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1 s2.0 S1658077X22001084 Main
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Review article
a r t i c l e i n f o a b s t r a c t
Article history: Moringa oleifera is a plant valued for its properties and applications in Ethnomedicine. It is cultivated in
Received 25 August 2022 India, tropical Africa, and America; some regions use their different tissues as food supplements.
Revised 6 December 2022 Although germination can increase seedlings’ phytochemical content, few studies have described the
Accepted 11 December 2022
phytochemical content of moringa seedlings during early growth. This study aimed to investigate and
Available online 21 December 2022
discuss the limited information dealing with moringa seed germination, sprout production, and seed-
lings’ chemical composition. This bibliographical research was systematically and thoroughly conducted
Keywords:
using some of the most internationally-recognized databases. M. oleifera plants are characterized by their
Functional foods
Nutrients
ability to grow under adverse environmental conditions. Although they generally germinate at rates
Glucosinolates greater than 70%, this response depends on the altitude, light periods, temperature, and nutrient avail-
Phenolic compounds ability. Pre-germination treatments have also been reported to help improve germination yields; the
Isothiocyanates most common is soaking exposure. The production of M. oleifera sprouts is a viable option for obtaining
functional food as this process can increase the content of nutrients (e.g. lipids, proteins) and phytochem-
icals (glucosinolates and phenolic compounds). Also, sprouts can be used as additives to enrich conven-
tional foods. It is concluded that there is little scientific information describing the germination process
and the chemical composition of both moringa seeds and moringa sprouts. Therefore, it is a niche oppor-
tunity to build new research that helps fill the informational gaps mentioned above. Meanwhile, it is
envisioned that biotic or abiotic agents might modulate the germination process and their chemical
compounds.
Ó 2022 The Authors. Production and hosting by Elsevier B.V. on behalf of King Saud University. This is an
open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Contents
1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 224
1.1. Objective . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 224
2. Moringa seedlings . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 224
2.1. Moringa seeds composition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 225
2.2. Glucosinolates in moringa seeds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 225
3. Seedling germination process . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 225
3.1. M. oleifera seed germination . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 225
⇑ Corresponding author.
E-mail address: jose.nunez@uacj.mx (J.A. Núñez-Gastélum).
1
First two authors contributed equally to this work.
Peer review under responsibility of King Saud University.
https://doi.org/10.1016/j.jssas.2022.12.002
1658-077X/Ó 2022 The Authors. Production and hosting by Elsevier B.V. on behalf of King Saud University.
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
José A. Núñez-Gastélum, A.A. Arguijo-Sustaita, José A. López-Díaz et al. Journal of the Saudi Society of Agricultural Sciences 22 (2023) 223–230
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José A. Núñez-Gastélum, A.A. Arguijo-Sustaita, José A. López-Díaz et al. Journal of the Saudi Society of Agricultural Sciences 22 (2023) 223–230
it has been seen that there are variabilities between the parame- 75 ppm of gibberellic acid did not affect the germination percent-
ters during the germination of M. oleifera seeds due to their posi- age of moringa seeds. In addition, Silva et al. (2021) report that M.
tion in the pod and their agroclimatic origin (Bayé-Niwah & oleifera is tolerant to the effect of salinity during the germination
Mapongmetsem, 2014; Dao et al., 2017). phases; however, seed vigor is reduced as a function of increasing
Regarding the effect of temperature, Hassanein et al. (2017) salinity as this condition reduces water uptake in seeds. Moreover,
found that under laboratory conditions at 20 °C, a germination once it emerges, the seedling maintains optimal growth in salinity
yield of around 90% is obtained. They mention that no germination concentrations lower than 3.5 dS m 1 (Ferreira et al., 2011; Farooq
was obtained below 10 °C and at 40 °C. Regarding light, Akinyemi et al., 2022).
et al. (2015) report that there were no significant differences in the In addition, various microorganisms can positively affect the
percentage of germination in light and darkness; however, this germination of moringa seeds. This has been observed when seeds
parameter decreased when the seeds were subjected to water are germinated in media with strains of rhizobia and Azotobacter sp
stress. (Bécquer et al., 2018; Barela, 2019). New technologies also con-
tribute to the germinative processes. It was recently found that
3.2. Pre-germinative treatments on M. oleifera seed germination the pretreatment of M. oleifera seeds with laser increased the agro-
nomic parameters, including the germination percentage (Bibi
Pre-germinative treatments allow breaking the dormant period et al., 2017).
in moringa seeds to promote rapid emergence and uniform seed-
lings. Exposure to soaking has been one of the few technologies
tested; the results indicate that it facilitates germination and even 4. Moringa sprouts
promotes plant tolerance to stress. Padilla et al. (2012), Barraza
(2017) and Montilla-Mota et al. (2017) report that soaking seeds The moringa seed has great nutritional value and health-
in water for 24 h before sowing accelerates the germination of promoting properties. However, their potential as a functional food
moringa seeds. The absorption of water by the seed (imbibition) has not yet been fully explored due to their limitations as a food
activates metabolic processes, mobilization of storage compounds component, the most crucial being; bitterness, astringency, hard-
that subsequently lead to the expansion of the embryo, and pene- ness and fibrous consistency. In cereals, the germination process
tration of the radicle and other organs through the surrounding tis- makes the seeds more flavorful and tender, and it has been sug-
sue (Tesfay et al., 2016). The water potential facilitates the gested that the sprouts provide a higher nutritional value and func-
activation of growth regulators, such as gibberellic acid and kine- tionality than the seeds. This process activates the metabolic
tin, which induce enzymes responsible for starch hydrolysis. This enzymatic pathways, which makes the seeds easier to digest,
triggers glucose metabolism, allowing ATP to be released for root increases the bioavailability of proteins, hydrolyzes starch,
protrusion (Nicasio-Arzeta et al., 2011; Amador-Alférez et al., enhances vitamin content, and the concentration of secondary
2013; Cardona-Ayala et al., 2014). El-Absy et al. (2019), obtained metabolites can increase or decrease depending on the conditions
a 65% germination percentage in seeds soaked for 48 h. It is worth (Lemmens et al., 2019).
mentioning that Yerima et al. (2016) recommend avoiding pro-
longed soaking because they noted that treatment of more than
4.1. Moringa sprouts production
four days could negatively affect its emergence and initial
development.
Regarding the chemical and/or nutritional characterization of
Scarification treatments, which in the case of moringa seed are
moringa sprouts, few studies have been reported, and we were
focused on removing the testa or ‘‘husk”, do not have conclusive
able to find five in the literature (Ijarotimi et al., 2013; Tesfay
results. Luna (2019), mentioned that the removal of the testa accel-
et al., 2016; Servín de la Mora-López et al., 2018; León-López
erates the germination process in liquid basal media. On the con-
et al., 2019; Coello et al., 2020). Table 1 shows the various germi-
trary, Montilla et al. (2017), found that the partial and/or
nation conditions used in the investigations mentioned above. It
complete removal (manual scarification) of the testa (distal, prox-
should be noted that in three of the studies, the sprouts were pro-
imal and lateral) did not show a significant effect on germination in
duced in the dark.
sandy substrate. Partial two-sided scarification has also been
reported to improve seedlings’ number of petioles, height, and
density (Ubaidillah et al., 2020). 4.2. Moringa sprouts chemical composition
Treatment fusions have also been explored; Candelaria-
Martínez et al. (2019) mention that soaking for 24 h and cracking Table 2 summarizes the data obtained from the chemical char-
the seed coat did not improve germination in 6-month-harvested acterization performed on the sprouts. The data obtained by Tesfay
seeds. In this case, storage time played a determining role. et al. (2016) are not presented in Table 2 because few parameters
Barrios-Gómez et al. (2022) evaluated the effect of storing moringa fit with those evaluated by the rest of the authors. For example,
seeds under atmospheric conditions and refrigeration (6 °C) on they report that for their best treatments, a phenol content of
germination rate. They found that, regardless of the type of storage, 122.5 mg GAE 100 g 1 and more than 2,000 lmol FeSO47H2O
the seeds of 2 and 3 months presented the best germination per- g 1 of antioxidant activity by the FRAP method. For the rest of
centages. For this reason, using new seeds with a storage period the study, the authors focused on the determination of enzymatic
of up to three months under ambient conditions is recommended. and non-enzymatic antioxidants and the quantification of
After that time, viability decreases due to biochemical processes monosaccharides. Regarding the proportion of macronutrients, a
that degrade the membrane and various components of plant cells predominance of carbohydrates is observed, followed by proteins.
(Mubvuma et al., 2013). In general, the profiles of amino acids and fatty acids show some
parity between the data of the two authors who report them. As
3.3. Use of plant elicitors previously noted, the leading causes of the differences observed
are attributable to the different germination conditions used, as
On the other hand, various studies exposing moringa seeds to well as the origin of the seeds. Mainly, moringa sprouts are postu-
stressors during germination have been conducted. For example, lated as an alternative source of amino acids to meet the require-
Lopéz et al. (2018) found that concentrations of 35 ppm and ments established by the 2007 WHO/FAO/UNU.
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José A. Núñez-Gastélum, A.A. Arguijo-Sustaita, José A. López-Díaz et al. Journal of the Saudi Society of Agricultural Sciences 22 (2023) 223–230
Table 1
Germination conditions of the reported studies on obtaining moringa sprouts.
Parameter Reference
Ijarotimi et al., 2013 Tesfay et al., 2016 Servín de la Mora-López et al., 2018 León-López et al., 2019 Coello et al., 2020
Soak time (h) 9h NU* NU 24 h 18 h
Germination substrate Paper Paper Paper Paper Paper
Fotoperiode Darkness Darkness 50% Darkness NE**
Temperature 30 °C 20–30 °C 25–40 °C 25–40 °C 28–36 °C
Humidity Ambient Ambient 80–90% 80–90% 95%
Germination time (days) 4 1–56 1–15 1–15 1–8
*
Not used.
**
Not specified.
Table 2
Comparison between the chemical characterizations of different moringa sprouts.
Parameter Reference
Ijarotimi et al., 2013* Servín de la Mora-López et al., 2018** León-López et al., 2019* Coello et al., 2020**
Macronutrients (%)
Protein 23.69 41.54 24.32 32.21
Lipids 14.62 32.72 17.39 33.39
Ash 4.34 NR 3.09 3.20
Carbohydrates 53.00 NR 55.20 35.01
Aminoacids profile (g 100 g 1 of protein)
Alanine 5.42 5.27 NR NR
Aspartic acid 18.13 1.10 NR NR
Serine 3.17 3.61 NR NR
Glutamic acid 20.23 7.74 NR NR
Proline 2.68 9.83 NR NR
Glycine 2.63 6.62 NR NR
Arginine 8.66 16.71 NR NR
Cysteine 1.79 NR NR NR
Tyrosine 2.09 2.68 NR NR
Histidine 2.50 3.94 NR NR
Lysine 0.36 1.89 NR NR
Threonine 3.35 5.28 NR NR
Valine 1.25 2.88 NR NR
Methionine 0.35 2.13 NR NR
Isoleucine 4.69 2.88 NR NR
Leucine 4.08 2.73 NR NR
Phenylalanine 3.57 4.55 NR NR
Fatty acids profile (% total fatty acids)
Myristic acid (C14:0) 0.42 0.17 NR NR
Palmitic acid (C16:0) 14.01 7.52 NR NR
Palmitoleic acid (C16:1n7) 0.26 1.73 NR NR
Stearic acid (C18:0) 13.57 4.69 NR NR
Oleic acid (C18:1n9) 10.25 76.62 NR NR
Linoleic acid (C18:2n6) 60.70 2.08 NR NR
Linolenic acid (C18:3n3) 0.13 1.60 NR NR
Arachidic acid (C20:0) NR 0.30 NR NR
Eicosenoic (C20:1n9) NR 2.27 NR NR
Behenic acid (C22:0) 0.13 2.95 NR NR
Phytochemicalsa (mg 100 g 1)
Phenolics 34.33 559 271.67 645.70
Flavonoids 5.50 NR NR NR
Tannins 181.67 NR 169.98 NR
Saponins 8.00 NR 681.50 NR
Phytates 40.00 NR 847.25 NR
Antioxidant activity (lmol Trolox equivalents 100 g 1
)
ORAC NR NR 10,927 9,856
ABTS NR 16,996 NR NR
DPPH NR 9,872 NR NR
*
The average value presented by the authors was taken.
**
The highest value was taken since the authors presented each treatment’s data.
a
Results may be expressed as equivalents of standard compounds. NR: Not reported.
An important point to highlight is that Ijarotimi et al. (2013) found that the content of phytochemicals decreases when the seed
report that the evaluated seeds and sprouts showed a percentage germinates, except for terpenes. In contrast, León-López et al.
of linoleic acid (60.7%) higher than that of oleic acid (10.6%). This (2019) mention that tannins and saponins increased during germi-
data contradicts the extensive scientific evidence that establishes nation. The latter obtained sprouts harvested at a longer time and
that the proportion of oleic acid in the seed of M. oleifera is greater higher relative humidity with respect to Ijarotimi et al. (2013).
than 70% of the total fatty acids and that linolenic acid represents On the other hand, Servín de la Mora-López et al. (2018),
less than 1% (Leone et al., 2016). Furthermore, these same authors León-López et al. (2019), and Coello et al. (2020) obtained a higher
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José A. Núñez-Gastélum, A.A. Arguijo-Sustaita, José A. López-Díaz et al. Journal of the Saudi Society of Agricultural Sciences 22 (2023) 223–230
antioxidant activity, regardless of the method, in the sprouts with 2.5 g 100 g 1, were found, respectively (Shi et al., 2004). Similar
respect to the seed. Previously, the importance of glucosinolates to phytates, there is no RDA for saponins.
as bioactive compounds and their presence in parts of the moringa Tannins are polymers of phenolic compounds that can precipi-
plant has been highlighted. Currently, only Coello et al. (2020) tate proteins, affecting their digestibility, which reduces the
determined these compounds’ content during moringa seeds’ ger- absorption of essential amino acids (Raes et al., 2014). Meantime,
mination. They found a behavior where on average, the glucosino- anticancer, antimicrobial, and antiviral properties have been
late content decreases from 205 lmol/g in seeds to 181.3 lmol/g in attributed to tannins. In addition, its intake and processing by
96 h sprouts. When seedlings germinate at a temperature of 32 °C, microbial flora generate catechins and phenolic acids, metabolites
glucosinolates decrease by 25%, while at 36 °C, the percentage is that can exert systemic pharmacological effects once absorbed
reduced by 11%. The authors germinated the seeds on paper and (Fabbrini et al., 2022). For example, Tanin rates of 0.03–1.3, 0.5–
did not specify the photoperiod, they refer to previous works where 1.05 y 0.05–7.2 g 100 g 1 have been reported for bean (Phaseolus
darkness conditions are reported. To maintain or increase the con- vulgaris L.), peas (Pisum sativum L.) and sorghum (Sorghum vulgare),
tent of glucosinolates in moringa sprouts, with respect to seeds, it is respectively (Gilani et al., 2005). Table 2 shows that moringa
necessary to evaluate the use of other types of substrates on the sprout values are comparable to the minimum ranges found in
behavior of phytochemicals, as well as the influence of light. other plant products.
Finally, some potential uses for moringa sprouts have been pro- Glucosinolates are glycosidic compounds that have sulfur and
posed, the addition of sprout powder to enrich traditional foods nitrogen atoms in their structure. These metabolites are found in
has been the most common. The fortification of fettuccine-type cruciferous vegetables, such as broccoli, cabbage, and cauliflower.
pasta improves the content of protein, lipids, minerals and fiber, They have been related to toxic effects that can produce thyroid
in addition to increasing the amount of thiamin and riboflavin; gland hypertrophy and induce goiter. Likewise, they are considered
however, parameters such as hardness, elasticity, stickiness, and anticancer agents in their native form or once they are transformed
chewiness decrease (Coello et al., 2021). The substitution of wheat into isothiocyanates and indolic compounds (Di Gioia et al., 2020).
flour for moringa sprout flour increased bread’s protein, crude Broccoli is a conventional food that most contributes to glucosino-
fiber, iron, calcium and zinc content and decreased carbohydrates lates to the diet, Rybarczyk-Plonska et al. (2016) reported that the
(Chinma et al., 2014). glucosinolates in this vegetable are around 35 lmol/g in samples
that included both shoots and stems as it is the way it is commonly
4.3. Components of moringa sprouts related with antinutritional consumed.
functions Finally, it is essential to mention that different methodologies
are proposed to reduce the content of these compounds associated
It has been reported that moringa sprouts contain glucosino- with antinutritional functions; these include soaking, grinding,
lates, phytates, tannins and saponins, to which antinutritional debarking, roasting, cooking, germination, and fermentation
functions or activities are attributed (Reddy & Sathe, 2001) and/ (Samtiya et al., 2020). For example, during the germination process,
or positives for human beings (Harland & Morris, 1995). The cur- a decrease in the content of phytates in cereals and legumes is
rent dichotomy in the scientific literature prompts a debate about reported. It can be attributed to the hydrolysis of phytate com-
the acceptance of foods containing these components. pounds mediated by the enzyme phytase, realising minerals assim-
Concerning phytates, their primary sources are seeds, legumes, ilated for seedling development (Egli et al., 2002; Elliott et al.,
and whole grains. Phytate has been considered an antinutrient for 2022).
decades because it can inhibit the digestive tract’s absorption of
minerals and trace elements. However, it has recently been found
5. Moringa sprouts: What is next?
that these compounds can act as antioxidants, anticancer, preven-
tives of kidney stone formation, antidiabetics, and anticholesterol
The authors of this work recommend conducting studies that
agents (Schlemmer et al., 2009). Phytate contents similar to those
examine the effect of environmental conditions on nutrients and
of moringa sprouts (Table 2) have been reported for rice sprouts
phytochemicals during the germination of moringa seeds, such as
(0.096 g 100 g 1), corn (0.072 g 100 g 1), sorghum (0.120 g
photoperiod, light intensity, temperature, relative humidity, type
100 g 1) and wheat (0.079 g 100 g 1) (Azeke et al., 2011). Mung
of substrate, among others. Also, it is suggested to analyze the
bean sprouts (Phaseolus aureus L.) are the most consumed products
impact of different stress triggers, both endogenous and exogenous.
of their type worldwide. Tajoddin et al. (2011) found an average of
On the other hand, it is worth noting the importance of moni-
0.26 g 100 g 1 of phytates for five varieties germinated for 48 h, a
toring the activation of enzymes involved in the different biosyn-
value within the range of what moringa sprouts presented. For
thetic pathways of phytochemicals, especially glucosinolates.
phytates, a Recommended Dietary Allowance (RDA) has not been
Lastly, studies should be conducted where sprouts are sensorially
established, but it is estimated that the Western citizen consumes
evaluated as non-conventional food. In addition, determine the
250–800 mg of phytates per day and that these values increase for
bioavailability and bioaccessibility of phytochemicals once the
vegetarians and developing countries whose diets mainly consist
sprouts are consumed is highly encouraged.
of cereals and legumes (Frølich et al., 2011). It is noted that the
concentration of phytates in moringa sprouts is not so different
from that found in conventional cereal sprouts. 6. Conclusions
Saponins have also aroused interest due to their both harmful
and beneficial properties. Scientific evidence suggests that these Many investigations discuss M. oleifera uses and potentialities,
compounds stimulate the immune system against cancer, reduce but there is scarce literature characterizing its seeds’ germination
blood lipids and glucose, and inhibit caries and platelet aggregation process. The search for non-conventional foods with important
(Shi et al., 2004). In addition, as an antinutrient, they have been nutritional properties and beneficial health effects is critical for
linked to hemolysis, inhibition of digestive enzymes, and reduced food science scientists, for which the agri-food area is highly rele-
absorption of fat-soluble vitamins (Samtiya et al., 2020). Saponin vant. As a working group, we are focused on addressing some of
concentrations of 0.008–0.680 g 100 g 1 have been reported in the issues described above to contribute to science by filling the
moringa sprouts, while in the soybean (Glycine max), chickpea information gap in the area and the technological development
(Cicer arietinum) and peas (Pisum sativum L.) values of 5.6, 3.6 y of new foods.
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