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Identification of pigment profiles and antioxidant activity of Rhizophora

mucronata mangrove leaves origin Lembeh, North Sulawesi, Indonesia

Article in Biodiversitas Journal of Biological Diversity · June 2021

DOI: 10.13057/biodiv/d220730

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B IOD I V E R S I TA S ISSN: 1412-033X
Volume 22, Number 7, July 2021 E-ISSN: 2085-4722
Pages: 2805-2816 DOI: 10.13057/biodiv/d220730

Identification of pigment profiles and antioxidant activity of Rhizophora

mucronata mangrove leaves origin Lembeh, North Sulawesi, Indonesia

ANTONIUS PETRUS RUMENGAN1,♥, ELVI SISKA MANDIANGAN2, WENDY ALEXANDER TANOD3,

DARUS SAADAH JOHANIS PARANSA1, CAROLUS PAULUS PARUNTU1, DESY MARIA HELENA MANTIRI1
1Department of Marine Science, Faculty of Fisheries and Marine Science, Universitas Sam Ratulangi. Jl. Kampus UNSRAT Bahu, Manado 95115, North
Sulawesi, Indonesia. Tel./fax.: +62-852-4027-3030, ♥email: [email protected]
2Research and Development Agency of North Sulawesi Province. Jl. 17 Agustus, Bumi Beringin, Wenang, Manado 95113, North Sulawesi, Indonesia
3Department of Fisheries and Marine, Politeknik Negeri Nusa Utara. Jl. Kesehatan, Mahena, Tahuna, Kepulauan Sangihe 95812, North Sulawesi,

Indonesia

Manuscript received: 23 May 2021. Revision accepted: 21 June 2021.

Abstract. Rumengan AP, Mandiangan ES, Tanod WA, Paransa DSJ, Paruntu CP, Mantiri DMH. 2021. Identification of pigment
profiles and antioxidant activity of Rhizophora mucronata mangrove leaves origin Lembeh, North Sulawesi, Indonesia. Biodiversitas 22:
2805-2816. Mangroves plants contain unique pigments which can serve both nutraceutical and pharmaceutical purpose. Therefore, this
preliminary study aims to identify the pigment profiles of Rhizophora mucronata mangrove leaves (HPLC method) and to computationally
evaluate the antioxidant mechanism of the pigments (PASS and STITCH analysis). Furthermore, it evaluated the antioxidant capacity of R.
mucronata leaves extracts (DPPH method), and the pigment profiles detected using HPLC were chlorophyll a (68.61%), chlorophyll b
(27.69%), lutein (29.94%), beta-carotene (14.05%), pheophytin a (8.72), violaxanthin (5.19%), and neoxanthin (3.65%). Beta-carotene,
lutein, neoxanthin, and violaxanthin were predicted to have potential as antioxidants properties using PASS analysis. While neoxanthin and
violaxanthin were predicted as free radical scavengers, beta-carotene was an Nrf-2 stimulant. The STITCH analysis showed that the
pigments contained in the leaves interacted synergistically by activating as antioxidant enzymes and inhibiting the expression of oxidative
stress proteins. The ethanol extract of R. mucronata leaves may be a potent antioxidant with an IC50 20.99 ± 0.33 µg/mL. Therefore, the
pigment contained in R. mucronata leaves is a potential source of antioxidants.

Keywords: Beta-carotene, chlorophyll, lutein, neoxanthin, violaxanthin

INTRODUCTION 2015a; 2015b; 2017). These are potential sources of

carotenoids pigments such as beta-carotene, alpha-
Mangrove plants live in low tide areas, and they play a carotene, xanthophylls including lutein, neoxanthin,
critical role in the coastal ecosystem by supporting zeaxanthin, and violaxanthin (Sarker and Oba 2021). In
fisheries, tourism, and a genetic reservoir (Liu 2012). It addition, leaves consist of other pigments such as phenolics
functions as a protector of the coastline, preventing and different groups of flavonoids, including flavonols,
seawater abrasion, the habitat of various aquatic biota, and flavones, flavanones (Sarker and Oba 2019a; 2020b;
acts best carbon storage ecosystem (Kepel et al. 2017; 2020c), and they all exhibit high antioxidant capacity
Rumengan et al. 2018; Saptiani et al. 2018; Tidore et al. (Sarker et al. 2018b).
2018). Furthermore, coastal communities have also used Previous studies also showed that mangroves contain
mangroves for house construction, charcoal making unique pigments which may serve nutraceutical and
materials (Dahdouh-Guebas et al. 2000), functional pharmaceutical functions (Banerjee et al. 2017). One of the
foodstuffs (Jariyah et al. 2014; Kardiman et al. 2017; mangroves has the potential to use its pigment content such
Analuddin et al. 2019), textile dyes (Pringgenies et al. as Rhizophora mucronata (Pringgenies et al. 2018). Prabhu
2017), and traditional medicine (Revathi et al. 2014; Rout and Bhute (2015) reported that the brown pigment from the
and Basak 2014; Alhaddad et al. 2019; Andriani et al. stem of R. mucronata was used as a textile dye.
2020). These plants have a self-defense mechanism Furthermore, it was previously reported that the leaves
because they live in areas with fluctuations in salinity and contain chlorophyll and carotenoid pigments (Flores-de-
temperature (Dewanto et al. 2018). The mechanism Santiago et al. 2016; Ridlo et al. 2017). However, no study
designed consists of enzymatic and non-enzymatic has reported the complete profile of the pigments in the
antioxidants defense (Sarker et al. 2018a; Sarker and Oba mangrove leaves of R. mucronata. The pigments can be
2018a; 2020a). Pigments in mangroves significantly affect used as a source of functional and natural food coloring
photosynthetic reactions, stress avoidance, and defense (Mapari et al. 2005).
mechanisms (Croft and Chen 2017). The mangrove Rhizophora mucronata showed
Previous studies reported that leaves are the natural medicinal potential for coastal communities. Meanwhile,
sources of pigments such as chlorophyll a, chlorophyll b, the fruit, leaves, bark, and flowers of R. mucronata were
betacyanins, betaxanthins, betalains (Sarker et al. 2014; used to treat various diseases, such as cognitive function
2806 B I OD I V E R S ITA S 22 (7): 2805-2816, July 2021

(Suganthy and Pandima Devi 2016), diabetes paper to separate the filtrate from the residue. Furthermore,
(Bandaranayake 1998; Aljaghthmi et al. 2017), diarrhea the filtrate was evaporated (rotary vacuum evaporator
(Puspitasar et al. 2012), hepatitis (Ravikumar and Buchi R-300) at 40°C during 4-6 hours to obtain a crude
Gnanadesigan 2012), and inflammation (Rohini and Das extract (Dewanto et al. 2018). According to Lichtenthaler
2009). The antioxidant capacity of the leaves obtained from (1987), the chlorophyll and carotenoid groups have a
India and Asia was widely reported (Imdadul et al. 2011). phytyl chain attached to the porphyrin ring system. The
This is a preliminary study to identify the pigment profiles possession of the phytyl side chain, which is esterified to
of Rhizophora mucronata mangrove leaves using the high- the ring carboxyl group, gives chlorophyll and carotenoids
performance liquid chromatography method and to their lipid character. Therefore, ethanol is one of the polar
computationally evaluate the antioxidant mechanism of the solvents used to extract fat-soluble pigments from living
pigments. Furthermore, it evaluated the antioxidant capacity plant tissues containing water. Figure 1 showed the
of R. mucronata leaves extracts using the DPPH method. location of mangrove leaves sampling.

Identification of pigment profiles

MATERIALS AND METHODS The identification of mangrove leaves pigments was
conducted on a High-Performance Liquid Chromatography
Sampling and extraction (HPLC-20AD-Shimadzu) with SPD-M20A photodiode
Mangrove leaves sample (1000 g) was obtained from array detector (PDA). The Pigment analysis was based on
Lembeh Island, North Sulawesi, Indonesia. Rhizophora the method by Hegazi et al. (1998), and the Shimadzu UV-
mucronata leaves were documented and put in a cool 1800 spectrophotometer was used in determining the
temperature container. They were collected in summer with wavelength. Meanwhile, the detection of mangrove leaves
hot sunny conditions (in July 2019) and were taken to the pigments was conducted by HPLC at 450 nm (carotenoids
laboratory for extraction. The leaves were finely mashed to detection) and 660 nm (chlorophyll detection) respectively.
a powder, and the extraction was performed three times The analytical column was a LiChroCART 250×4 mm I.D.
with ethanol pure grade (Merck) solvent. In addition, the R. packed with Lichrospher 100, RP-18e (5µm spherical
mucronata leaves powder (100 g) was macerated using particles), and the precolumn was an ODS-hypersil (C18)
ethanol (1:3 w/v) for 48 hours, with occasional shaking. with a diameter of 5µm, 20×4 mm.
The resultant maceration product was filtered through filter

Figure 1. Location of Rhizophora mucronata mangrove leaves sampling in Lembeh Island, North Sulawesi, Indonesia (1° 27' 8.78" N and
125° 14' 41.90" E)
 RUMENGAN et al. – Pigment profiles and antioxidant activity of Rhizophora mucronata mangrove leaves 2807

Dry pigment crude extract was dissolved in 5 mL following equation was used to determine the percentage of
acetone (Paransa et al. 2014) and filtered using a filter DPPH inhibition:
membrane (0.2 μm), then 20 μL was injected into HPLC.
The pigment elution was conducted at a 1 mL/min flow
rate at 30 °C using a gradient elution system from a
mixture of methanol, acetone, and ammonium acetate (1
M) solutions. Acetone was used in the pigment extraction Where :
because of its amphipathic nature of having a polar and a A: Sample absorbance
nonpolar end. Also, it has a significant partial negative and B: Absorbance control sample
positive charge on the oxygen and carbonyl atom with two C: Absorbance of negative control
nonpolar alpha carbons. However, it is less polar than D: Absorbance blank
water and ethanol and can dissolve nonpolar substances.
The nature of its small polarity allows it to dissolve polar
substances and has fewer properties than water and ethanol. RESULTS AND DISCUSSION
Therefore, acetone is an appropriate solvent, which allows
more excellent resolution for detecting pigments using The dry extract of Rhizophora mucronata mangrove
chromatography. It breaks chlorophyll lipid bonds to plant leaves was detected for pigment profiles by HPLC at a
thylakoid structures and suspends pigments in solution wavelength of 450 and 660 nm, with a retention time of 20
(Henriques et al. 2007). to 40 minutes. Table 1 and Figure 2 showed the pigment
profiles, and the chromatogram for the leaves extract.
Computational analysis Table 1 showed that the R. mucronata leaves extract
The pigment detected with HPLC predicted biological detected seven pigments dominated by chlorophyll a
activity-related antioxidants using the PASS (prediction of (68.61%) and chlorophyll b (27.69%). Chlorophyll is a
activity spectra for substances) analysis unique green pigment in almost every green part of plants,
http://www.pharmaexpert.ru/passonline/index.ph. PASS is such as leaves (İnanç 2011). Chlorophyll a is a pigment
a tool used for predicting the biological activity of compounds with a chlorine ring, where magnesium is surrounded by
(Riyadi et al. 2020). The predicted activity requires a structural four nitrogen atoms (Taiz et al. 2006). Meanwhile, in
formula in the form of canonical SMILE obtained from the chlorophyll b, the ‒CHO group replaces ‒CH3 on the C7
National Center for Biotechnology Information atom (Pareek et al. 2017). There is also chlorophyll a and b
https://pubchem.ncbi.nlm.nih.gov/. The pigments were epimer at 11.69% and 5.19%, and Limantara and Heriyanto
analyzed for their interactions with the STITCH database (2012) stated that they always accompany the presence of
(search tool for interactions of chemicals) http://stitch.embl.de/. chlorophyll. Chlorophyll a and b are common and
dominant pigments in the leaves of green plants, such as
Antioxidant assay mangroves (Liu 2012; Dou et al. 2018). Ridlo et al. (2017)
Measurement of the antioxidant capacity of mangrove reported R. mucronata leaves to contain chlorophyll and
leaves was carried out using the DPPH method (Oke and carotenoid pigments. Furthermore, Flores-de-Santiago et al.
Hamburger 2002), and the assays were conducted using 96 (2016) also reported that Rhizophora mangle leaves contain
well plate microplates. The ethanol extract of Rhizophora chlorophyll a and b. Their levels depend on the season and
mucronata leaves was prepared in series concentrations of physiological conditions of the mangroves. Bohn and
10, 20, 40, 80 µg/mL in methanol solution (Merck). Then, Walczyk (2004) detected chlorophyll a and the epimer at
160 µL of extract from each concentration series was fed the wavelength spectrum of 429, 664 nm, while chlorophyll
into the microplate well. Furthermore, 40 µL of DPPH b and the epimer were discovered at 456, 648 nm. Kusmita
(Merck) 0.76 mM solution was added to each well that et al. (2015) detected chlorophyll-b at the wavelength
contained a sample. A comparison control used vitamin C spectrum of 456, 596, 645 nm.
with a concentration series of 4, 6, 8, 10 µg/mL. As a Lutein is a member of the xanthophyll and carotenoid
control sample, each series of dilutions (160 µL) was added family (Al-ali et al. 2020), and it has a yellowish-orange
to the microplate well before adding 40 µL of methanol. A color, called macular pigment, which is not in abundance
negative control (without extract) was made by adding 160 (Landrum and Bone 2001; Aruldass et al. 2018). Ngginak
µL methanol with 40 µL DPPH, and 200 µL methanol was et al. (2017) reported detecting lutein on the wavelength
blank. The microplate was incubated in a dark room at 25- spectrum of 417, 443, and 472 nm, while Kurniawan et al.
28 °C for 30 minutes, and after that, the absorbance of each (2020) reported detected it at 447, 451, 472 nm. Also,
well was measured with the Multiskan GO Microplate Sarker and Oba (2021) reported that leaves contain good
Spectrophotometer (Thermo Scientific) at a wavelength of macular pigment lutein. Previously, no study has detected
517 nm. The IC50 determination was measured from the lutein pigment in mangrove leaves. The detection was
inhibition percentage data in units of µg/mL, and a probit conducted using random sampling of old mangrove leaves
analysis was used to determine the IC50 value. The that were yellowish in color.
2808 B I OD I V E R S ITA S 22 (7): 2805-2816, July 2021

Table 1. Identification of pigment profiles from Rhizophora mucronata leaves with HPLC

Wavelength Retention Wavelength References

Area
detection time spectrum Pigment profiles (Jeffrey et al. 1997; Zapata et al. 2000)
(%)
(nm) (min) (nm) Retention time (min) Wavelength spectrum (nm)
450 20.06 3.65 415, 437, 465 Neoxanthin ‒ 415.1, 438.5, 467.1
450 21.72 5.19 417, 442, 470 Violaxanthin 21.32 416, 440, 470
450 29.29 24.94 421, 447, 475 Lutein 27.65 422, 446, 475
450 33.91 20.65 462, 598, 647 Chlorophyll b 31.62 462, 599, 648
660 7.04
450 34.20 5.19 461, 599, 648 Chlorophyll b epimer 31.87 462, 599, 650
450 35.53 11.30 430, 617, 663 Chlorophyll a 33.15 431, 617, 662
660 35.53 57.31
450 35.89 2.08 430, 617, 663 Chlorophyll a epimer 33.48 430, 615, 664
660 35.89 9.61 430, 616, 663
660 37.63 8.72 409, 505, 535, Pheophytin a ‒ 409.5, 505.3, 534.7, 608.9, 665.5
608, 664
450 38.39 14.05 453, 479 Beta-carotene 35.95 426, 452, 477

Beta-carotene is one of the red-yellow, orange or red- pathway for photosystem II plants (Eijckelhoff and Dekker
orange carotenoids in natural plants that carry out 1997). Bohn and Walczyk (2004) detected pheophytin-a on
photosynthesis (Kusbandari and Susanti 2017). It may be the wavelength spectrum of 405, 661 nm while Kusmita et
fat-soluble, insoluble in water, easily damaged, unstable at al. (2015) were on wavelength spectrum of 408, 505, 535,
high temperatures, and precursor of vitamin A (Strobel et 609, 665 nm.
al. 2007). Furthermore, carotenoids including beta-carotene Violaxanthin is a natural xanthophyll pigment with an
act as an antioxidant. Previous studies showed that they orange color found in various plants (Giossi et al. 2020). It
have strong DPPH and ABTS antioxidant activity in is biosynthesized from zeaxanthin by an epoxidation
different amaranth species such as drought-tolerant reaction and has a 5,6-epoxy double group found in orange
amaranth (Sarker and Oba 2020d), A. gangeticus (Sarker et fruits, green vegetables, and microalgae (Melendez-
al. 2020a), A. hypochondriacus (Sarker and Oba 2020e), Martınez et al. 2008). Furthermore, it plays a role in
stem amaranth (Sarker et al. 2020b), A. blitum (Sarker and photoprotection mechanisms such as the ability of plants to
Oba 2020f), green amaranth (Sarker et al. 2020c), weedy adapt to contrasting light environments (Bowen-O'Connor
amaranth (Sarker and Oba 2019b), and red amaranth et al. 2013). Wang et al. (2018) detected violaxanthin
(Sarker and Oba 2019c). Furthermore, carotenoids pigments at the wavelength spectrum of 417.6, 440.9, and
including beta-carotene protect the photosynthetic tissue 470.1 nm while Ruban et al. (2001) detection was at 470
through direct quenching of triplet chlorophyll. This nm. These pigments were also reported in mangroves with
prevents the generation of singlet oxygen from oxidative high salinity (Falqueto et al. 2008).
damage in abiotic stress like salinity and drought (Sarker Neoxanthin pigments are carotenoids of xanthophylls
and Oba 2020a). It also detoxifies various forms of reactive groups. It acts as an intermediary for the biosynthesis of the
oxygen species (ROS) (Sarker and Oba 2018b; 2018c) hormone abscisic acid in plants (Perreau et al. 2020).
through increasing beta-carotene concentration (Sarker and Furthermore, it serves as a protection against
Oba 2018d; 2018e; 2019d). Beta-carotene is a pigment photooxidative stress (Dall'Osto et al. 2007). Neoxanthin is
synthesized by plants (Bogacz-Radomska and Harasym the primary xanthophyll pigment found in green plants
2018). Radu et al. (2012) reported detecting this pigment (Giossi et al. 2020). Chandrika et al. (2005) detected
on a wavelength spectrum of 445, 472, 498 nm. neoxanthin in the wavelength spectrum of 413, 436, 465
Meanwhile, it was detected by Mangunsong et al. (2019) at nm, and was detected by Gupta et al. (2015) at 415, 437,
a wavelength spectrum of 460 nm. Beta-carotene was also 465 nm. In mangroves, the neoxanthin pigment was found
detected on the wavelength spectrum of 450.20 and 477.60 in mangroves Avicennia alba (Sasamoto et al. 2020).
nm (Kusbandari and Susanti 2017). The literature showed The pigment detected in R. mucronata leaves extract
that this pigment was detected in the leaves and roots of predicted its probability to be active (Pa) value as an
mangroves Avicennia officinalis, Excoecaria agallocha, antioxidant. Bioactivity prediction was conducted using
Kandelia candel, and Rhizophora mucronata (Ravindran et PASS analysis (Filimonov et al. 2014). The Pa value
al. 2012). In addition, it was also detected in the mangroves describes the potential activity of a compound. When the
of Bruguiera gymnorrhiza, Sonneratia alba, and Pa > 0.7, it is estimated to have a high bioactivity potential,
Xylocarpus granatum (Analuddin et al. 2019). both for computational and laboratory assays. Meanwhile,
Pheophytin a pigment is a chlorophyll a without Mg2+ when the value is 0.3 ≤ Pa ≤ 0.7, then the compound has
ion, and it is dominant in fresh green leaves, which is the computational ability as an antioxidant, but it has not
degraded due to heating and storage processes (Hsu et al. been proven in the laboratory. Also, when the Pa < 0.3, it is
2013). It is produced naturally by plant leaves and acts as predicted that the compound has a low bioactivity potential
an intermediary for the first electron carrier in the transfer (Aisiah et al. 2020; Riyadi et al. 2021). However, the
 RUMENGAN et al. – Pigment profiles and antioxidant activity of Rhizophora mucronata mangrove leaves 2809

bioactivity of chlorophyll a and b may not be predicted by reported chlorophyll a and b from medicinal plants with
PASS analysis because they have a metal element in their high potential antioxidants. Pérez-gálvez et al. (2020)
structure. The pigments beta-carotene, lutein, neoxanthin, stated that chlorophyll b showed higher antioxidant activity
pheophytin-a, and violaxanthin have their potential than chlorophyll a.
bioactivity as antioxidants, free radical scavengers, and Kurniawan et al. (2020) stated that lutein can act as an
NF-E2-related factor (Nrf-2) stimulant. Figure 3 showed antioxidant and maintaining organs such as the eyes, brain,
the probability to be active as the antioxidant of the and skin. The content in marigold plant (Tagetes spp.) was
pigment in the R. mucronata leaves extract. reported to have a DPPH radical inhibition ability of
Figure 3 showed that beta-carotene, lutein, neoxanthin, 89.90% (Ingkasupart et al. 2015). Furthermore, it was
and violaxanthin are predicted to have potential as general reported to work as an antioxidant in the photo-stressed
antioxidants. Neoxanthin and violaxanthin were also retina (Kamoshita et al. 2016)
predicted to be free radical scavengers. Meanwhile, beta- Beta-carotene is also reported to be an antioxidant and
carotene was predicted as an Nrf-2 stimulant, which an anti-carcinogen (Paolini et al. 2003). Berti et al. (2014)
regulates antioxidant protein as protection from oxidative stated that it is effective as a radioprotective agent and acts
damage (Ma 2013; Cui et al. 2016; Riyadi et al. 2019). as an antioxidant. Mueller and Boehm (2011) reported that
Chlorophyll cannot be predicted by PASS analysis as an beta-carotene and its derivatives showed antioxidant
antioxidant, even though it has antioxidant properties as properties measured by the αTEAC, chemiluminescence
predicted by previous studies (İnanç 2011; Keleş et al. (CL), and ferric reducing activity (FRAP) methods.
2016; Sarker et al. 2018c; 2018d). Durga et al. (2015)

Figure 2. HPLC Chromatogram of Rhizophora mucronata leaves ethanol extract

Figure 3. Probability to be active of pigments contain in Rhizophora mucronata leaves as an antioxidant with PASS analysis
2810 B I OD I V E R S ITA S 22 (7): 2805-2816, July 2021

Furthermore, Figure 3 showed the prediction of beta- metabolism of intracellular vitamin A (Blaner et al. 2020).
carotene bioactivity as an Nrf-2 stimulant. The literature Figure 4 showed that lutein affects the expression of BCO2
showed beta-carotene can activate the Nrf2-ARE (Beta, beta-carotene 9 ', 10'-oxygenase) to catalyze beta
(antioxidant response element) pathway to provide a carotene. In addition, Lietz et al. (2012) also reported that
neuroprotective effect from traumatic brain injury (Chen et BCO2 contributes to the formation of vitamin A to improve
al. 2019). Ben-dor et al. (2005) reported that beta-carotene antioxidant performance and immune function (Zhang et al.
stimulates Nrf-2 in the leukemia promyelocytic core body 2019).
and regulates phase II enzyme expression (associated with Figure 4 also showed that lutein affects the PPARA
cancer-preventing gene activation). gene (Peroxisome proliferator-activated receptor alpha),
Dall'Osto et al. (2007) stated that neoxanthin acts as an which strengthens antioxidant and anti-inflammatory
antioxidant in the photosystem II supercomplex in plant defense systems (Moran et al. 2014) by increasing
thylakoid to protect membrane lipids photooxidation. In regulation of the enzyme expression and inhibiting the
addition, Giossi et al. (2020) reported that neoxanthin was activity of NF-κB (nuclear factor kappa b) (Gao and Li
directly involved in photoprotection as an antioxidant to 2012). PPARA activates BCMO1 to metabolize vitamin A.
increase the activity of ROS scavenge under extreme light It also regulates the expression of SCARB1 (scavenger
conditions. Sarker and Oba (2020g) reported that the receptor class B type 1), which is an HDL (high-density
neoxanthin contained in Amaranthus tricolor showed lipoprotein) receptor protein that mediates carotenoid
DPPH radical scavenging activity. Neoxanthin reduces uptake (Hoekstra and Sorci-Thomas 2017). Soran et al.
oxidative-induced DNA base damage by less than 50%. In (2015) reported that HDL showed an antioxidant effect in
lower concentrations than lutein, it is a better inhibitor of protecting oxidative stress due to increased LDL (low-
oxidative-induced DNA damage (Şahin et al. 2020). density lipoprotein). Figure 4 showed that lutein affects
Dall'Osto et al. (2007) also reported the antioxidant UCP1 (uncoupling protein 1) expression directly or
properties of violaxanthin as photoprotection, even though through activation by PPARA. UCP1 gene reduces the
it is lower than neoxanthin. The literature also reports the production of ROS (reactive oxygen species) in
antioxidant properties of violaxanthin and its derivatives mitochondria (Oelkrug et al. 2014) to prevent oxidative
isolated from mangoes, with strong lipid peroxidation stress in adipose tissue (Shabalina et al. 2006).
inhibition capabilities (Araki et al. 2016). Furthermore, Figure 4 showed beta-carotene affects BDNF (Brain-
violaxanthin isolated from microalgae Eustigmatos cf. derived neurotrophic factor) expression and it is a gene in
polyphem was also reported to have radical scavenger the brain that promotes the survival of nerve cells (neurons)
capabilities with 2,2-diphenyl-1-picrylhydrazyl (DPPH), by playing a role in the growth, maturation
and 2,2-azobis-3-ethylbenzthiazoline-6-sulphonic acid (differentiation), and maintenance of neuron cells. Wu et
(ABTS) radical assays (Wang et al. 2018). However, al. (2016) reported that BDNF increases superoxide
Figure 2 showed that pheophytin a has a low Pa value as an dismutases and glutathione reductase expression. It also
antioxidant, and it prevents oxidative DNA damage and reduces the oxidative protein damage index (Lee et al.
lipid peroxidation. It works by reducing reactive oxygen 2009), reduces antioxidant protein expression (Wu et al.
species, such as DPPH, and by chelation of metal ions, 2012), restores reduced mitochondrial electron-coupling
such as Fe (II) (Hsu et al. 2013). Kusmita et al. (2015) also capacity, and increases mitochondrial uncoupling protein 2
reported that pheophytin a contained in green tea has an (UCP2). It acts as an antioxidant by reducing the
antioxidant capacity (DPPH method) with IC50 = 573 ± production of superoxide anions (Chan et al. 2010). Figure
0.23 mg/L. 4 also showed that beta-carotene and lutein inhibit the
The mechanism of antioxidant action of the pigments in activation of the protein MMP9 (Matrix Metalloproteinase-
R. mucronata leaves extract should be properly understood 9) through increased BDNF expression. Furthermore, the
Furthermore, the pigments in Table 1 were evaluated by MMP9 gene regulates the tissue remodeling process by
STITCH. This is a tool for integrating information about activating cytokines and chemokines, causing inflammation
the interactions of metabolic pathways, crystal structure, and fibrosis in the tissue (Yabluchanskiy et al. 2013).
binding experiments, and relationships between chemicals Figure 4 showed that beta-carotene activates FN1
(Kuhn et al. 2008). Figure 4 showed the interactions (Fibronectin 1) action to inhibit the enzyme lipoxygenases
between the pigments. (LOX) and MMP9 expression. LOX enzyme oxidizes fatty
Figure 4 showed the interaction between the working acids and causes inflammation in tissues (Ratnasari et al.
mechanism of the pigments in the R. mucronata leaves 2017). Meanwhile, FN1 is activated through the Nrf-2
extract. Chlorophyll a, chlorophyll b, neoxanthin, and pathway (Prestigiacomo and Suter-Dick 2018) to bind
violaxanthin support the performance of lutein and beta- LOX. Oxidation and inflammation in the tissue can be
carotene. Furthermore, Beta-carotene pigments activate and inhibited (Fogelgren et al. 2005). In summary, the pigments
catalyze the transcriptional regulation of the BCMO1 in the leaves of R. mucronata work synergistically by
protein (beta, beta-Carotene 15,15'-monooxygenase-1), activating antioxidant enzymes and inhibiting the
which is a key enzyme in vitamin A metabolism (Lietz et expression of oxidative stress proteins.
al. 2010). BCMO1 was reported to be expressed in The extract of R. mucronata leaves was evaluated for
intestinal tissue and plays a role in lipid metabolism (Lietz its antioxidant capacity as a free radical scavenger using
et al. 2012). It affects the RBP2 protein (Retinol-binding the DPPH method. Meanwhile, DPPH is a stable free
protein 2), which plays a role in the absorption and radical which accepts electrons or hydrogen atoms to form
 RUMENGAN et al. – Pigment profiles and antioxidant activity of Rhizophora mucronata mangrove leaves 2811

stable diamagnetic molecules (Tanod et al. 2019a). The Increased concentration of the extract also increased the
antioxidant capacity was evaluated by calculating DPPH percentage of DPPH free radical inhibition. Table 2
purple light intensity level proportional to the decrease in showed that the inhibition percentage was evaluated for
DPPH concentration. This reduction was caused by the IC50 determination by probit analysis. According to the
reaction of the 2,2-diphenyl-1-picrylhydrazyl molecule Blois (1958) category, antioxidant activity can be
with the hydrogen atoms released by the components of the categorized as very strong (IC50 < 50 µg/mL), strong (50 ≤
sample molecule. It formed hydrazine diphenyl picril IC50 ≤ 100 µg/mL), moderate (100 ≤ IC50 ≤ 150 µg/mL),
compound and caused DPPH to change color from purple weak (150 ≤ IC50 ≤ 200 µg/mL), and very weak (IC50 > 200
to yellow (Tanod et al. 2019b). The reactivity of the R. µg/mL).
mucronata leaves extract with stable free radicals was also
evaluated, and the antioxidant capacity was compared with Table 2. The IC50 value of the Rhizophora mucronata leaves
vitamin C (Figure 5). In addition, Vitamin C is commonly extract using the DPPH method was compared with vitamin C
used to compare assaying antioxidant activity because it is
cheaper and easier to obtain (Lung and Destiani 2014). Sample IC50 (µg/mL)
Figure 5 showed that the R. mucronata leaves extract
has antioxidant activity because hydrogen atoms or R. mucronata leaves 20.99 ± 0.33
Vitamin C 9.62 ± 0.09
electrons were donated to react with DPPH radicals.

Figure 4. Mechanism action as an antioxidant of pigments in Rhizophora mucronata leaves with STITCH analysis
2812 B I OD I V E R S ITA S 22 (7): 2805-2816, July 2021

reported an IC50 with a DPPH concentration of 0.01%

(w/v) to be 4.71 µg/mL. Dewanto et al. (2019) reported an
IC50 of vitamin C with a DPPH concentration of 50 µM to
be 31.35 ± 0.81 µg/mL.
Mangroves are plants that live in tidal areas, and they
experience variations in environmental pressure. In
addition, variations in ecological pressure trigger reactive
oxygen species (ROS) production and interfere with
mangrove growth (Dasgupta et al. 2012). The pigments
contained in mangroves produce antioxidant substances
useful for the self-defense mechanism of ROS (Thatoi et al.
2014; Sarker and Oba 2018c; Dewanto et al. 2021).
Therefore, it can be concluded that chlorophyll a,
chlorophyll b, beta-carotene, lutein, neoxanthin,
pheophytin a, and violaxanthin are the pigment profiles in
Rhizophora mucronata mangrove leaves. All pigments
Figure 5. DPPH radical inhibition from the Rhizophora detected have strong potential as antioxidants, especially as
mucronata leaves extract compared to vitamin C
free radical scavengers and Nrf-2 stimulants. They interact
with each other to inactivate antioxidant enzymes and
inhibit the expression of oxidative stress proteins. This
Table 2 showed that the R. mucronata leaves extract study showed that the pigment in R. mucronata leaves is a
and vitamin C had very strong antioxidant activity, with a potential source of antioxidants for human health.
DPPH concentration of 0.76 mM. Literature studies Furthermore, it was developed by isolating the pigments
showed that the IC50 of the same sample can vary from Rhizophora mucronata leaves and comparing the
depending on the DPPH concentration, sample origin, antioxidant power with standards for nutraceuticals and
conditions, and the solvent used (Dewanto et al. 2019). pharmaceuticals preparation.
Furthermore, fractionation and crude extract of R.
mucronata mature leaves from Penunggul, East Java,
Indonesia showed IC50 from 82.97 ± 51.15 to 491.78 ± ACKNOWLEDGEMENTS
427.59 µg/mL, while the IC50 ascorbic acid (vitamin C)
was 12.36 µg/mL, with a DPPH concentration of 0.4 mM The authors are grateful to the Rector of Universitas
(Sasmito et al. 2016). The ethanol extract obtained from Sam Ratulangi, Manado, Indonesia for research grant No.
Sunderban, India, was reported to show DPPH radical 042.01.2.400959/2019 (Universitas Sam Ratulangi DIPA
scavenging (IC50) 6.65 ± 0.10 µg/mL, with a DPPH research funding), and are also grateful to Andreas Marbun
concentration of 0.135 mM (Adhikari et al. 2016). Two and Maikel Tiolung for their assistance.
compounds isolated from the methanol extract of the leaves
from Vallarpadam, India, showed IC50 of 0.76-0.84
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