273-2289. S2CID   84375704.
  20. ↑ Masaru O, Tadao H (1972). "Molecular Properties of Multiple Forms of Plant Myrosinase". Agricultural and Biological Chemistry. 36 (13): 2495–2503. doi: 10.1271/bbb1961.36.2495 .
  21. ↑ Lönnerdal B, Janson JC (1973). "Studies on myrosinases. II. Purification and characterization of a myrosinase from rapeseed (Brassica napus L.)". Biochimica et Biophysica Acta (BBA) - Enzymology. 315 (2): 421–429. doi:10.1016/0005-2744(73)90272-6.
  22. ↑ Nakamura Y, Yoshimoto M, Murata Y, Shimoishi Y, Asai Y, Park EY, et al. (May 2007). "Papaya seed represents a rich source of biologically active isothiocyanate". Journal of Agricultural and Food Chemistry. 55 (11): 4407–4413. doi:10.1021/jf070159w. PMID   17469845.
  23. ↑ Husebye H, Arzt S, Burmeister WP, Härtel FV, Brandt A, Rossiter JT, Bones AM (December 2005). "Crystal structure at 1.1 Angstroms resolution of an insect myrosinase from Brevicoryne brassicae shows its close relationship to beta-glucosidases". Insect Biochemistry and Molecular Biology. 35 (12): 1311–1320. doi:10.1016/j.ibmb.2005.07.004. PMID   16291087.
  24. ↑ Bridges M, Jones AM, Bones AM, Hodgson C, Cole R, Bartlet E, et al. (January 2002). "Spatial organization of the glucosinolate-myrosinase system in brassica specialist aphids is similar to that of the host plant". Proceedings. Biological Sciences. 269 (1487): 187–191. doi:10.1098/rspb.2001.1861. PMC   1690872 . PMID   11798435.
  25. ↑ Brabban AD, Edwards C (June 1994). "Isolation of glucosinolate degrading microorganisms and their potential for reducing the glucosinolate content of rapemeal". FEMS Microbiology Letters. 119 (1–2): 83–88. doi: 10.1111/j.1574-6968.1994.tb06871.x . PMID   8039675.
  26. ↑ Bones AM, Rossiter JT (1996). "The myrosinase-glucosinolate system, its organisation and biochemistry". Physiologia Plantarum. 97: 194–208. doi:10.1111/j.1399-3054.1996.tb00497.x.
  27. ↑ "Isothiocyanates". Micronutrient Information Center, Linus Pauling Institute, Oregon State University. 1 April 2017. Retrieved 26 June 2022.
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