Mistletoe Contains Higher Secondary Metabolites
Than the Host Plant at the Host-Parasite Interface:
Insights From Tapinanthus Globiferus Collected In
Enugu, Nigeria
Godswill Ajuziogu
University of Nigeria Faculty of Biological Sciences
G C Agbo
University of Nigeria Faculty of Pharmaceutical Sciences
Reginald Njokuocha
University of Nigeria Faculty of Biological Sciences
Anthony Nweze
University of Nigeria Faculty of Biological Sciences
Eugene O Ojua ( eugene.ojua.pg78127@unn.edu.ng )
University of Nigeria Faculty of Biological Sciences https://orcid.org/0000-0001-8280-1175
Pamela Ogujawa
University of Nigeria Faculty of Biological Sciences
Research article
Keywords: Host-parasite interface, Phytochemicals, Quercetin, Tapinanthus globiferus, Wood chemistry
DOI: https://doi.org/10.21203/rs.3.rs-409650/v1
License: This work is licensed under a Creative Commons Attribution 4.0 International License.
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Page 1/13
Abstract
Background: This study aims at evaluating the phytochemicals composition at the host-parasite
interfaces of parasitic plant Tapinanthus globiferus (mistletoe) and four host plants. Wood tissues of the
hosts and the parasite at the host-parasite interface were collected and analyzed to determine the
presence secondary metabolites.
Results: The result showed that avonoids, saponins, and glycosides were present in the plants and
parasite samples. The results revealed higher concentration of avonoids (P < 0.05) in the parasite of C.
acuminata (1190.33 ± 48.23 mgQE/g) and P. macrophylla (1482.55 ± 31.35 mgQE/g) than in the host
plant. Saponins was signi cantly (P < 0.05) higher in the parasites as compared to their respective host.
Conclusion: At the host-parasite interface, signi cantly higher phytochemicals in the wood portion of T.
globiferus was observed as compared to the host plants wood; however, the variability in phytochemical
content of T. globiferus is dependent on the host. Therefore, milestoe would be a better source of
bioactive compounds with high medicinal values than their host plants if explored further.
Background
Enormous biologically active compounds with a variety of chemical structures and properties are all
deposited in the plant kingdom.[1] Phytochemical is a broad word generally used to describes a wide
diversity of compounds that are found naturally in plants. They are found in the different parts of the
plants; such as roots, stem, barks, leaves, owers, seeds and pulps.[2] Phytochemicals otherwise known
as secondary metabolites present in smaller quantities in higher plants, include the avonoids, alkaloids,
terpenoids, tannins, steroids etc.[3] These bioactive secondary metabolites helps the plant to overcome
temporal or continuous threats integral to their environment, while also controlling essential functions of
growth and reproduction. In other words, they are essential for the survival and proper functioning of
plants.[4]
Medicinal properties of plants are dependent on a number of chemically active substances that produces
a de nite physiological action on a biological assay. In general terms, the phytochemicals in plants play
an important role in their medicinal properties. Nevertheless, medicinal plants are the richest bio-resource
of drugs in traditional system of medicine and the phytochemicals are responsible for the different
avours, colours, and smell of plants. These secondary metabolites (phytochemicals) have recently
become of great interest owing to their versatility.[5] Phytochemicals in plants are been utilized globally as
the traditional herbal medicine. These phytochemicals are present in the different plant parts and are
used for healing of certain disorder like diabetes, arthritis, cancer, etc.[6] Secondary metabolites are
economically vital in the manufacturing of drugs, fragrances, dyes, pesticides and food additives.
Therefore, researchers have laid more emphasis on phytochemical studies.[2]
Page 2/13
Tapinanthus globiferus (mistletoes) are the predominant group of plant semi-parasitic ever green shrubs
which belong to the family Loranthaceae. They grow on the branches of host trees or shrubs and take
water and nutrients from the host’s vasculature. Mistletoes include notorious parasites and are capable
of destroying the trees and shrubs of economic value. However, they have been reported to attack a large
number of varieties of taxonomically unrelated hosts and their attack has been proved to be fatal to
various trees and shrubs.[7] This parasitic plant thrives on deciduous trees preferring those with soft bark
like old apple trees, guava, cocoa, citrus and other trees.
Though Mistletoes are generally recognized as destructive agents to various valuable species, they do not
seem to have received much attention from both researchers and plant scientists. Presence of various
phytochemicals such as glycosides, alkaloids, viscotoxins, phenylpropannoids, tannins, lignins, lectins
and sugars has been reported in the mistletoe collected from different host plant. Mistletoes found on
various host trees is endowed with different antioxidant activity; however, the antioxidant capacity of the
extract could vary according to the harvesting time of the plant as well as nature of the host tree[8, 9]. Very
often, host trees that are attacked by mistletoes suffer from them as the triumph of mistletoes lead to
poor growth and productivity and eventual death of such host plants. The reason for the successful
parasitism of mistletoes may be related to the phytochemical interaction between the host and the
parasite. Nevertheless, there is insu cient information on the phytochemical study of parasitic plants
and their hosts in order to detect the secondary metabolites present at the host-parasite interface. The
increasing interest in powerful biological activity of phytochemicals outlined the necessity of determining
their composition at the host-parasite interface of T. globiferus and its four named hosts. This study
generally aims at evaluating the phytochemical composition at the host-parasite interfaces among Citrus
sinensis, Pentaclethra macrophylla, Cola acuminata and Persea americana.
Results
The qualitative phytochemistry as presented in Table 1 shows that only avonoids, saponins and
glycosides were present in the different plant host and parasites at different level of abundance. The
quercetin calibration curve gave a regression equation of Abs = 0.0003[ avonoids] + 0.0479 with a
96.05% coe cient of determination to determine the avonoids concentration (Supplementary material,
Fig. 1). The absorbance of digitoxin standards which was plotted against digitoxin concentration gave a
regression equation of Abs = 0.00015[glycosides] + 0.0479 and R2 of 0.9700 for the determination of the
total glycoside content (TGC) of the wood extracts (Supplementary material, Fig. 2). Similarly, the
absorbance readings of diosgenin standard varied from 0.0377 to 0.1386. However, the total saponins
content (TSC) of the extracts were determined from the regression equation for the calibration curve (Abs
= 0.0013[saponins] + 0.0042; R2 = 0.9459) (Supplementary material, Fig. 3).
Page 3/13
Table 1
Qualitative Phytochemical Analysis of the Pulverised Samples
Pulverised Samples
P. americana
C. acuminata
P. macrophylla
C. sinensis
Host
Parasite
Host
Parasite
Host
Parasite
Host
Parasite
Flavonoids
-
-
++
++
-
++
++
-
Tannins
-
-
-
-
-
-
-
-
Saponins
-
+
-
+
-
+++
++
+++
Alkaloids
-
-
-
-
-
-
-
-
Glycosides
-
-
+
++
-
++
-
-
Terpenoids
-
-
-
-
-
-
-
-
Steroids
-
-
-
-
-
-
-
-
Phyto-constituents
+ = low in abundance; ++ = moderate in abundance; +++ = high in abundance; - = absent
Flavonoids was observed to be present in both the C. acuminata host and milestoe parasite, however,
avonoids was signi cantly (P < 0.05) concentrated in the parasite as compared to the host plant
(Table 2). Similarly, the parasite recorded considerably a signi cant (P < 0.05) amount of avonoids in P.
macrophylla as compared to the host plant whereby avonoids was not detected. In contrast, avonoids
was found in the host of C. sinensis but was not detected in the parasite (Table 2). The total glycosides
content recorded in the host and parasite of C. acuminata were not signi cantly different, while P.
macrophylla and P. Americana had total glycosides content in their respective parasites but the different
host had no glycosides (Table 3). Saponins was observed to be present in both the host and milestoe
parasite of C. sinensis, however, it was signi cantly (P < 0.05) higher in the parasite as compared to the
host plant (Table 4). Alternatively, saponins content was only found in the parasites of C. acuminata, P.
macrophylla and P. Americana (Table 4).
Page 4/13
Table 2
Total Flavonoids content (mgQE/g) of the host and parasites of the studied plants
Plant
Host
Parasite
C. acuminata
849.22 ± 9.09a,2
1190.33 ± 48.23b,1
P. macrophylla
0.00 ± 0.00c,2
1482.55 ± 31.35a,1
C. sinensis
409.22 ± 7.78b,1
0.00 ± 0.00c,2
P. americana
0.00 ± 0.00c,1
0.00 ± 0.00c,1
*means with different alphabet along each vertical array represents signi cant differences (P < 0.05)
among the plants and parasites, while means with different numbers along each horizontal array
signi es signi cant differences (P < 0.05) between the host and parasite.
Table 3
Total glycosides content (mgDE/g) of the host and parasites of the studied plants
Host
Parasite
C. acuminata
276.00 ± 88.19a,1
398.44 ± 4.44a,1
P. macrophylla
0.00 ± 0.00b,2
360.54 ± 0.11b,1
C. sinensis
0.00 ± 0.00b,1
0.00 ± 0.00c,1
P. americana
0.00 ± 0.00b,2
367.33 ± 6.67b,1
*means with different alphabet along each vertical array represents signi cant differences (P < 0.05)
among the plants and parasites, while means with different numbers along each horizontal array
signi es signi cant differences (P < 0.05) between the host and parasite.
Table 4
Total saponins content (mgDE/g) of the host and parasites of the studied plants
Host
Parasite
C. acuminata
0.00 ± 0.00b,2
39.39 ± 9.07c,1
P. macrophylla
0.00 ± 0.00b,2
59.54 ± 9.78ab,1
C. sinensis
36.23 ± 8.53a,2
74.71 ± 1.11a,1
P. americana
0.00 ± 0.00b,2
45.28 ± 13.07bc,1
*means with different alphabet along each vertical array represents signi cant differences (P < 0.05)
among the plants and parasites, while means with different numbers along each horizontal array
signi es signi cant differences (P < 0.05) between the host and parasite.
Discussion
Page 5/13
The aim of this study was to evaluate the phytochemicals present in the extracts of selected plants and T.
globiferus at the host-parasite interface. The levels of the phytochemical contents evaluated varied
signi cantly by plant species and their parasites. The in uence of the host plant on secondary metabolite
levels of mistletoes is well-known. This has been associated to their parasitic habit that photosynthesizes
but depends on the host for water and nutrients for photosynthesis.[14, 15] It was observed that the
parasite generally contained higher concentrations of the phytochemicals evaluated than their host
species. This observation is similar to the report of Lo Gullo et al.[16] who reported higher concentrations
of minerals in parasites than their host species. The variation in secondary metabolites had been
described by Urban et al.[17] to be as a result of the transpiration rates of mistletoes being higher than that
of the host plants.[9, 15] However, the differences in phytochemicals in the wood of the host plant and the
parasite at the interface could signify that they were two different plant species. More so, the differences
in phytochemical contents in mistletoes from different host could also be in uenced by the environment
the host plant faces, such as soil fertility.[15, 18] Therefore, the inconsistent concentration of
phytochemicals observed in our study could be due to the differences in species as well as in the
environment.
Flavonoids defend plants against a variety of biotic and abiotic stresses by demonstrating a wide
spectrum of biological functions and play a signi cant function in the interaction between the plant and
their environment.[19] The increased avonoid content in C. acuminata and P. macrophylla could be an
indication that the parasites were more exposed to environmental stress than the host. Studies show that
avonoids could have a determinant role in response to different stresses such as drought.[20] In this
regard, Nakabayashi et al.[21] reported that the over expression of some genes involved in avonoid
metabolism and over accumulation of avonoids would caused an increase in drought tolerance.
Therefore it would be reasonable to suggest that, the parasites utilizes this as a medium of survival since
the transpiration rates of mistletoes are higher than that of the host plants.[17]
Saponins are usually found in tissues that are highly susceptible to attacks by bacteria, fungi or insects.
[22]
Hence, it is assumed that one of the roles saponins plays in plants is to act as a chemical barrier in
opposition to prospective pathogens. Therefore, this would account for their antimicrobial activity.[23, 24]
Due to their toxicity to various organisms, saponins can be utilised for their insecticidal, antibiotic,
fungicidal, and pharmacological properties.[24]
Conclusion
At the host-parasite interface, signi cantly higher phytochemicals in the wood portion of Tapinanthus
globiferus (milestoe) was observed as compared to the host plants wood, however, the variability in
phytochemical content of Tapinanthus globiferus is dependent on the host. From these ndings, milestoe
grown on C. acuminata and P. macrophylla will be rich in avonoids, while C. sinensis host favours the
production of saponins in milestoe. Therefore, milestoe would be a better source of bioactive compounds
with high medicinal values than their host plants if explored further.
Page 6/13
Materials And Methods
Collection and Authentication of Plant Specimens
The twigs of mistletoes parasites from C. sinensis, P. macrophylla, C. acuminata and P. americana and
their respective host stems were collected from farmlands in Alor-Agu, Igboeze South L.G.A, Enugu,
Nigeria with the approval of the locals and authenticated and deposited by Mr. Felix Nwafor in the
Department of Pharmacognosy and Environmental Medicines Habarium, University of Nigeria Nsukka,
Enugu, Nigeria with voucher specimen number of PCG/UNN/00266 (Tapinanthus globiferus),
PCG/UNN/0056 (C. sinensis), PCG/UNN/0080 (P. macrophylla), PCG/UNN/0330 (C. acuminata) and
PCG/UNN/0012) P. americana. The plant specimens were cleaned, air-dried at room temperature and
reduced to ne particles. The air-dried samples were pulverised and 10g of each samples were macerated
with 100mL of methanol and kept at room temperature for 48hrs with agitation. The solvents were dried
in vacuo at 40°C to obtain the dry extracts.[10]
Qualitative phytochemical analysis of the pulverised samples was done to determine the presence of
secondary metabolites ( avonoids, tannins, saponins, alkaloids, glycosides, terpenoids and steroids)
according to standard procedure.[11] The con rmed metabolites where then further analyzed
quantitatively.
Preparation of the Calibration Curves
Quercetin
A quercetin stock solution was prepared by dissolving 10mg in 10mL methanol to give a stock solution of
(1000 mg/L). The stock solution was further diluted to different concentrations of 100, 80, 60, 40 and
20mg/L. 1mL each of the different concentration of quercetin was mixed with 4mL of distilled water and
0.30mL of 5% (w/v) sodium nitrite. After 5 min, 0.30mL of 10% (w/v) AlCl3.6H2O solution was added to
the mixture, followed by addition of 2mL of 1.0M NaOH after another 5min and diluted to 10mL with
distilled water. The absorbance of the different concentrations was then measured against the reagent
blank at 510nm with a UV/Visible spectrophotometer.
Digitoxin: The standard curve was prepared by adding 0.2mg/mL digitoxin in chloroform – methanol
(1:1; v/v). A solution of 0.1, 0.2, 0.3, 0.4 and 0.5mL each (equivalent to 0.02, 0.04, 0.06, 0.08 and 0.10mg
of digitoxin respectively) was transferred to a dry Erlenmeyer asks and evaporated to a small bulk
(0.35mL) and made up to volume with distilled water. Freshly prepared Baljet’s reagent (10mL) was
added to each ask and allowed to stand for 1 h at room temperature and the resulting mixture diluted
with 20mL of distilled water. The absorbance of the colour developed was determined using a
spectrophotometer against a suitable blank at 495 nm.
Diosgenin
Page 7/13
Diosgenin standard (0.20mg/mL) was dissolved in methanol and 0.1, 0.2, 0.3, 0.4 and 0.5mL (equivalent
to 0.02, 0.04, 0.06, 0.08 and 0.10mg of diosgenin respectively) each of the standard solution was
transferred to a dry test tubes. Vanillin-acetate solution (0.20mL of 5% (w/v)) was added, and followed by
the addition of 0.80mL sodium perchlorate solution. The mixture was shaken and heated for 15mins in a
water bath at 60oC. After cooling, 5mL of glacial acetic acid was added to each test tubes and the
absorbance of the mixtures determined against the blank using a UV/Visible spectrophotometer at 548
nm.
Determination of Total Flavonoids Content (TFC)
Aluminium-chloride colourimetric assay was used to determine the total avonoids content in the extracts
as adopted by Agbo et al.[10] The extracts (1mg/mL) were prepared following the same procedure in
preparing quercetin as reported above. The absorbance of the extracts was measured against the reagent
blank at 510nm with a UV/Visible spectrophotometer. The total avonoids content was determined from
the calibration curve and expressed as milligram of quercetin equivalent per gram of extracts (mgQE/g).
Determination of Total Glycosides Content (TGC)
Balet’s reagent colourimetric method was used for the determination of the total glycosides content of the
extracts as previously reported with slight modi cation by To ghi et al.[12] The extract (1mg/mL) was
dissolved with 6mL of distilled water and 1mL of 12.5% (w/v) lead acetate solution was added. The
mixture was made up to 10mL with distilled water and ltered. The ltrate (5mL) was transferred to a
volumetric ask, 1mL of 4.77% (w/v) Na2HPO4 solution added, and made up to 10mL with distilled water
and ltered. Baljet’s reagent (10mL) was added to 1mL of the clear ltrate and the mixture allowed to
stand for 1h and diluted with 20mL of distilled water. The absorbance of the mixture was read against
the blank at 495nm with a UV/Visible spectrophotometer. The total glycosides content was determined
from the calibration curve and expressed as milligram of digitoxin equivalent per gram of extracts
(mgDE/g).
Determination of Total Saponins Contents (TSC)
Vanillin-acetate colourimetric method was used for the determination of the total saponins content of the
extracts as previously reported by Benyong et al.[13] with slight modi cation. A freshly prepared 5% (w/v)
vanillin-acetate solution (0.20mL) was added to 0.10mL of the extract (1mg/mL) in a test tube followed
by the addition of 0.80mL (w/v) sodium perchlorate solution. The mixture was shaken and heated for
15mins in a water bath at 60oC and cooled. 5mL of glacial acetic acid was added to the mixture and the
absorbance of the mixture read against the blank at 548nm using a UV/Visible spectrophotometer. The
total avonoids content was determined from the calibration curve and expressed as milligram of
diosgenin equivalent per gram of extracts (mgDE/g).
Data analysis
Page 8/13
The entire quantitative tests were carried out in triplicates and data collected were for the host and
parasite were subjected to Analysis of Variance (ANOVA) using IBM SPSS ver. 20.
Abbreviations
TGC - Total glycoside content
TSC - Total saponins content
AlCl3.6H2O - Aluminium chloride hexahydrate
NaOH - Sodium Hydroxide
ANOVA - Analysis of Variance
Declarations
Ethics approval and consent to participate: Not applicable
Consent for publication: Not applicable
Competing interests: The authors declare that they have no competing interests
Funding: No funding received
Authors' contributions: AGC and OPC managed the analyses of the study, edited the draft of the
manuscript. NRC and OEO managed the literature searches, performed the statistical analysis and
wrote the rst draft of the manuscript. AGC and NAE designed the study, wrote the protocol and
edited the draft of the manuscript. All authors read and approved the nal manuscript.
Acknowledgements: God almighty for his faithfulness and the Department of Plant Science and
Biotechnology for providing the enabling environment for this research
Availability of Data and Materials: Not applicable
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Figures
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Figure 1
Calibration Curve for Quercetin Standards
Figure 2
Calibration Curve for Digitoxin Standards
Page 12/13
Figure 3
Calibration Curve for Diosgenin Standards
Page 13/13