Production and Evaluation of A Moringa Oleifera Liquid Biofertilizer To Improve Seedling Growth of Three Crop Plants

Chan-Keb et al.
: Production and evaluation of a Moringa oleifera liquid biofertilizer to improve seedling growth of three crop plants
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PRODUCTION AND EVALUATION OF A MORINGA OLEIFERA

LIQUID BIOFERTILIZER TO IMPROVE SEEDLING GROWTH
OF THREE CROP PLANTS
CHAN-KEB, C. A.1 – AGRAZ-HERNÁNDEZ, C. M.2 – GUTIÉRREZ-ALCÁNTARA, E. J.1 – RUIZ-
HERNÁNDEZ, J.1 – PÉREZ-BALAN, R. A.1* – DZUL-CAAMAL, R.2 – MAS-QUI, O. O.1 – UC-
PERAZA, R. G.3 – CAMACHO-CHAB, J.4 – MENDOZA-ARROYO, G. E.5
1
Facultad de Ciencias Químico Biológicas, Universidad Autónoma de Campeche, Avenida Ing.
Humberto Lanz Cárdenas S/N, Colonia Ex Hacienda Kalá, C.P. 24085 San Francisco de
Campeche, Campeche, México
Instituto EPOMEX, Universidad Autónoma de Campeche, Av. Heroe de Nacozari #480,

2
Campus 6 de Investigaciones, C.P. 24029, San Francisco de Campeche, Campeche, México

3
División de Desarrollo Sustentable, Universidad Autónoma de Quintana Roo, C.P. 77019
Chetumal, Quintana Roo, México
Departamento de Microbiología Ambiental y Biotecnología, Universidad Autónoma de

4
Campeche Colonia Buenavista, San Francisco de Campeche 24039, Campeche, México

5
Instituto Tecnológico de Chiná, Laboratorio de Microbiología, Tecnológico Nacional de
México, C. P. 24520, Campeche, Campeche, México
*Corresponding author
e- mail: roaperez@uacam.mx; phone: + 52-981-811-9800 (ext. 2010110)
(Received 12th Nov 2023; accepted 18th Jan 2024)
Abstract. The growing demand for food due to the increase in the world’s population has led to an
increased demand for chemical fertilizers of industrial origin and improper management of crops, causing
adverse effects on the environment and soil. In this research, the effect of Moringa oleifera as a
biofertilizer on morphometric variables (seed germination, root, and stem elongation) was evaluated in
lettuce (Lactuca sativa), corn (Zea mays L.) and beans (Phaseolus vulgaris L.), for each species were
exposed to 5 dilutions of the aqueous solution of the biofertilizer. The highest percentage of germination
was observed at a concentration of 12.5% of the biofertilizer in the three species, however, no significant
differences were observed between treatment and species (p > 0.05). Likewise, greater growth in stem
and root length was observed at a concentration of 12.5% in the 3 species, showing significant differences
between species and treatment (p < 0.05). On the other hand, it was generally observed that increasing the
concentration of the biofertilizer inhibits the growth of the stem and root. The results obtained in this
study could contribute as a reference to future chronic studies of exposure to biofertilizers using lettuce,
corn, and beans considering other types of bioindicators to be evaluated in the plant, at different
concentrations of exposure. This is to contribute to the use of biofertilizers in commercially important
sustainable agricultural plantations and thus be able to prevent or mitigate environmental impacts in the
short, medium, and long term on soils and crops, as well as the reduction or replacement of the use of
inorganic fertilizers of industrial origin and the promotion of the use of biofertilizers.
Keywords: nutrients, corn, Phaseolus vulgaris, morphometry, germination
Introduction
In recent decades, the need to meet the growing demand for food due to the increase
in population has led to the demand for the consumption of agricultural products, where
the objective of producers is to achieve high crop yields per unit area, without
APPLIED ECOLOGY AND ENVIRONMENTAL RESEARCH 22(2):1455-1465.

http://www.aloki.hu ● ISSN 1589 1623 (Print) ● ISSN 1785 0037 (Online)
DOI: http://dx.doi.org/10.15666/aeer/2202_14551465
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Chan-Keb et al.: Production and evaluation of a Moringa oleifera liquid biofertilizer to improve seedling growth of three crop plants
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considering the sustainability of production (feasibility, technique, profitability, and

environmental damage) (Grageda-Cabrera et al., 2012). In this quest to improve the
production rate, elemental nutrients, such as phosphorus, potassium, and nitrogen were
supplied to soils by the application of chemical fertilizers (Navarro-García, 2023).
Fertilizers increase crop yields, however, it has been observed that the constant use of
chemical-based fertilizers affects the quality of soils and poses a health risk to
consumers (Calderón et al., 2019). Therefore, producers currently prefer to change
production techniques towards green agricultural practices with the use of new
biotechnologies, such as the use of biofertilizers. (Deepika and MubarakAli, 2020).
Biofertilizers are organic fertilizers that can be composed of living microorganisms,
organic debris (plant debris and animal waste), and plant extracts (Armenta Bojórquez
et al., 2010; Emongor, 2015). The latter is used as plant growth regulators, as they
positively modify plant growth by improving the efficiency of photosynthesis (Pérez-
Gómez et al., 2019).
In this sense, one of the plants with the greatest potential for the manufacture of plant
extracts is Moringa oleifera Lam (syn. M ptreygosperma Gaertn). This plant is one of
the best-known and widely studied species around the world, due to its versatile
usefulness as food, nutraceutical, medicinal uses, and pharmacological properties.
(Anwar et al., 2007). By the Phytochemical Analysis of M. oleifera researchers from
different countries have shown that the leaves are particularly rich in potassium,
calcium, phosphorus, iron, vitamin D, essential amino acids, as well as known
antioxidants such as carotene, vitamin C, and flavonoids (Al_husnan and Alkahani,
2016). For this reason, various medicinal properties have been attributed to almost all
parts of the plant: root, bark, gum, leaf, fruit (pods), flowers, seed, and seed oil (Anwar
et al., 2007). Antihypertensive, diuretic, and cholesterol-lowering activity has been
reported, due to the combination of diuretic, lipid-lower, and hypotensive components
that make the plant very useful against cardiovascular disorders (Patel et al., 2010).
Similarly, it has been reported that the roots of M. oleifera They antispasmodic,
antiulcer and hepatoprotective activity (Anwar et al., 2007; Pérez-Gómez et al., 2019).
In addition, ethanol extract and its leaf components have been found to have
antispasmodic effects, possibly through blockade the of calcium channels. (Cáceres et
al., 1992). Finally, it has been shown that M. oleifera has an antimicrobial effect on
pathogenic bacteria, attributed to antimicrobial peptides and bioactive compounds
(Tirado-Torres et al., 2019)
Biotechnology offers alternatives to meet the growing demand for food, through
biofertilizers that provide plants with growth regulation to positively modify plant
growth and improve yields per hectare. (Emongor, 2015). Therefore, M. oleifera
appears to be an ideal candidate for the manufacture of extracts for plant breeding of
agricultural production due to the active substances it contains. (Olson, 2011). Moringa
leaf extract has been reported to contain, zeatin, dihydrozeatin, and isopenthyladenine,
which are natural cytokinins that stimulate cell division, tissue growth, slow senescence,
and aging processes in many plant tissues, promote nutrient partitioning and absorption
(Anwar et al., 2007; Cáceres et al., 1992; Emongor, 2015). The use of Moringa extracts
as a potential plant growth enhancer has the potential to provide an environmentally
safe, easily accessible means of increasing crop yields and meeting the exponentially
growing demand for food. The use of biofertilizers, which enhance plant growth, could
improve production and yield conditions in agriculture and have significant economic
advantages. Therefore, the objective of this study was to evaluate the germination and

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growth of agriculturally important seedlings such as beans (Phaseolus vulgaris), lettuce

(Lactuca sativa), and maize (Zea mays) through the use of the aqueous extract of
Moringa (Moringa oleifera Lam) as a biofertilizer at different concentrations.
Materials and methods

Experimental design with a liquid biofertilizer from Moringa oleifera
The experiment was conducted at the Faculty of Chemical-Biological Sciences of the
Autonomous University of Campeche, Mexico. The sowing of the lettuce seeds and the
analysis of the samples were carried out in February 2022.
Lettuce (Lactuca sativa), corn (Zea mays L.), and bean (Phaseolus vulgaris L.) seeds
were used to perform the bioassay. For this bioassay, 1 liter of stock solution of 3 g L-1
(w/v) of powdered dried leaves of Moringa oleifera (Therbal ®) was prepared by
infusion with distilled water. The nutritional information of Moringa oleifera leaves is
shown in Table 1.
Table 1. Nutrition information and average concentration (± standard deviation) of nutrients

per 100 g dry weight of Moringa oleifera leaves
Nutritional content Concentration/100 g
Energy 304 ± 47 kcal
Humidity 7.4 ± 2.0 mg
Protein 22 ± 5 g
Carbohydrates 28 ± 9.2 g
Grease 7 ± 2.5 g
Fibre 9 ± 7.45 g
Tannins 1.2 ± 1.4 g
Ca 1890 ± 748.4 mg
P 298 ± 149.0 mg
Na 220 ± 180.0 mg
K 1467 ± 636.7 mg
Mg 473 ± 429.4 mg
Fe 32.5 ± 10.78 mg
Zn 2.0 ± 1.10 mg
Cu 0.95 ± 0.40 mg
The analysis of the concentration of nutrients in the leaves of Moringa Moringa

oleifera was carried out according to the Mexican Official Standard (NOM-086-SSA1-
1994).
To determine the effect of Moringa oleifera as a biofertilizer, 5 treatments were
carried out for each species of agricultural importance with concentrations of 12.5%,
25%, 50%, 75%, and 100%, which were obtained from successive dilutions in triplicate
and for the negative control of germination and growth, distilled water was used, for a
total of 48 experimental units. For each unit and treatment, 15 seeds of each species
were placed in a 100 mm diameter polyethylene container (Petri dish), with filter paper
(Whatman® No. 3) at the bottom as a support. Subsequently, 15 ml of each of the
concentrations of the aqueous solution were applied, 3 times a day. All units were kept
at a controlled room temperature of 29°C ± 1 for 240 h (10 days). At the end of the

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exposure period, the number of germinated seeds was counted and the length of the root
and stem was measured. The mean and standard deviation of radicle length and
hypocotyls were determined as response variables, in the negative control and each
treatment (exposure concentrations). In addition, the germination percentage (%G) of
the seeds for each concentration concerning negative control was determined according
to the equation of Chan Keb et al. (2018) (Eq. 1).
(Eq.1)
Statistical analysis
To evaluate the effect of Moringa oleifera as a biofertilizer on morphometric variables
(seed germination, root, and stem elongation) in lettuce (Lactuca sativa), corn (Zea mays
L.), beans (Phaseolus vulgaris L.), were compared between the five treatments and the
exposed control, to determine the variation or interaction of these two factors, applying a
two-way ANOVA. Before this comparison analysis, the normality of the variables was
validated with the method of Shapiro and Wilks (1965), with a significance level
α = 0.05, as it did not meet the assumption of normal distribution, the data were
transformed using the Box-Cox method, so that the variables presented the assumptions
of normal distribution (Zar, 2010). Post-hoc analysis was realized with least significant
difference (LSD) Fisher test. All statistical analyses were performed using STATISTICA
V.12 (©Copyright StatSoft, Inc., Palo Alto, CA, USA, 1984–2014).
Results
Figure 1 shows the data on the percentage of germination of the seeds of lettuce
(Lactuca sativa), corn (Zea mays L.), and beans (Phaseolus vulgaris L.) concerning the
negative control of distilled water. The seeds of the germinated species in the negative
control were lower than the exposed treatments, however, statistically, no significant
differences were observed (p ≥ 0.05, Table 2). The highest amount of germinated seeds
of the three species was observed at concentration of 12.5% and the lowest amount was
observed in Lactuca sativa at a concentration of 25% (Fig. 1).
Exposure to different concentrations of the liquid biofertilizer made from Moringa
oleífera leaves showed variation in the development of root length and hypocotyls of
lettuce, beans, and corn (Fig. 2A, B). A 2-way ANOVA showed significant differences
between species and exposure concentrations in the average root length and hypocotyl
development of Lactuca sativa, beans, and maize (Tables 2 and 3). From the above,
considering all the concentrations of the liquid biofertilizer made from Moringa oleífera
exposed, greater root growth was observed in the corn seedlings, compared to the root
of the bean and lettuce seedlings (Fig. 2A; Table 3); it was also observed that in the
treatments to which the 3 species were exposed, the highest root growth was presented
at a concentration of 12.5% of the biofertilizer (Fig. 3).
Figure 2B shows the effect of growth on the stem of the 3 species exposed to the
different concentrations of the biofertilizer, and it was also observed that the greatest
stem growth occurred in the bean seedlings, compared to the stem length of the corn
and lettuce seedlings. However, it was also observed in the treatments to which the 3
species were exposed the highest stem growth at a concentration of 12.5% of the
biofertilizer (Fig. 3).

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Table 2. Two-way analysis of variance concerning germination, root length, and hypocotyls
of Lactuca sativa corn and beans between concentrations of the biofertilizer (Control,
12.5%,25%, 50%, 75%, and 100%), with a significance level of p < 0.05
Parameter Factor df F p
Treatment 5 9.97 0.0001
Species 2 4.17 < 0.024
Germination (%)
Treatment*Especies 10 1.31 0.260
Error 36
Treatment 5 19.85 < 0.0001
Species 2 987.73 < 0.0001
Root length (cm)
Treatment*Especies 10 7.08 < 0.0001
Error 36
Treatment 5 34.85 < 0.0001
Species 2 1086.22 < 0.0001
Hypocotyl length (cm)
Treatment*Especies 10 5.93 < 0.0001
Error 36
Table 3. Post-hoc testing by the Fisher method (LSD), of the treatment and species
interaction of germination, stem, and root length parameters
Treatment*Species Germination (%) Root length (cm) Hypocotyl length (cm)
Control*Corn 95de 13.5652b 4.0783ef
12.5*Corn 100a 16.8913a 6.3961d
25*Corn 96.5cde 12c 3.7ef
50*Corn 96.5cde 12.3333bc 3.9429ef
75*Corn 95de 10.3611de 3.7222ef
100*Corn 96.5cde 11.3958cd 2.7958fg
Control*Beans 95.517de 9.8393e 16.2393b
12.5*Beans 99.017ab 11.2708cd 21.3333a
25*Beans 97bcd 10.5185de 15.9444b
50*Beans 95.517de 9.6364ef 15.5455b
75*Beans 98abc 8.3478fg 12.8043c
100*Beans 98abc 7.7273g 12.9773c
Control*Lettuce 95.167de 1.3333h 3.85ef
12.5*Lettuce 98.936ab 1.7083h 5.1542de
25*Lettuce 94.252e 1.5714h 4.1821ef
50*Lettuce 95.619de 1.1706h 3.5588f
75*Lettuce 94.85de 1.5368h 3.3421f
100*Lettuce 96.205cde 1.445h 1.795g
Means that do not share a letter are significantly different, with a 95% confidence level

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Figure 1. Average germination of seeds of lettuce (Lactuca sativa), corn (Zea mays L.), and
bean (Phaseolus vulgaris L.) between the concentrations of the liquid biofertilizer made from
Moringa oleifera leaves. The error bars represent the standard deviation
Discussion
In general terms, germination, root and stem length of L. sativa, Z. mays, and P.
vulgaris showed variation concerning the control, due to the effect of the moringa
biofertilizer to which they were exposed at different concentrations, which were
absorbed through the roots. The results in the germination of the seeds of L. sativa, Z.
mays, and P. vulgaris show that there was no effect of the biofertilizer at different
concentrations, the highest percentage of germination was observed at a concentration
of 12.5% of the biofertilizer in the three species, similar studies are reported by
Deepika et al. (2020), where they studied the production and evaluation of a liquid
microalgae fertilizer to improve the growth of four crop plants, the four cultivated
species germinated approximately 100% and the highest growth in stem and root were
obtained at 20% in the dilution of a biofertilizer made from microalgae.
For this study, the effect of increased root and stem growth of L. sativa, Z. mays,
and P. vulgaris was greatest at concentrations of 12.5% of the exposed liquid
biofertilizer. In this regard, studies carried out by Pérez-Gómez et al. (2019),
determined that the aqueous extract of moringa leaves favored the initial stage of
acclimatization of pineapple, this is because Moringa oleifera Lam. Leaves have
several chemical constituents such as amino acids, mineral ions, ascorbate,
phytohormones, and secondary metabolites. This means that its extracts are used to
boost the growth of some plants.

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(A)
(B)
Figure 2. Average growth in (A) root length; (B) length of the hypocotyl of Lettuce (Lactuca
sativa), corn (Zea mays L.), and bean (Phaseolus vulgaris L.) between the concentrations of the
liquid biofertilizer made from Moringa oleifera leaves. The error bars represent the standard
deviation

Figure 3. Average growth in (A) root length; (B) length of the hypocotyl of Lettuce (Lactuca
sativa), corn (Zea mays L.), and bean (Phaseolus vulgaris L.) between the concentrations of the
Chan-Keb et al.: Productionmade
liquid biofertilizer and evaluation of a Moringaoleifera
from Moringa oleifera liquid biofertilizer
leaves. The toerror
improve seedling
bars growth ofthe
represent threestandard
crop plants
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deviation.
Crops
Plants Exposure concentrations of Moringa oleifera liquid biofertilizer
Control (0%) 12.5 % 25 % 50 % 75 % 100 %
(a)
(b)
(c)
Figure 3. Crop plant growth benchmarking: bean (Phaseolus vulgaris L.) (a), maize (Zea mays
Figure
L.) (b)4.and
Crop Plant (Lactuca
lettuce Growth Benchmarking: Bean (Phaseolus
sativa) (c), at different vulgarisofL.)
concentrations the(a), Maize
liquid (Zea mays
biofertilizer
L.) (b) and Lettuce (Lactuca
madesativa) (c), at different
from Moringa oleiferaconcentrations of days
leaves after 10 the liquid biofertilizer made
from Moringa oleifera leaves after 10 days.
Also, for this study the effects of biofertilizer on root and stem length decrease in L.
sativa, Z. mays, and P. vulgaris, was observed at the concentration of 75 to 100%, the
effect of decrease was evident in roots and stem length in corn and lettuce. Therefore, we
describe that the root was more sensitive to the aqueous solutions of the biofertilizer, due
to the direct contact in the absorption of the components of the biofertilizer, generating a
physiological stress effect. On the other hand, the absorption of the biofertilizer that is
available in aqueous solution, is through the root system, as the main route for transfer
and direct contact, where the absorption of nutrients and water is also regulated in the
three species of agricultural importance, that is, the morphology, anatomy and biomass
production of the roots which is also associated with the effect on the absorption of
biofertilizer (Rodríguez-Ruiz et al., 2015), as observed in this study. In this regard,
Gómez-Oliván et al. (2014) mention that the presence of high concentrations of isolated
inorganic compounds in the soil can induce oxidative stress in plants and influence their
antioxidant defenses leading to different responses (phytotoxic effects), this will depend
on the type of substance, its concentration and the sensitivity of the plant species
(Carvalho et al., 2014; Marsoni et al., 2014; Minden et al., 2017). Authors such as Biruk
et al. (2017) found that lettuce seeds were more sensitive to extracts containing inorganic
elements than inorganic extracts. On the other hand, Christou et al. (2019) mention that
the bioaccumulation of pollutants in plant tissues depends on the type of soil, the

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physicochemical properties of the pollutants, and the interactions of these factors, as well
as the type of species. Based on the results obtained from this research, more future
studies can be carried out on the evaluation of other types of biofertilizer using lettuce,
corn, and beans considering other types of biochemical indicators of the plant to be
evaluated, different concentrations of the biofertilizer or similar to those used in this
study, to contribute to the use of sustainable biofertilizers in agricultural plantations of
commercial importance and thus be able to prevent or mitigate short-, medium- and long-
term environmental impacts on soils and crops. As well as the reduction or replacement of
the use of inorganic fertilizers of industrial origin.
Conclusions
The present study, it showed high percentages of seed germination in all exposed
crops that had been treated with liquid biofertilizer made from Moringa oleífera leaves
at different concentrations (0%, 12.5%, 25%, 50%, 75%, and 100%), and no significant
differences were observed between the species and treatment in terms of germination.
The growth of root and stem length in the 3 expo sed species showed a maximum
growth in the concentration of 12.5% of the liquid biofertilizer made from the leaves of
Moringa oleifera, however, the liquid biofertilizer in a higher concentration inhibits the
growth of the stem and root. Based on the results of this research, it shows that the use
of biofertilizers is viable for sustainable agricultural practices. Likewise, the application
of Moringa oleifera-based liquid fertilizer, could be useful to enrich the soil and achieve
a high yield in agricultural production. Moringa oleífera biofertilizer applied to 12.5%
in the cultivation of the 3 species showed better results in growth parameters. This may
be due to the high nutrient content contained in the leaves of Moringa oleifera, which is
also commonly known as the tree of life, due to its high benefits to human health and
the high nutrient content it presents. In this way, Moringa oleifera-based liquid
fertilizer could be applied to various crop plants to enrich the nutrients in the soil and, in
turn, increase growth and improve agricultural production.
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Production and Evaluation of A Moringa Oleifera Liquid Biofertilizer To Improve Seedling Growth of Three Crop Plants

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Chan-Keb et al.

PRODUCTION AND EVALUATION OF A MORINGA OLEIFERA

Instituto EPOMEX, Universidad Autónoma de Campeche, Av. Heroe de Nacozari #480,

Campus 6 de Investigaciones, C.P. 24029, San Francisco de Campeche, Campeche, México

Departamento de Microbiología Ambiental y Biotecnología, Universidad Autónoma de

Campeche Colonia Buenavista, San Francisco de Campeche 24039, Campeche, México

APPLIED ECOLOGY AND ENVIRONMENTAL RESEARCH 22(2):1455-1465.

considering the sustainability of production (feasibility, technique, profitability, and

APPLIED ECOLOGY AND ENVIRONMENTAL RESEARCH 22(2):1455-1465.

growth of agriculturally important seedlings such as beans (Phaseolus vulgaris), lettuce

Materials and methods

Table 1. Nutrition information and average concentration (± standard deviation) of nutrients

The analysis of the concentration of nutrients in the leaves of Moringa Moringa

APPLIED ECOLOGY AND ENVIRONMENTAL RESEARCH 22(2):1455-1465.

APPLIED ECOLOGY AND ENVIRONMENTAL RESEARCH 22(2):1455-1465.

APPLIED ECOLOGY AND ENVIRONMENTAL RESEARCH 22(2):1455-1465.

APPLIED ECOLOGY AND ENVIRONMENTAL RESEARCH 22(2):1455-1465.

APPLIED ECOLOGY AND ENVIRONMENTAL RESEARCH 22(2):1455-1465.

Control (0%) 12.5 % 25 % 50 % 75 % 100 %

APPLIED ECOLOGY AND ENVIRONMENTAL RESEARCH 22(2):1455-1465.

[1] Al_husnan, L. A., Alkahtani, M. D. F. (2016): Impact of Moringa aqueous extract on

APPLIED ECOLOGY AND ENVIRONMENTAL RESEARCH 22(2):1455-1465.

APPLIED ECOLOGY AND ENVIRONMENTAL RESEARCH 22(2):1455-1465.

of Moringa oleifera against multidrug-resistant Staphylococcus aureus isolated from raw

APPLIED ECOLOGY AND ENVIRONMENTAL RESEARCH 22(2):1455-1465.

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