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Lipoxygenase in fruits and vegetables: A review
Enzyme and Microbial Technology 40 (2007) 491–496
Review
Lipoxygenase in fruits and vegetables: A review Taner Baysal a , Aslıhan Demird¨oven b,∗ a
Ege University, Engineering Faculty, Food Engineering Department, Izmir 35100, Turkey b Ege University, Institute of Natural and Applied Sciences, Izmir 35100, Turkey
Received 4 July 2006; received in revised form 27 November 2006; accepted 30 November 2006
Abstract Lipoxygenase (LOX) is one of the most widely studied enzyme in plants and animal kingdom which is found in more than 60 species. Lipoxygenase catalyses the bioxygenation of polyunsaturated fatty acids (PUFA) containing a cis,cis-1,4-pentadiene unit to form conjugated hydroperoxydienoic acids. Lipoxygenases have food-related applications in bread making and aroma production; they also have negative implications for the color, off-flavour and antioxidant status of plant-based foods. The significance of plant lipoxygenase for fruit and vegetables are reviewed with particular reference to the enzymes from plants. Various aspects of the sources of lipoxygenases, their oxidation mechanism, isozymes and inhibition of oxidation are discussed. © 2006 Elsevier Inc. All rights reserved. Keywords: Lipoxygenase; Oxidation mechanism; Isozymes; Inhibition
Contents 1. 2. 3.
4. 5.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Lipoxygenase contents of plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Mechanism of lipoxygenase-catalysed oxidation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Lipoxygenase isozymes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Iron content . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Inhibition of lipoxygenase oxidation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Introduction Lipoxygenase (LOX) is an enzyme that is found in many plants and animals, which catalyses the oxygenation of polyunsaturated fatty acids (PUFA) to form fatty acid hydroperoxides. They are present in a wide range of biological organs and tissues, but they are particularly abundant in grain legume seeds (beans and peas) and potato tubers [1]. Lipoxygenase from different sources, catalyses oxygenation at different points along the carbon chain, referred to as “positional” or “regio” specificity, such specificity has significant implications for the ∗
Corresponding author. E-mail addresses: [email protected] (T. Baysal), [email protected] (A. Demird¨oven). 0141-0229/$ – see front matter © 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.enzmictec.2006.11.025
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metabolism of the resultant hydroperoxides into a number of important secondary metabolites [2,3]. Linoleic and linolenic acid are the major polyunsaturated fatty acids in plant tissues, and insertion of the oxygen takes place at either the 9 or 12 position to generate the corresponding 9- or 13-hydroperoxides. While most LOXs so far characterized are soluble cytosolic enzymes, some are chloroplastic, mitochondrial, or located in the vacuoles. In soybean, lipoxygenases have been identified with involvement in nitrogen and assimilate partitioning and appear to be regulated in response to plant nitrogen status in both tissue-specific and developmentally controlled patterns [1–4]. A key role for some LOX isoforms is in the generation of fatty acid hydroperoxides destined for jasmonic acid (JA), which triggers gene activation during wound response in plants. The fatty acid hydroperoxides generated by the activity of LOX are potentially deleterious to membrane function by
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causing increased rigidity and would not, therefore, be expected to accumulate [4]. Lipoxygenase not only has food-related applications in bread making [5] and aroma production [6]; but also has negative implications for color, off-flavour and antioxidant status of plantbased foods [2]. In many applications it is possible to use crude plant materials or extracts [6], but such materials usually contain multiple enzymes that may reduce polyunsaturated fatty acid substrate availability or metabolize the hydroperoxide products, thereby modulating lipoxygenase action, which has led to understand the activities and properties of plant and other lipoxygenases as food processing additives and to remove selectively specific lipoxygenase from plants based on such understanding [2]. The significance of plant lipoxygenase is reviewed, with particular reference to the enzymes from some fruits and vegetables. Various aspects of the sources of lipoxygenases, their oxidation mechanism, isozymes and inhibition of oxidation are discussed. 2. Lipoxygenase contents of plants There is ample evidence that lipoxygenase is crucial elements of plants defence strategies. Removal of a specific tobacco leaf lipoxygenase, by genetic engineering, converts a strain of tobacco that is resistant to Phytophthora parasitica var. nicotiana to one that is susceptible [7]. Although the mechanism of resistance is unknown, this unambiguously shows that lipoxygenase is an essential part of the resistance. Many plants respond to insect damage or wounding by the production of jasmonate (Fig. 1), and the activation of proteinase inhibitor genes in both wounded and non-wounded leaves [8,9]. Removal of wound-induced lipoxygenase activity from potato leaves eliminates the production of jasmonate and/or proteinase inhibitor in response to wounding, which lead to increased susceptibility to insect attack [9]. Leaves of French beans that are resistant to
Pseudomonas syringae pv phaseolicola show, on infection, an elevated production of six-carbon aldehydes that are believed to derive from lipoxygenase-produced hydroperoxides; the aldehydes are produced in bacteriocidal amounts and thus act as a defence mechanism against Pseudomonas attack [10]. Lipoxygenase in vegetative tissues therefore provide hydroperoxide substrates that can be metabolized to compounds that play important roles in plant defence. Although, it is less clear why seeds and tubers have large amounts of lipoxygenase and in such cases they are possibly dispensable; genetic removal of specific soybean [11] or pea [12] seed isoforms, for instance, appears not to compromise plant health. As part of a drive to understand more fully the roles of various lipoxygenases in plant biology, many of them have been cloned and produced as recombinant enzymes [2]. 3. Mechanism of lipoxygenase-catalysed oxidation Various aspects of the sources of the enzymes, their activities, substrate and product specificities, and co-oxidation potential are discussed in the context of food quality and shelf life. The sequences of lipoxygenases, predicted from DNA sequences, from different plants, are compared and the significance of sequence differences assessed in relation to enzyme specificity and the three-dimensional structure of soybean lipoxygenase1. A novel scheme is proposed for the mechanism of the lipoxygenase-catalysed dioxygenation of polyunsaturated fatty acids in which two different pathways are suggested for the anaerobic and aerobic oxidations (Fig. 2) [13,14]. 3.1. Lipoxygenase isozymes The enzyme lipoxygenase (linoleate oxygen oxidoreductase, EC 1.13.11.12) is present in a wide variety of plant and animal tissues [15]. The enzyme in oil-bearing seeds, e.g. soybeans,
Fig. 1. Parts of the pathway of plant oxylipin metabolism leading from linolenic acid to jasmonate and volatile aldehydes [2].
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Fig. 2. Pathway of lipoxygenase-catalysed oxidation [14].
can be an important source of hydroperoxides formed in the oil during extraction. In vegetables, oxidative changes due to the enzyme may lead to off-flavours during storage. The enzyme does, however, contribute to flavor formation in some plant foods including tomato and cucumber. Lipoxygenase activity requires the presence of free polyunsaturated fatty acids. Linoleic acid is the most common substrate in plant-based foods. The enzyme occurs in a variety of isozymes, which often vary in optimum pH, as well as product and substrate specificity. Lipoxygenase catalyses the bioxygenation of polyunsaturated fatty acids containing a cis,cis-1,4-pentadiene unit to form conjugated hydroperoxydienoic acids [16]. Lipoxygenase from soybean seed is the best characterized among plant LOX, although the physiological roles of these enzymes are not completely known [17]. Soybean seed lipoxygenase catalyses the hydroperoxidation of polyunsaturated fatty acids, such as linoleic and linolenic acids, leading to the production of several reactive molecules that account for the grassy beany taste in soybean processed foods. In soybean leaves, LOX has been intensively examined [18] but the diversity and characteristics of the different forms of LOX are not yet known. Given the occurrence of multiple LOX isoenzymes in soybean leaves and the proposed roles of these enzymes in the plant metabolism, it is possible that individual isoenzymes play specific functions [19]. Soybean lipoxygenase is the most extensively studied for which molecular structure has been reported by Boyington et al. [20]. Four isozymes have been isolated from soybeans: (1) Soy isozyme has an optimum pH of 9.0. It only acts on free polyunsaturated fatty acids and it forms 9- and 13hydroperoxides in the ratio of 1:9 at room temperature [20]. Some types of lipoxygenases can also catalyse the co-oxidation of carotenoids in the presence of PUFAs. Soybean lipoxygenase type-1 (LOX-1) has been used for the bleaching of wheat flour and also been shown to act as a
bread improver and a valuable processing aid during dough development [21]. (2) Soy isozyme has an optimum pH of 6.8, it acts on triglycerides as well as free polyunsaturated fatty acids and it forms 9- and 13-hydroperoxide in the ratio of about 1:1 at room temperature [20]. A bleached color can also indicate deterioration in either fresh vegetables, such as yellow French beans or fruits and processed food products, where carotenoids are important natural colorants and antioxidants. It has been reported that type-2 lipoxygenases (LOX-2 and -3) of soybean, pea and wheat are pigment bleachers in the presence of linoleic acid [22], but most of the reported studies for the co-oxidation of carotenoids have been for soybean LOX-1. It has been claimed that, under anaerobic conditions, this enzyme shows strong co-oxidising activities in the presence of PUFA or a corresponding acyl hydroperoxide [23], whereas, under aerobic conditions, it is not an efficient catalyst for the bleaching reaction [24,13,1,25]. (3) Soy isozyme is similar to isozyme 2, but its activity is inhibited by calcium ions, whereas lipoxygenase-2 is stimulated by the metal [20]. (4) Lipoxygenase is very similar to isozyme 3, but can be separated by gel chromatography or electrophoresis [20]. Lipoxygenase isozymes are commonly classified as type 1, which have an optimum pH in the alkaline region and are specific for free fatty acids and type 2, which has optimum activity at neutral pH and causes co-oxidation of carotenoids. The ability of lipoxygenase type 2 to bleach carotenoids has found practical application in the addition of soybean flour to wheat flour in order to bleach the flour in the manufacture of white bread [16]. For LOX-3 an increase in foaming activity has been reported, as well as an overall improvement in bread making quality of wheat flour. The bakery yeast Saccharomyces cerevisiae also contains LOX. Recently, this enzyme was partially purified, but
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its potential, if any, on bread making remains to be established. Nowadays, it is feasible to change the profile and content of LOX (iso)enzymes in plants either by classical means, or potentially by genetic modification [7,25]. For example, by appropriate crosses, near-isogenic soybean seeds have been developed that lack either isoenzymes L1 and L3, or isoenzymes L2 and L3. These LOX-minus mutants still grow well in the field. In principle, transgenic plants lacking or over expressing one or more LOX isoenzymes could be constructed and tailored to specific applications [20]. To that end, the heterologous expression of one or more soybean LOX isoenzymes in wheat could be of interest. It is interesting to note that the use of soybean lipoxygenase was described in the 1930s as a means to bleach the flour in preparation of white bread. More recent experiments have shown that carotenoids present in wheat flour are destroyed by co-oxidation. Wheat flour itself contains little LOX activity, but LOX is abundantly present in soybeans [4,11,16]. To that end, wheat flour is often fortified with up to 0.5% enzyme-active soy flour. Other applications of LOX include the bleaching of noodles, whey products, rice and wheat bran [4]. In plant tissues, various enzymes occur that cause the conversion of hydroperoxides to other products, some of which are important as flavour compounds. These enzymes include hydroperoxide lyase, which catalyses the formation of aldehydes and oxo acids, hydroperoxide-dependent peroxygenase and epoxygenase, which catalyse the formation of epoxy and hydroxy fatty acids, and hydroperoxide isomerase, which catalyses the formation of epoxyhydroxy fatty acids and trihydroxy fatty acids. Lipoxygenase produces similar flavour volatiles to those produced during autoxidation, although the relative proportions of the products may vary widely depending on the specificity of the enzyme and the reaction conditions [16]. Potato lipoxygenase, although up to date studies have not well realized, is unusual as it is a plant enzyme, which resembles mammalian lipoxygenase and catalyses the oxidation of the 20-carbon atom PUFA, arachidonic acid, to form 15hydroperoxyeicosatetraenoic acid as the major product [9,15]. In animals, this hydroperoxide is the precursor of biologically active compounds of considerable pharmaceutical interest. Thus, potato lipoxygenase is of special interest because of its greater availability and its potential use as a model and alternative for the mammalian enzyme. Three isoenzymes of lipoxygenase have been isolated from potato [26] and defined as LOX-1, -2 and -3. Linoleic acid has been claimed to be the preferred substrate for potato LOX-1 and the 9-hydroperoxide as the dominant product. On the other hand, linolenic acid has been claimed as the preferred substrate for both potato LOX-2 and -3, which produce the 13-hydroperoxide as the main product. Also potatoes contain different leaf and tuber lipoxygenases [26] with different regiospecificities; the leaf lipoxygenase that produces 13-hydroperoxides from linolenic acid is involved in the synthesis of jasmonate [27,28], an important elicitor of plant defence gene expression, through the so-called “octadecanoid signalling” pathway [8]. Tomato also contain a fruit 9-lipoxygenase activity and a leaf activity [29,30]. In tomatoes at least two isoenzymes have
been identified different thermal stabilities. Similarly, resistant and labile lipoxygenase isoenzymes have already been observed in many vegetable products (potato, wheat germ, green beans, peas), as well as in tomato [31]. This LOX activity also causes color degradation for frozen tomato cubes during storage. In tomato cubes, LOX activity was investigated during frozen storage and it has been observed that LOX activity was increased during storage. In order to prevent color degradation of tomato cubes, they were coated by modified starch. The results showed that LOX activity decreased and the color was found better than the uncoated samples during frozen storage [32]. The cucumber LOX enzyme was similar to the potato and tomato enzymes, both in pH characteristics and substrate specificity [33]. In apples, LOX activity during storage was investigated in the core, flesh and peel. Activity was always highest in the core and peel. On storage, activity was increased in each part of the fruit but especially in the core and peel. Increase in LOX preceded the browning of the core. LOX may be responsible for the browning and may be concerned in the induction of superficial scald [34]. LOX has been reported to be involved in ripening process in strawberry fruit and thus, albino fruit have lower LOX activity due to poor color development in them [35]. Pea has a complex lipoxygenase gene family with at least five enzymes each in seeds [36] and nodules [37] and yet more in stems and roots [36]. In some species the leaf enzymes have been shown to be targeted to the chloroplast [26,28]; such plastidial enzymes are sufficiently different from other lipoxygenases to be classified as a separate group [38]. 3.2. Iron content Lipoxygenase molecules contain one atom of iron. The iron atom is in the high spin Fe(II) state in the native resting form of lipoxygenase, and must be oxidised to Fe(III) by the reaction product, fatty acid hydroperoxides or hydrogen peroxide before activating as an oxidation catalyst [1,2]. As a consequence of this requirement for oxidation of the iron in the enzyme, a lag period is observed, when the enzyme is used with pure fatty acid substrates. The active enzyme abstracts a hydrogen atom stereospecifically from the intervening methylene group of a polyunsaturated fatty acid in a rate limiting step with the iron being reduced to Fe(II) [3,4]. The enzyme–alkyl radical complex is then oxidised by molecular oxygen to an enzyme–peroxy radical complex under aerobic conditions, before the transference of electron from the ferrous atom to the peroxy group occurs [14,17]. Protonation and dissociation from the enzyme allow the formation of the hydroperoxide. Under anaerobic conditions, the alkyl radical dissociates from the enzyme–alkyl radical complex and then a mixture of products including dimers, ketones and epoxides is produced by radical reactions [15]. 4. Inhibition of lipoxygenase oxidation Blanching is the inactivation of enzymes that caused undesirable changes during the processing and subsequent storage of the products. It has also a number of other advantages including color stability, improvement in texture and decrease in
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microbial population [39]. Heating vegetables to a temperature high enough to inactivate peroxidase (POD) is generally more than enough to destroy the undesirable enzymes, since POD activity has not been shown to be directly responsible for quality deterioration during frozen storage of vegetables. The use of LOX as indicator of proper blanching has been recommended as more significant in determining storage stability in frozen vegetables [40,41]. LOX has been associated with quality deterioration because of its involvement in off-flavour and odor production, loss of pigments such as carotenes and chlorophylls, and destruction of essential fatty acids [42]. Lipoxygenases can be thermally inactivated above 60 ◦ C with a resulting improvement in the shelf life of foods. However, heating also increases non-enzymatic oxidation and thus may exceed the oxidation due to lipoxygenase [43]. Optimum oxidative stability can be achieved by minimizing exposure of lipids and lipid containing food products to air, light and higher temperatures during processing and storage. Theoretically, the most convenient way of preserving fatty foods from oxidative spoilage is to remove all oxygen from the food during manufacture and from the packaging container. Modern packaging material and equipment allows inert-gas vacuum packaging, but residual oxygen levels of less than 1% are extremely difficult to obtain in a production environment. Liquid oils were traditionally packaged in clear glass containers and brown bottles were sometimes used to protect unstable oils from light oxidation. Glass bottles have now been replaced by plastic containers. Since it is superior to polyethylene, which is more permeable to oxygen, polyvinyl chloride is preferred [15].
[4] [5]
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5. Conclusion [16]
In order to develop new food products, for achieving higher rates and levels of extraction, or improve food quality in terms of, e.g. flavour, some enzymes are positively utilized during food processing for recovery of by-products. On the other hand, enzymes might also have detrimental effects on food quality. Food quality defects can be caused by enzymes naturally present in the food or by enzymes produced by certain microorganisms. Hence, besides microbial inactivation, preservation technologies aim at inactivating enzymes with deteriorative action. Owing to the beneficial and/or detrimental effects of enzymes, control of enzymatic activity is required in many food processing steps. The use of LOX as indicator of proper blanching has been recommended, which is more significant in determining storage stability in frozen vegetables. For industry, rapid detecting methods of LOX activation must be studied. References [1] Casey R. Lipoxygenases. In: Casey R, Shrewy PR, editors. Seed proteins. London: Chapman and Hall; 1998. [2] Casey R, Domoney C, Forster C, Robinson D, Wu Z. In: Fenwick GR, Hedley C, Richards RL, Khokhar S, editors. The significance of plant lipoxygenases to the agrifood industry in agrifood quality: an interdisciplinary approach. The Royal Society of Chemistry; 1996. p. 127–30. [3] Veldink GA, Hilbers MP, Nieuwenhuizen WF, Vliegenthart JFG. In: Rowley AF, K¨uhn K, Schewe T, editors. Plant lipoxygenase: structure and
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Review
Lipoxygenase in fruits and vegetables: A review Taner Baysal a , Aslıhan Demird¨oven b,∗ a
Ege University, Engineering Faculty, Food Engineering Department, Izmir 35100, Turkey b Ege University, Institute of Natural and Applied Sciences, Izmir 35100, Turkey
Received 4 July 2006; received in revised form 27 November 2006; accepted 30 November 2006
Abstract Lipoxygenase (LOX) is one of the most widely studied enzyme in plants and animal kingdom which is found in more than 60 species. Lipoxygenase catalyses the bioxygenation of polyunsaturated fatty acids (PUFA) containing a cis,cis-1,4-pentadiene unit to form conjugated hydroperoxydienoic acids. Lipoxygenases have food-related applications in bread making and aroma production; they also have negative implications for the color, off-flavour and antioxidant status of plant-based foods. The significance of plant lipoxygenase for fruit and vegetables are reviewed with particular reference to the enzymes from plants. Various aspects of the sources of lipoxygenases, their oxidation mechanism, isozymes and inhibition of oxidation are discussed. © 2006 Elsevier Inc. All rights reserved. Keywords: Lipoxygenase; Oxidation mechanism; Isozymes; Inhibition
Contents 1. 2. 3.
4. 5.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Lipoxygenase contents of plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Mechanism of lipoxygenase-catalysed oxidation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Lipoxygenase isozymes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Iron content . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Inhibition of lipoxygenase oxidation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Introduction Lipoxygenase (LOX) is an enzyme that is found in many plants and animals, which catalyses the oxygenation of polyunsaturated fatty acids (PUFA) to form fatty acid hydroperoxides. They are present in a wide range of biological organs and tissues, but they are particularly abundant in grain legume seeds (beans and peas) and potato tubers [1]. Lipoxygenase from different sources, catalyses oxygenation at different points along the carbon chain, referred to as “positional” or “regio” specificity, such specificity has significant implications for the ∗
Corresponding author. E-mail addresses: [email protected] (T. Baysal), [email protected] (A. Demird¨oven). 0141-0229/$ – see front matter © 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.enzmictec.2006.11.025
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metabolism of the resultant hydroperoxides into a number of important secondary metabolites [2,3]. Linoleic and linolenic acid are the major polyunsaturated fatty acids in plant tissues, and insertion of the oxygen takes place at either the 9 or 12 position to generate the corresponding 9- or 13-hydroperoxides. While most LOXs so far characterized are soluble cytosolic enzymes, some are chloroplastic, mitochondrial, or located in the vacuoles. In soybean, lipoxygenases have been identified with involvement in nitrogen and assimilate partitioning and appear to be regulated in response to plant nitrogen status in both tissue-specific and developmentally controlled patterns [1–4]. A key role for some LOX isoforms is in the generation of fatty acid hydroperoxides destined for jasmonic acid (JA), which triggers gene activation during wound response in plants. The fatty acid hydroperoxides generated by the activity of LOX are potentially deleterious to membrane function by
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causing increased rigidity and would not, therefore, be expected to accumulate [4]. Lipoxygenase not only has food-related applications in bread making [5] and aroma production [6]; but also has negative implications for color, off-flavour and antioxidant status of plantbased foods [2]. In many applications it is possible to use crude plant materials or extracts [6], but such materials usually contain multiple enzymes that may reduce polyunsaturated fatty acid substrate availability or metabolize the hydroperoxide products, thereby modulating lipoxygenase action, which has led to understand the activities and properties of plant and other lipoxygenases as food processing additives and to remove selectively specific lipoxygenase from plants based on such understanding [2]. The significance of plant lipoxygenase is reviewed, with particular reference to the enzymes from some fruits and vegetables. Various aspects of the sources of lipoxygenases, their oxidation mechanism, isozymes and inhibition of oxidation are discussed. 2. Lipoxygenase contents of plants There is ample evidence that lipoxygenase is crucial elements of plants defence strategies. Removal of a specific tobacco leaf lipoxygenase, by genetic engineering, converts a strain of tobacco that is resistant to Phytophthora parasitica var. nicotiana to one that is susceptible [7]. Although the mechanism of resistance is unknown, this unambiguously shows that lipoxygenase is an essential part of the resistance. Many plants respond to insect damage or wounding by the production of jasmonate (Fig. 1), and the activation of proteinase inhibitor genes in both wounded and non-wounded leaves [8,9]. Removal of wound-induced lipoxygenase activity from potato leaves eliminates the production of jasmonate and/or proteinase inhibitor in response to wounding, which lead to increased susceptibility to insect attack [9]. Leaves of French beans that are resistant to
Pseudomonas syringae pv phaseolicola show, on infection, an elevated production of six-carbon aldehydes that are believed to derive from lipoxygenase-produced hydroperoxides; the aldehydes are produced in bacteriocidal amounts and thus act as a defence mechanism against Pseudomonas attack [10]. Lipoxygenase in vegetative tissues therefore provide hydroperoxide substrates that can be metabolized to compounds that play important roles in plant defence. Although, it is less clear why seeds and tubers have large amounts of lipoxygenase and in such cases they are possibly dispensable; genetic removal of specific soybean [11] or pea [12] seed isoforms, for instance, appears not to compromise plant health. As part of a drive to understand more fully the roles of various lipoxygenases in plant biology, many of them have been cloned and produced as recombinant enzymes [2]. 3. Mechanism of lipoxygenase-catalysed oxidation Various aspects of the sources of the enzymes, their activities, substrate and product specificities, and co-oxidation potential are discussed in the context of food quality and shelf life. The sequences of lipoxygenases, predicted from DNA sequences, from different plants, are compared and the significance of sequence differences assessed in relation to enzyme specificity and the three-dimensional structure of soybean lipoxygenase1. A novel scheme is proposed for the mechanism of the lipoxygenase-catalysed dioxygenation of polyunsaturated fatty acids in which two different pathways are suggested for the anaerobic and aerobic oxidations (Fig. 2) [13,14]. 3.1. Lipoxygenase isozymes The enzyme lipoxygenase (linoleate oxygen oxidoreductase, EC 1.13.11.12) is present in a wide variety of plant and animal tissues [15]. The enzyme in oil-bearing seeds, e.g. soybeans,
Fig. 1. Parts of the pathway of plant oxylipin metabolism leading from linolenic acid to jasmonate and volatile aldehydes [2].
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Fig. 2. Pathway of lipoxygenase-catalysed oxidation [14].
can be an important source of hydroperoxides formed in the oil during extraction. In vegetables, oxidative changes due to the enzyme may lead to off-flavours during storage. The enzyme does, however, contribute to flavor formation in some plant foods including tomato and cucumber. Lipoxygenase activity requires the presence of free polyunsaturated fatty acids. Linoleic acid is the most common substrate in plant-based foods. The enzyme occurs in a variety of isozymes, which often vary in optimum pH, as well as product and substrate specificity. Lipoxygenase catalyses the bioxygenation of polyunsaturated fatty acids containing a cis,cis-1,4-pentadiene unit to form conjugated hydroperoxydienoic acids [16]. Lipoxygenase from soybean seed is the best characterized among plant LOX, although the physiological roles of these enzymes are not completely known [17]. Soybean seed lipoxygenase catalyses the hydroperoxidation of polyunsaturated fatty acids, such as linoleic and linolenic acids, leading to the production of several reactive molecules that account for the grassy beany taste in soybean processed foods. In soybean leaves, LOX has been intensively examined [18] but the diversity and characteristics of the different forms of LOX are not yet known. Given the occurrence of multiple LOX isoenzymes in soybean leaves and the proposed roles of these enzymes in the plant metabolism, it is possible that individual isoenzymes play specific functions [19]. Soybean lipoxygenase is the most extensively studied for which molecular structure has been reported by Boyington et al. [20]. Four isozymes have been isolated from soybeans: (1) Soy isozyme has an optimum pH of 9.0. It only acts on free polyunsaturated fatty acids and it forms 9- and 13hydroperoxides in the ratio of 1:9 at room temperature [20]. Some types of lipoxygenases can also catalyse the co-oxidation of carotenoids in the presence of PUFAs. Soybean lipoxygenase type-1 (LOX-1) has been used for the bleaching of wheat flour and also been shown to act as a
bread improver and a valuable processing aid during dough development [21]. (2) Soy isozyme has an optimum pH of 6.8, it acts on triglycerides as well as free polyunsaturated fatty acids and it forms 9- and 13-hydroperoxide in the ratio of about 1:1 at room temperature [20]. A bleached color can also indicate deterioration in either fresh vegetables, such as yellow French beans or fruits and processed food products, where carotenoids are important natural colorants and antioxidants. It has been reported that type-2 lipoxygenases (LOX-2 and -3) of soybean, pea and wheat are pigment bleachers in the presence of linoleic acid [22], but most of the reported studies for the co-oxidation of carotenoids have been for soybean LOX-1. It has been claimed that, under anaerobic conditions, this enzyme shows strong co-oxidising activities in the presence of PUFA or a corresponding acyl hydroperoxide [23], whereas, under aerobic conditions, it is not an efficient catalyst for the bleaching reaction [24,13,1,25]. (3) Soy isozyme is similar to isozyme 2, but its activity is inhibited by calcium ions, whereas lipoxygenase-2 is stimulated by the metal [20]. (4) Lipoxygenase is very similar to isozyme 3, but can be separated by gel chromatography or electrophoresis [20]. Lipoxygenase isozymes are commonly classified as type 1, which have an optimum pH in the alkaline region and are specific for free fatty acids and type 2, which has optimum activity at neutral pH and causes co-oxidation of carotenoids. The ability of lipoxygenase type 2 to bleach carotenoids has found practical application in the addition of soybean flour to wheat flour in order to bleach the flour in the manufacture of white bread [16]. For LOX-3 an increase in foaming activity has been reported, as well as an overall improvement in bread making quality of wheat flour. The bakery yeast Saccharomyces cerevisiae also contains LOX. Recently, this enzyme was partially purified, but
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its potential, if any, on bread making remains to be established. Nowadays, it is feasible to change the profile and content of LOX (iso)enzymes in plants either by classical means, or potentially by genetic modification [7,25]. For example, by appropriate crosses, near-isogenic soybean seeds have been developed that lack either isoenzymes L1 and L3, or isoenzymes L2 and L3. These LOX-minus mutants still grow well in the field. In principle, transgenic plants lacking or over expressing one or more LOX isoenzymes could be constructed and tailored to specific applications [20]. To that end, the heterologous expression of one or more soybean LOX isoenzymes in wheat could be of interest. It is interesting to note that the use of soybean lipoxygenase was described in the 1930s as a means to bleach the flour in preparation of white bread. More recent experiments have shown that carotenoids present in wheat flour are destroyed by co-oxidation. Wheat flour itself contains little LOX activity, but LOX is abundantly present in soybeans [4,11,16]. To that end, wheat flour is often fortified with up to 0.5% enzyme-active soy flour. Other applications of LOX include the bleaching of noodles, whey products, rice and wheat bran [4]. In plant tissues, various enzymes occur that cause the conversion of hydroperoxides to other products, some of which are important as flavour compounds. These enzymes include hydroperoxide lyase, which catalyses the formation of aldehydes and oxo acids, hydroperoxide-dependent peroxygenase and epoxygenase, which catalyse the formation of epoxy and hydroxy fatty acids, and hydroperoxide isomerase, which catalyses the formation of epoxyhydroxy fatty acids and trihydroxy fatty acids. Lipoxygenase produces similar flavour volatiles to those produced during autoxidation, although the relative proportions of the products may vary widely depending on the specificity of the enzyme and the reaction conditions [16]. Potato lipoxygenase, although up to date studies have not well realized, is unusual as it is a plant enzyme, which resembles mammalian lipoxygenase and catalyses the oxidation of the 20-carbon atom PUFA, arachidonic acid, to form 15hydroperoxyeicosatetraenoic acid as the major product [9,15]. In animals, this hydroperoxide is the precursor of biologically active compounds of considerable pharmaceutical interest. Thus, potato lipoxygenase is of special interest because of its greater availability and its potential use as a model and alternative for the mammalian enzyme. Three isoenzymes of lipoxygenase have been isolated from potato [26] and defined as LOX-1, -2 and -3. Linoleic acid has been claimed to be the preferred substrate for potato LOX-1 and the 9-hydroperoxide as the dominant product. On the other hand, linolenic acid has been claimed as the preferred substrate for both potato LOX-2 and -3, which produce the 13-hydroperoxide as the main product. Also potatoes contain different leaf and tuber lipoxygenases [26] with different regiospecificities; the leaf lipoxygenase that produces 13-hydroperoxides from linolenic acid is involved in the synthesis of jasmonate [27,28], an important elicitor of plant defence gene expression, through the so-called “octadecanoid signalling” pathway [8]. Tomato also contain a fruit 9-lipoxygenase activity and a leaf activity [29,30]. In tomatoes at least two isoenzymes have
been identified different thermal stabilities. Similarly, resistant and labile lipoxygenase isoenzymes have already been observed in many vegetable products (potato, wheat germ, green beans, peas), as well as in tomato [31]. This LOX activity also causes color degradation for frozen tomato cubes during storage. In tomato cubes, LOX activity was investigated during frozen storage and it has been observed that LOX activity was increased during storage. In order to prevent color degradation of tomato cubes, they were coated by modified starch. The results showed that LOX activity decreased and the color was found better than the uncoated samples during frozen storage [32]. The cucumber LOX enzyme was similar to the potato and tomato enzymes, both in pH characteristics and substrate specificity [33]. In apples, LOX activity during storage was investigated in the core, flesh and peel. Activity was always highest in the core and peel. On storage, activity was increased in each part of the fruit but especially in the core and peel. Increase in LOX preceded the browning of the core. LOX may be responsible for the browning and may be concerned in the induction of superficial scald [34]. LOX has been reported to be involved in ripening process in strawberry fruit and thus, albino fruit have lower LOX activity due to poor color development in them [35]. Pea has a complex lipoxygenase gene family with at least five enzymes each in seeds [36] and nodules [37] and yet more in stems and roots [36]. In some species the leaf enzymes have been shown to be targeted to the chloroplast [26,28]; such plastidial enzymes are sufficiently different from other lipoxygenases to be classified as a separate group [38]. 3.2. Iron content Lipoxygenase molecules contain one atom of iron. The iron atom is in the high spin Fe(II) state in the native resting form of lipoxygenase, and must be oxidised to Fe(III) by the reaction product, fatty acid hydroperoxides or hydrogen peroxide before activating as an oxidation catalyst [1,2]. As a consequence of this requirement for oxidation of the iron in the enzyme, a lag period is observed, when the enzyme is used with pure fatty acid substrates. The active enzyme abstracts a hydrogen atom stereospecifically from the intervening methylene group of a polyunsaturated fatty acid in a rate limiting step with the iron being reduced to Fe(II) [3,4]. The enzyme–alkyl radical complex is then oxidised by molecular oxygen to an enzyme–peroxy radical complex under aerobic conditions, before the transference of electron from the ferrous atom to the peroxy group occurs [14,17]. Protonation and dissociation from the enzyme allow the formation of the hydroperoxide. Under anaerobic conditions, the alkyl radical dissociates from the enzyme–alkyl radical complex and then a mixture of products including dimers, ketones and epoxides is produced by radical reactions [15]. 4. Inhibition of lipoxygenase oxidation Blanching is the inactivation of enzymes that caused undesirable changes during the processing and subsequent storage of the products. It has also a number of other advantages including color stability, improvement in texture and decrease in
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microbial population [39]. Heating vegetables to a temperature high enough to inactivate peroxidase (POD) is generally more than enough to destroy the undesirable enzymes, since POD activity has not been shown to be directly responsible for quality deterioration during frozen storage of vegetables. The use of LOX as indicator of proper blanching has been recommended as more significant in determining storage stability in frozen vegetables [40,41]. LOX has been associated with quality deterioration because of its involvement in off-flavour and odor production, loss of pigments such as carotenes and chlorophylls, and destruction of essential fatty acids [42]. Lipoxygenases can be thermally inactivated above 60 ◦ C with a resulting improvement in the shelf life of foods. However, heating also increases non-enzymatic oxidation and thus may exceed the oxidation due to lipoxygenase [43]. Optimum oxidative stability can be achieved by minimizing exposure of lipids and lipid containing food products to air, light and higher temperatures during processing and storage. Theoretically, the most convenient way of preserving fatty foods from oxidative spoilage is to remove all oxygen from the food during manufacture and from the packaging container. Modern packaging material and equipment allows inert-gas vacuum packaging, but residual oxygen levels of less than 1% are extremely difficult to obtain in a production environment. Liquid oils were traditionally packaged in clear glass containers and brown bottles were sometimes used to protect unstable oils from light oxidation. Glass bottles have now been replaced by plastic containers. Since it is superior to polyethylene, which is more permeable to oxygen, polyvinyl chloride is preferred [15].
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5. Conclusion [16]
In order to develop new food products, for achieving higher rates and levels of extraction, or improve food quality in terms of, e.g. flavour, some enzymes are positively utilized during food processing for recovery of by-products. On the other hand, enzymes might also have detrimental effects on food quality. Food quality defects can be caused by enzymes naturally present in the food or by enzymes produced by certain microorganisms. Hence, besides microbial inactivation, preservation technologies aim at inactivating enzymes with deteriorative action. Owing to the beneficial and/or detrimental effects of enzymes, control of enzymatic activity is required in many food processing steps. The use of LOX as indicator of proper blanching has been recommended, which is more significant in determining storage stability in frozen vegetables. For industry, rapid detecting methods of LOX activation must be studied. References [1] Casey R. Lipoxygenases. In: Casey R, Shrewy PR, editors. Seed proteins. London: Chapman and Hall; 1998. [2] Casey R, Domoney C, Forster C, Robinson D, Wu Z. In: Fenwick GR, Hedley C, Richards RL, Khokhar S, editors. The significance of plant lipoxygenases to the agrifood industry in agrifood quality: an interdisciplinary approach. The Royal Society of Chemistry; 1996. p. 127–30. [3] Veldink GA, Hilbers MP, Nieuwenhuizen WF, Vliegenthart JFG. In: Rowley AF, K¨uhn K, Schewe T, editors. Plant lipoxygenase: structure and
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[35] Sharma RR, Krishna H, Patel VB, Dahuja A, Singh R. Fruit calcium content and lipoxygenase activity in relation to albinism disorder in strawberry. Scientia Horticulturae 2006;107:150–4. [36] Domoney C, Firmin JL, Sidebottom C, Ealing PM, Slabas A, Casey R. Lipoxygenase heterogeneity in Pisum sativum. Planta 1990;181: 35–43. [37] Wisniewski JP, Gardner CD, Brewin NJ. Isolation of lipoxygenase cDNA clones from pea nodule mRNA. Plant Mol Biol 1999;39:775–83. [38] Shibata D, Slusarenko A, Casey R, Hildebrand D, Bell E. Lipoxygenases. Plant Mol Biol Rep 1994;12(CPGN Suppl.):41–2. [39] Murcia MA, Lopez-Ayerra B, Garcia-Carmona F. Effect of processing methods and different blanching times on broccoli: proximate composition and fatty acids. Lebensmittel-Wissenschaft und Technologie 1999;32:238–43. [40] Williams DC, Lim MH, Chen AO, Pangborn RM, Whitaker JR. Blanching of vegetables for freezing—which indicator enzyme to choose. Food Technol 1986;40:130–40. [41] Sheu SC, Chen AO. Lipoxygenase as blanching index for frozen vegetable soybeans. J Food Sci 1991;56(2):448–51. [42] King DL, Klein BP. Effect of flavonoids and related compounds on soybean lipoxygenase-1 activity. J Food Sci 1987;52(1):220–1. [43] Wang YJ, Miller LA, Addis PB. Effect of heat inactivation of lipoxygenase on lipid oxidation in lake herring (Coregonus artedii). J Am Oil Chem Soc 1991;68:752–5.