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. 2020 Nov 2;58(11):4178–4184. doi: 10.1007/s13197-020-04886-5

Inhibitory effect of Malaysian coastal plants on banana (Musa acuminata colla “Lakatan”), ginger (Zingiber officinale Roscoe) and sweet potato (Ipomoea batatas) polyphenol oxidase

Win Yee Lim 1, Yi Wei Cheng 1, Li Bin Lian 1, Eric Wei Chiang Chan 2, Chen Wai Wong 1,✉
PMCID: PMC8405737  PMID: 34538902

Abstract

Undesired browning reaction catalyzed by polyphenol oxidase (PPO) has reduced the nutritional quality and customer acceptance of the products. The inhibitory effects of six coastal plants including Sonneratia alba, Rhizophora apiculata, Syzygium grande, Rhizophora mucronata, Hibiscus tiliaceus and Bruguiera gymnorhiza on PPO in banana, sweet potato and ginger were studied based on oxidation of pyrocatechol. Banana exhibited the highest PPO activity (141,600 U), followed by sweet potato (43,440 U) and ginger (26,880 U). Banana PPO was strongly inhibited by R. apiculata (70.87%) and sweet potato PPO was strongly inhibited by S. alba (82.00%). In general, most banana PPO was the most susceptible to inhibition with all inhibitors having inhibition higher than 60.00% at 0.5 mg/ml and ginger PPO was the least susceptible with all inhibitors showing less than 50.00% inhibition at 0.5 mg/ml. Coastal plant extracts are potentially to be developed as natural inhibitors for preventing enzymatic browning of fruits and vegetables.

Keywords: Polyphenol oxidase, Coastal plant extracts, Natural inhibitor, Browning reaction

Introduction

Polyphenol oxidase (PPO) (EC 1.14.18.1) is a copper containing enzyme that catalyses the phenolic compounds oxidation forming corresponding quinone intermediates that polymerize to form pigments in the presence of oxygen. The process of pigmentation occurred in food is called enzymatic browning, which is a very common issue found on various type of fruits and vegetables. Browning reaction results in changes of the appearance, aromatic, flavour, texture and also nutritional value of food. Browning reaction may be beneficial for the production of coffee, cocoa and tea. However, it is considered undesirable in food industry, especially for fresh-cut industry. This is because mechanical injury allows the contact between phenolic compounds from vacuoles and PPO from chloroplast (Taranto et al. 2017).

Research on controlling and preventing food browning are being carried out in order to reduce the amount of food waste caused by enzymatic browning reaction. Chemicals such as antioxidant, chelating agents and acidifying agents and physical treatment like freezing and blanching have been used in previous studies to inhibit the PPO activity from various sources (Ali et al. 2014; Lim and Wong 2018). However, some of the chemical agents that act as food additives and preservatives were found to cause allergies in consumers (Bahna and Burkhardt 2019). Thus, research on studying the effect of natural inhibitors on PPO activity is in need.

Banana (Musa acuminata), is an important tropical fruit crop and has a capital economic importance all over the tropical regions of the world. It is either eaten raw or processed, and also as a functional ingredient in various food products. Kumar et al. (2012) and Sidhu and Zafar (2018) have reported large amount of health promoting components like potassium, vitamins and some phenolics compounds in banana.

Ginger (Zingiber officinale Roscoe) belongs to the family Zingiberaceae, which the rhizome part is widely used as a spice, condiment and ingredient in traditional herbal medicine and other products such as ginger oil and flavouring tea. Ginger is found to be effective against several pharmacological actions which are attributed to its rich phytochemicals (Radhika et al. 2017).

Sweet potato (Ipomoea batatas) is a well-known long-term species with moist and delicate tubers with a sweetish taste, pleasant and aromatic smell. It is a valuable medicinal food with high nutritional properties and also with acclaimed sources for natural products. Sweet potato is rich in dietary fibre, minerals and vitamins, providing over 90% of nutrients per calorie required for most people (Mohanraj and Sivasankar 2014).

Coastal forests are believed to play vitally important roles in shoreline protection and providing habitat for juvenile fish and other reef species. Few studies have documented the bioactivity such as antioxidant and antityrosinase activity of the huge number of novel metabolites found in coastal plants (Dahibhate et al. 2019; Suganthy and Devi 2015). Limited information was obtained for their effect on the PPO activity.

Six coastal plants namely Sonneratia alba, Rhizophora apiculata, Syzygium grande, Rhizophora mucronata, Hibiscus tiliaceus and Bruguiera gymnorhiza were chosen for this study. Some parts of the chosen plants such as fruits, leaves and shoots are edible. For example, leaves of H. tiliaceus can be eaten raw or cooked, while the leaves of R. mucronata were used as an alternative source of tea (Abdul-Awal et al. 2016; Suganthy and Devi 2016). The purpose of this study was to evaluate the inhibition properties of the six coastal plants on PPO extracted from banana, ginger and sweet potato.

Materials and methods

Chemicals and reagents

All reagents and solvents used in this study were of analytical grade. Phosphate buffer solution was prepared using anhydrous di-sodium hydrogen phosphate from Systerm (Malaysia) and anhydrous sodium dihydrogen phosphate from Merck (Germany). Dimethyl sulfoxide (DMSO) and pyrocatechol was purchased from Merck (Germany), methanol was obtained from Systerm (Malaysia) and polyvinylpyrrolidone (PVP) was purchased from Sigma (Germany).

Plant materials

“Lakatan” banana (Musa acuminata colla “Lakatan”), ginger (Zingiber officinale Roscoe) and yellow sweet potato (Ipomoea batatas) originated from Philippines, Malaysia and China, respectively were bought from NSK Trade City (Kuchai Lama, Kuala Lumpur, Malaysia). In this study, six types of Malaysian coastal plants were chosen as natural inhibitors, namely Sonneratia alba, Rhizophora apiculata, Syzygium grande, Rhizophora mucronata, Hibiscus tiliaceus and Bruguiera gymnorhiza. These coastal plant leaves were freshly collected from Pulau Indah and Telok Gong, Klang, Malaysia.

Extraction of crude PPO

Crude PPO was extracted from banana, ginger and sweet potato according to the methods by Ng and Wong (2015) with slight modification. Banana, ginger and sweet potato were first washed, peeled and cut into small pieces (1 cm × 1 cm × 1 cm). The plant materials (50 g) were then homogenized with 2% (w/v) PVP dissolved in 50 mL of 0.1 M prechilled (4 °C) sodium phosphate buffer (pH 6.5) at 22,000 rpm for 1 min using LB-8011ES industrial blender (Waring, USA). The homogenate was filtered with gauze and cotton in ice and centrifuged at 7,000 rpm for 20 min at 4 °C. The supernatant was filtered again using Whatman filter paper No.1, pore size 11 μm. Crude PPO extract obtained was stored at 4 °C for further usage.

Extraction of natural inhibitors

The leaves of coastal plants were extracted as described by Begashaw et al. (2017). The leaves were washed, blot dried and cut into small pieces before oven dried at 50 °C. 10 g of dried leaves were then powdered using a grinder (HR2021/75, Philips, Malaysia) prior to extraction using 200 mL of methanol with continuous swirling (150 rpm) overnight at room temperature using an orbital shaker (SI500, Stuart, United Kingdom). Extracts were obtained through filtration using filter paper (Whatman No.1) and rotary evaporation (50 °C). Further oven-drying process was done at 50 °C. The extracts were stored in sample bottle at room temperature for further use.

PPO assay

PPO activities of banana, ginger and sweet potato were determined by measuring the increase in absorbance at 410 nm for pyrocatechol according to the method of Lin et al. (2016) with slight modifications. Enzyme solution (50µL) was mixed with 650 µL 0.1 M sodium phosphate buffer, pH 6.5, and incubated at 37 °C for 1 min. 300µL of 0.1 M pyrocatechol was then added into the mixture and absorbance was measured using spectrophotometer (Secomam UviLine 9400, Champigny-sur-Marne, France) at 15 s interval for 5 min at room temperature. A mixture of 700µL 0.1 M sodium phosphate buffer, pH 6.5 and 300µL 0.1 M pyrocatechol was used as blank. A 20 × dilution of crude banana PPO extract was used due to the high enzyme activity. Initial velocity for quinone formation was monitored and obtained from the slope of the graph of absorbance against time. Enzyme unit was calculated, where one unit (U) of PPO activity was defined as the amount of enzyme that caused a 0.001 absorbance change per min (Lim and Wong 2018).

Effect of coastal plant extracts on PPO activity of banana, ginger and sweet potato

The coastal plant extracts stock solution (10 mg/mL) were prepared by using dimethyl sulfoxide (DMSO). The PPO inhibitory effect of these extracts on banana, ginger and sweet potato PPOs were studied with different concentrations of coastal plant extracts (0.125 mg/mL, 0.25 mg/mL and 0.5 mg/mL). PPO activities of banana, ginger and sweet potato in the presence of natural inhibitors were assayed using various concentration of pyrocatechol (10–100 mM). Mixture of 50µL enzyme, 450µL 0.1 M phosphate buffer, pH 6.5, and 200µL natural inhibitors were subjected to incubation at 37 °C. After 1 min of incubation, 300 µL of substrate was added and the PPO activity was determined (Lin et al. 2016). The results were reported as percentage inhibition (%) using the PPO activity without inhibitor as initial activity. Lineweaver–Burk plots were plotted for enzyme activities without inhibitors and with inhibitors. I50 value, Michaelis–Menten constant (Km), maximum velocity (Vmax), inhibition constant (Ki) and type of inhibition were determined.

Statistical analysis

All experimental data obtained were analyzed using Microsoft Office Excel 2013. All assays were carried out in triplicate (n = 3). The data were presented as means ± standard deviation (STD) and percent relative activity.

Results and discussion

PPO assay

Pyrocatechol, an excellent substrate for measuring PPO activity was used in this study (Benaceur et al. 2019). Banana exhibited the highest PPO activity (141,600 U), followed by sweet potato (43,440 U) and ginger (26,880 U). The PPO activities of these three plant sources were found to be lower than that of Whangkeumbae pear (1,617,000 U) and Chinese parsley (1,300,000 U) as reported by Zhou et al. (2018) and Lin et al. (2016), respectively. However, the PPO activities were higher than that of round brinjal (7,650 U) as reported by Ng and Wong (2015). The difference of PPO activity in different fruits and vegetables are affected by several factors that involved total phenol (TP) concentration, amount of polyphenol oxidase (PPO) and peroxidase (POX) enzymes as well as the presence of ascorbic acid and other bioactive compounds (Koushesh Saba and Moradi 2016).

Effect of coastal plants extracts on banana, ginger and sweet potato PPO activity

Table 1 show the inhibitory effect of the coastal plant extracts towards banana PPO activity. It can be seen that all the coastal plant extracts (0.5 mg/mL) were able to inhibit more than 60.00% of banana PPO. Moreover, all coastal plant extracts with low concentration (0.125 mg/mL) exhibited an inhibition percentage (45.63–64.08%) towards banana PPO activity which inhibit nearly or higher than 50.00% of the PPO activity of banana, except H. tiliaceus and B. gymnorhiza. R. apiculata shown the highest inhibitory effect (70.87%) on banana PPO among all the coastal plant extracts.

Table 1.

Effect of inhibitors on banana polyphenol oxidase. Km, Vmax, Ki and I50 values were shown

Inhibitors [I] (mg/mL) I50 (mg/mL) Inhibition (%) Vmax (EU/min/mL) Km (mM) Ki (mM) Type of inhibition
Control – 383,731.33 79.36 –
Sonneratia.alba 0.125 0.132 50.49 114,331,19 28.93 0.05/1.22 Mixed
0.25 52.43 101,532.43 26.90 0.09/1.28
0.5 61.17 95,152.01 25.98 0.17/1.32
Rhizophora apiculata 0.125 0.006 64.08 136,209.72 76.12 0.07 Non-competitive
0.25 68.93 124,773,54 77.03 0.12
0.5 70.87 103,146.06 76.00 0.18
Syzygium grande 0.125 0.054 55.34 159,929.89 76.28 0.09 Non-competitive
0.25 57.28 156,006.24 79.88 0.17
0.5 63.11 134,779.06 76.57 0.27
Rhizophora mucronata 0.125 0.194 45.63 108,920.72 35.96 0.05/1.59 Mixed
0.25 54.37 93,735.65 33.45 0.08/1.72
0.5 63.11 88,813.10 32.41 0.15/1.76
Hibiscus tiliaceus 0.125 0.401 22.33 184,188.52 81.82 0.12 Non-competitive
0.25 32.04 158,911.01 79.39 0.18
0.5 61.17 155,864.72 80.10 0.34
Bruguiera gymnorhiza 0.125 0.254 35.92 120,276.30 47.25 0.06/1.90 Mixed
0.25 58.25 104,697.68 44.43 0.09/2.05
0.5 60.19 100,596.23 43.95 0.18/2.11
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According to Table 2, the inhibitory effect of coastal plant extracts on ginger PPO was less than 50.00% (10.80–44.13%). Low concentration (0.125 mg/mL) of S. alba, R. apiculata and S.grande exhibited a higher inhibition percentage (23.47–32.39%) towards ginger PPO than R. mucronata, H. tiliaceus and B. gymnorhiza (10.80–15.0.49%). A totally converse outcome was obtained when higher concentration (0.5 mg/mL) of the coastal plant extracts were used in which R. mucronata, H. tiliaceus and B. gymnorhiza exhibited a slightly higher inhibition percentage.

Table 2.

Effect of inhibitors on ginger polyphenol oxidase. Km, Vmax, Ki and I50 values were shown

Inhibitors [I] (mg/mL) I50 (mg/mL) Inhibition (%) Vmax (EU/min/mL) Km (mM) Ki (mM) Type of inhibition

Control

Sonneratia.alba

 25,241.12 3.29
0.125 1.013 24.88 17,420.45 3.28 0.28 Non-competitive
0.25 34.27 15,994.98 3.24 0.43
0.5 35.68 15,305.64 3.28 0.77
Rhizophora apiculate 0.125 0.672 23.47 18,570.31 4.31 0.35/1.78 Mixed
0.25 39.44 15,392.52 4.72 0.39/2.35
0.5 40.85 15,038.48 5.02 0.74/2.56
Syzygium grande 0.125 1.005 32.39 17,515.04 2.45 0.28 Un-competitive
0.25 35.21 15,740.07 2.16 0.41
0.5 39.91 15,106.13 2.08 0.75
Rhizophora mucronata 0.125 0.535 15.49 21,311.33 2.95 0.68 Un-competitive
0.25 41.31 14,656.42 2.16 0.35
0.5 44.13 13,864.16 2.03 0.61
Hibiscus tiliaceus 0.125 0.560 14.55 21,418.46 3.49 0.70/1.25 Mixed
0.25 36.62 15,393.00 3.81 0.39/1.90
0.5 43.19 14,328.29 3.91 0.66/2.09
Bruguiera gymnorhiza 0.125 0.527 10.80 22,194.50 2.86 0.91 Un-competitive
0.25 39.44 14,570.95 1.86 0.34
0.5 44.13 13,523.47 1.70 0.58
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Inhibitory effect of the coastal plants towards sweet potato PPO was shown in Table 3. H. tiliaceus and B. gymnorhiza exhibited relatively low inhibition towards sweet potato PPO in which they inhibited less than 50.00% of PPO activity even when 0.5 mg/mL plant extracts were used. S. alba was the most effective inhibitor for sweet potato PPO as it inhibited up to 82.00% of the PPO activity.

Table 3.

Effect of inhibitors on sweet potato polyphenol oxidase. Km, Vmax, Ki and I50 values were shown

Inhibitors [I] (mg/mL) I50 (mg/mL) Inhibition (%) Vmax (EU/min/mL) Km (mM) Ki (mM) Type of inhibition
Control – 43,264.76 11.67
Sonneratia.alba 0.125 0.081 55.14 17,232.08 4.78 0.08 Un-competitive
0.25 78.57 8,203.78 2.68 0.06
0.5 82.00 7,421.59 2.50 0.10
Rhizophora apiculate 0.125 0.217 40.86 24,854.79 6.11 0.17 Un-competitive
0.25 58.29 17,105.07 4.28 0.16
0.5 62.29 14,960.92 3.71 0.26
Syzygium grande 0.125 0.286 37.14 26,418.06 6.34 0.20 Un-competitive
0.25 54.00 18,898.59 4.17 0.19
0.5 59.71 17,217.78 3.68 0.33
Rhizophora mucronata 0.125 0.385 32.00 26,017.07 11.70 0.08 Non-competitive
0.25 44.29 20,816.98 11.76 0.23
0.5 56.29 17,183.19 11.72 0.33
Hibiscus tiliaceus 0.125 0.633 24.00 32.819.17 13.67 0.39/1.54 Mixed
0.25 33.71 29,392.49 14.18 0.53/1.79
0.5 42.86 20,497.77 15.64 0.45/2.82
Bruguiera gymnorhiza 0.125 0.673 24.29 29,230.62 11.67 0.26 Non-competitive
0.25 39.14 24,382.57 11.59 0.32
0.5 41.14 19,483.80 11.68 0.41
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It is found that the inhibitory effect of all coastal plant extracts on PPO of banana, ginger and sweet potato were comparable with some chemical inhibitors such as sodium chloride, citric acid and ascorbic acid that were reported by Ali et al. (2014), Lim and Wong (2018) as well as Lim et al. (2019). This indicates that coastal plants, especially R. apiculata and S. alba, could replace the usage of chemicals in inhibiting browning reaction. The inhibition of ginger and sweet potato PPO by coastal plant extracts were also comparable with some natural inhibitors like honey and onion extracts (Lim and Wong 2018; Lim et al 2019).

Inhibition percentage increases as the concentration of natural inhibitors increase from 0.125 to 0.5 mg/mL. This indicates that coastal plant extracts with a higher concentration exhibited a stronger inhibition on banana, ginger and sweet potato PPOs. Inhibition capability of the inhibitors can be determined based on I50 value, which is defined as the concentration of inhibitors required to inhibit 50.00% of enzyme activity at a particular substrate concentration. R. apiculata and S. alba exhibited the lowest I50 values among all extracts towards banana PPO (0.006 mg/mL) and sweet potato PPO (0.081 mg/mL), respectively.

Parameters of inhibition such as Km, Vmax and Ki values as well as type of inhibition were also shown in Tables 1, 2 and 3. Lower Vmax values were obtained for all inhibitors as compared to the initial Vmax values of control. This indicates that the maximum reaction rate of PPO reduced in the presence of coastal plant extracts. Km value determines the binding affinity of PPO for substrates, in which the lower the Km value, the stronger the binding of enzyme to substrate (Bisswanger 2017). For example, banana PPO with S. alba (Table 1) showed a lower Km value than control, which indicates that S. alba had a stronger binding affinity towards banana PPO.

Besides, Km and Vmax values are related to the type of inhibition for different inhibitors. Non-competitive inhibitor would exhibit a lower Vmax value and similar Km value, while un-competitive inhibitor exhibits a lower Vmax and Km values (Yadav and Magadum 2017). Ki value is calculated after the determination of type of inhibition for each inhibitor. Similar to Km value, a lower Ki value indicates a better binding affinity of inhibitors towards enzyme. For sweet potato PPO, S. alba exhibited the lowest Ki value (0.08–0.1 mM) (Table 3), which means that it would binds strongly to the PPO.

According to Tables 1, 2 and 3, different types of inhibition were determined when various coastal plants extracts were used on PPO from banana, ginger and sweet potato. S. alba acted as mixed, non-competitive and uncompetitive inhibitors toward banana (Table 1), ginger (Table 2) and sweet potato (Table 3) PPO, respectively. The difference in inhibitory effect of the coastal plants on PPO studied could due to the presence of different PPO isomers in the food. Studies have proven the phenol content, antioxidant and tyrosinase inhibitory activities of S. alba leaves and fruits (Djuhria et al. 2017; Suh et al. 2014). Thus, the phytochemicals in S. alba leaves may contributed to its tyrosinase inhibitory activities.

The effect of PPO inhibition by R. apiculata was more prominent in banana (Table 1) and sweet potato (Table 3) as compared to ginger (Table 2). In the year of 2007, Loo et al. had proposed the total phenolics content, free radical scavenging activity, reducing power and antioxidant activity of the pyroligneous acid from R. apiculata. The results imply that the R. apiculata might be a potential source of natural antioxidants (Gao and Xiao 2012). The antioxidant effect of pyroligneous acid in R. apiculata may contribute to its ability to control browning reaction. Antioxidants can prevent the initial reaction of polyphenol oxidase by reacting with oxygen. It can also revert the PPO activity by reducing the o-quinone back to o-diphenol (Gögüs et al. 2009).

S.grande was reported to be a potent antioxidant in free radical scavenging activity test using 2,2-diphenylpicrylhydrazyl (DPPH) and 2,2′-azino-bis(3-ethylbenzothiazoline-6-sulfonic acid (ABTS) assay (Jothiramshekar et al. 2014). Ajam (2014) also proposed that S. grande extract can be considered as promising candidates for the development of an antimicrobial and antioxidant agents. The phytochemicals including triterpenoids, sterols and flavonoids present in S. grande extract, may be responsible for its antioxidant activity, which inhibit the production of brown pigment (Samy et al. 2014). As shown in Table 1, S. grande extract non-competitively inhibits banana PPO, whereas it inhibits both ginger and sweet potato PPO uncompetitively.

R. mucronata inhibits banana PPO the most (45.63–63.11%) (Table 1), followed by sweet potato PPO (32.00–56.29%) (Table 3) and ginger PPO (15.49–44.13%) (Table 2). These results clearly indicated that R. mucronata is a potent inhibitor of PPO and it is suitable to be used as natural anti-browning agent. According to Sur et al. (2015), R. mucronata exhibited some major phytoconstituents such as alkaloids, phenolics, flavonoids, triterpenoids, steroids, glycosides, saponins, and tannins. It has been recognized that phenolics and flavonoids was responsible for the antioxidant and radical scavenging properties of R. mucronata. PPO would bind to the phytoconstituents, which are alternative substrates instead of binding to the original substrates (catechol). Hence, reduce the formation of quinone and diphenols (Ali et al. 2014).

According to Wong et al. (2010), H. tiliaceus was found to exhibit antioxidant and anti-tyrosinase activity. The outstanding antioxidant properties could be due to the high phenolic and flavonoid content of the plant extracts. The presence of phytochemicals like tannins and flavonoids in H. tiliaceus were also reported by Abdul-Awal et al. (2016). Reducing agents or antioxidants can prevent the initial reaction of tyrosinase by reacting with oxygen and also reduce the o-quinone back to o-diphenol. Therefore, this has linked to its browning inhibitory attribute. As shown in Table 1, non-competitive inhibition by H. tiliaceus was observed for banana PPO, whereby mixed-type-inhibition was determined for both ginger PPO and sweet potato PPO. Similar result was also reported by Lim and Wong (2018), a mixed-type-inhibition (28.38%) on ginger PPO was found when natural inhibitor (onion) was used. A mixed type inhibition may be due to the presence of various compounds found in the plant extracts (Mannering, 2013).

Similar as H. tiliaceus, B. gymnorhiza exhibits the greatest inhibition on banana PPO (Table 1), followed by ginger PPO (Table 2) and sweet potato PPO (Table 3). B. gymnorhiza is a potential source of bioactive compounds. It contains a substantial number of flavonoids and other phenolic compounds such as gallic acid, quercetin, and coumarin, which could exerts powerful antioxidant properties (Sur et al. 2016; Sudirman et al. 2014). Mahmud et al. (2017) has also reported the presence of metabolites like gallic acid, vanillic acid, vanillin and ellagic acid in B. gymnorhiza. These organic acids can act as chelating agents, which could chelate the copper at PPO active site and stop the enzyme’s catalytic action (Silvera et al. 2015).

Conclusion

This study concluded that coastal plants can be used as potent natural inhibitor for PPO from banana, ginger and sweet potato. R. apiculata and S. alba exerted the greatest inhibitory effect on banana PPO (70.87%) and sweet potato PPO (82.00%). Most of the natural inhibitors (0.5 mg/mL) worked well in inhibiting banana and sweet potato PPOs (41.14–82.00%), but not for ginger PPO. It is worthwhile to further study the inhibitory effect of S. alba and R. apiculata towards PPO of fruits and vegetables. The development of biodegradable and edible film incorporated with natural anti-browning agent to prevent food browning can also be studied.

Footnotes

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