Morphological Characterization of Ficus religiosa Genotypes in Iran by Multivariate Analysis

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  • 1 Department of Horticultural Sciences, Faculty of Agriculture, University of Tehran, Karaj, Iran
  • 2 Department of Horticultural Science, Faculty of Agriculture, Khuzestan Agricultural Sciences and Natural Resources University, Mollasani, Iran

Ficus religiosa L. is one of the most popular species in the Moraceae family that is known as a multipurpose forest tree species because of its medicinal, ornamental, and religious value. F. religiosa is an important tree in South Asia, and it possesses various common names such as peepal, bodhi, bo tree, and asvattha. This species as a traditional tree is broadly planted as a roadside tree, and it plays an important role as a medicinal tree in various diseases such as asthma, stomatitis, diabetes, inflammations, glandular swelling disorders, and wound healing. Because F. religiosa is characterized as a subtropical tree, it fully grew in southern parts of Iran. The morphological variation of 72 individuals of F. religiosa from six southern regions of Iran was investigated based on multivariate analysis. Our results indicated that the highest tree, leaf, and petiole lengths, as well as leaf width, were observed in Kish and Qeshm genotypes, whereas the Chabahar genotype had the lowest petiole length. Results of simple correlation analysis showed the existence of significant positive and negative correlations among some important parameters. The highest correlation was observed between leaf, tree, and petiole lengths. Populations were clustered in four groups. The Kish and Qeshm genotypes were closely related to each other and differentiated from the Chabahar genotype. The whole dataset was subjected to principal component analysis (PCA). PCA showed that the first two factor components explained 84.51% of the variation and the first factor component had the positive relationship with leaf, tree, and petiole lengths.

Abstract

Ficus religiosa L. is one of the most popular species in the Moraceae family that is known as a multipurpose forest tree species because of its medicinal, ornamental, and religious value. F. religiosa is an important tree in South Asia, and it possesses various common names such as peepal, bodhi, bo tree, and asvattha. This species as a traditional tree is broadly planted as a roadside tree, and it plays an important role as a medicinal tree in various diseases such as asthma, stomatitis, diabetes, inflammations, glandular swelling disorders, and wound healing. Because F. religiosa is characterized as a subtropical tree, it fully grew in southern parts of Iran. The morphological variation of 72 individuals of F. religiosa from six southern regions of Iran was investigated based on multivariate analysis. Our results indicated that the highest tree, leaf, and petiole lengths, as well as leaf width, were observed in Kish and Qeshm genotypes, whereas the Chabahar genotype had the lowest petiole length. Results of simple correlation analysis showed the existence of significant positive and negative correlations among some important parameters. The highest correlation was observed between leaf, tree, and petiole lengths. Populations were clustered in four groups. The Kish and Qeshm genotypes were closely related to each other and differentiated from the Chabahar genotype. The whole dataset was subjected to principal component analysis (PCA). PCA showed that the first two factor components explained 84.51% of the variation and the first factor component had the positive relationship with leaf, tree, and petiole lengths.

Ficus is the genus of 1000 species in the family Moraceae, mainly distributed throughout tropical and subtropical regions (Hesami and Daneshvar, 2018). Many of this species have ornamental value and are also used as medicinal plants. Ficus religiosa L. is a long-lived, large, fuel wood, medicinal, ornamental, and evergreen perennial tree with glossy green foliage, native to India, mainly found in Pakistan, Bangladesh, Ceylon, China, Burma, Thailand, and Iran (Hesami et al., 2017b; Hesami et al., 2018b; Singh et al., 2011). It is also known as a roadside tree and most frequently found near temples. Different parts of F. religiosa are extensively used in indigenous medicine, especially for their antibacterial (Pawar and Nabar, 2010), anticonvulsive (Patil et al., 2011), antidiabetic (Kirana et al., 2009), antinephropathic (Ballabh et al., 2008), wound healing (Ghosh et al., 2016), anti-inflammatory and analgesic (Singh et al., 2011), antimicrobial and antiviral (Cagno et al., 2015), antihyperlipidemic (Keshari et al., 2016), antioxidant (Pandit et al., 2010), immunostimulant (Mallurwar and Pathak, 2008), antiasthmatic (Vinutha et al., 2007), and anticancer activities (Sankar et al., 2014) and parasympathetic modulatory (Dwivedi et al., 2014), as well as nootropic effects (Bhangale et al., 2016). F. religiosa can be multiplicated by various methods, such as seed or vegetative methods (Hesami et al., 2017a; Hesami et al., 2018a; Salmi and Hesami, 2016). Recently, the intricate taxonomy of F. religiosa and other related species was highlighted by Ferrer-Gallego et al. (2016). Some traditional techniques for identification and characterization of genotypes and species are mainly focused on phenotypic observations. Morphological traits are known as an efficient and applicable way for preliminary evaluation because they can be applied as a general method for evaluating genetic diversity among morphologically distinguishable individuals and their simple evaluation as well. Morphological features in accompany with multivariate statistical methods, such as PCA that was broadly used, and cluster analysis, are applicable means for screening individuals for many plants such as Cerasus subgenus (Khadivi-Khub et al., 2012), Prunus dulcis (Chalak et al., 2007), Origanum vulgare (Andi et al., 2011), and Punica granatum (Sarkhosh et al., 2009). Also, multivariate methods can help to assess large datasets and resolve various phenotypic and genotypic evaluations into fewer more interpretable and more easily visualized groups (Hesami et al., 2017c).

The feasible details about the diversity of morphological features within and among various subspecies of F. religiosa may be applied in the delimitation of subspecies and also it can be used in breeding programs and conservation of this valuable plant. Therefore, this article explains morphological variable of F. religiosa in different regions of Iran that also could apply to understanding the taxonomy of this valuable plant.

Materials and Methods

A total of 72 individuals of F. religiosa were studied in their natural habitats from six regions of southern parts of Iran (Fig. 1). Twelve plants were sampled randomly from each population. Sampling locations and their geographic coordinates are shown in Table 1. The interval between samples was 300–500 m, whereas the pairwise distance between main regions was 300–600 km. The sampled stands were chosen to provide a maximum representation of the ecological conditions of the area.

Fig. 1.
Fig. 1.

Geographic location of selected sites of Ficus religiosa populations.

Citation: HortScience horts 53, 7; 10.21273/HORTSCI13058-18

Table 1.

Locations of studied Ficus religiosa genotypes.

Table 1.

The morphological study was conducted in Spring and Summer of 2016. Eight morphological traits were (flake thickness, fruit diameter, leaf length, leaf width, peduncle length, petiole length, tail-like tips, and tree length) evaluated in natural ecosystems. Morphological data were analyzed by SAS program for analysis of variance (ANOVA). Mean of values were compared using ANOVA and Duncan’s multiple range test. The simple correlation coefficient was calculated to indicate the relationships between the studied traits, and PCA was performed using the SPSS software. Morphological characteristics were measured to evaluate the Euclidean distance between all pairs of individuals using the Signed module of NTSYS-pc software version 2.01. These distance coefficients were applied for constructing a dendrogram using the unweighted pair group method with arithmetic averages using the sequential, hierarchical, agglomerative, and nested clustering algorithm. Also, scatter plot of the first two meaningful principal components was created by PAST statistics software.

Results and Discussion

According to Table 2, the highest tree, leaf, and petiole lengths, as well as leaf width, were observed in Kish and Qeshm genotypes, and also Chabahar genotype had the lowest petiole length (Fig. 2).

Table 2.

Morphological traits of Ficus religiosa genotypes in different regions.

Table 2.
Fig. 2.
Fig. 2.

Pictures of (A) leaves, (B) fruits, (C) petiole, and tail-like tips of Ficus religiosa in this study.

Citation: HortScience horts 53, 7; 10.21273/HORTSCI13058-18

Results of simple correlation analysis (Table 3) showed the existence of significant positive and negative correlations among some important parameters. The highest correlation was observed between leaf, tree, and petiole length.

Table 3.

The correlation between all morphological traits.

Table 3.

Populations were clustered in four groups (Fig. 3). The Kish and Qeshm genotypes were closely related with each other and differentiated from the Chabahar genotype. The highest distance was observed between the Kish and Chabahar genotypes (Fig. 3).

Fig. 3.
Fig. 3.

The cluster analysis of six genotypes of Ficus religiosa L.

Citation: HortScience horts 53, 7; 10.21273/HORTSCI13058-18

According to Table 4, PCA showed that the first two factor components explained 84.51% of the variation.

Table 4.

Principal component analysis of morphological traits.

Table 4.

The first factor component had the positive relationship with leaf, tree, and petiole lengths and the second one had a negative effect with flake thickness, leaf length, peduncle, petiole, and tree lengths (Table 5).

Table 5.

Components weight of morphological traits.

Table 5.

These results have a high paramount to the success of a breeding program that mainly depends on the availability of a broad genetic base. Also, the maintaining of genetic diversity is one of the most important objectives in preserving endangered and threatened plants (Akbari et al., 2018; Ebrahimi et al., 2012a, 2012b; Farajpour et al., 2011; Hesami and Daneshvar, 2016a, 2016b; Khadivi-Khub et al., 2012). The knowledge of genetic diversity among populations gives some essential details in the formulation of suitable management strategies for preserving (Francisco-Ortega et al., 2000; Milligan et al., 1994). First, it should be prohibited to keep efficient population sizes because the population size is a critical restoration consideration in endangered plants (Allendorf, 1986). Cruse-Sanders et al. (2005) recommended that preserving a proportion of the individuals in populations is of high paramount to secure the evolutionary potential and reproductive fitness of the species. Second, the construction of an in situ preservation area is a perfect way to secure wild F. religiosa genetic resources. It will result in the efficient preservation of their genetic resources and the evolution of the resources under natural conditions. Third, it is necessary to provide a long-term schedule to preserve existing natural populations to protect as much genetic diversity as possible. Fourth, ex situ preservation that mainly focused on seed harvest from various sources should be conducted to capture most of the genetic diversity existed among populations. As an important conventional medicinal plant, promoting domestication and cultivation of this wild resource is very essential both to satisfy market demand and secure the wild resource. Successful cultivation may decline the harvest of the wild genetic diversity of F. religiosa and contribute to the conservation of this important medical plant.

Conclusions

Iran has the national and international heritage of some valuable medicinal plants such as F. religiosa and it is necessary to schedule a long-term plan to identify and understand the growth habitat of this valuable plant. Our results indicated that the Qeshm and Kish genotypes of F. religiosa had the highest tree, leaf, and petiole lengths, as well as leaf width. Also, these two genotypes had a close relationship with each other in comparison with other genotypes. The simple correlation analysis indicated that the leaf, tree, and petiole lengths had the highest positive correlation with each other. Overall, it seems that the Kish and Qeshm genotypes had a high similarity to each other and they had a significant difference with the Chabahar genotype. The feasible details about the diversity of morphological features within and among various subspecies of F. religiosa may be applied in the delimitation of subspecies and also it can be used in breeding programs and conservation of this valuable plant.

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Contributor Notes

Corresponding author. E-mail: rahmati@ramin.ac.ir.

  • View in gallery

    Geographic location of selected sites of Ficus religiosa populations.

  • View in gallery

    Pictures of (A) leaves, (B) fruits, (C) petiole, and tail-like tips of Ficus religiosa in this study.

  • View in gallery

    The cluster analysis of six genotypes of Ficus religiosa L.

  • Akbari, M., Farajpour, M., Aalifar, M. & Sadat Hosseini, M. 2018 Gamma irradiation affects the total phenol, anthocyanin and antioxidant properties in three different Persian pistachio nuts Nat. Prod. Res. 32 322 326

    • Search Google Scholar
    • Export Citation
  • Allendorf, F.W. 1986 Genetic drift and the loss of alleles versus heterozygosity Zoo Biol. 5 181 190

  • Andi, S., Nazeri, V., Zamani, Z. & Hadian, J. 2011 Morphological diversity of wild Origanum vulgare (Lamiaceae) in Iran Iran. J. Bot. 17 211 221

  • Ballabh, B., Chaurasia, O., Ahmed, Z. & Singh, S.B. 2008 Traditional medicinal plants of cold desert Ladakh-used against kidney and urinary disorders J. Ethnopharmacol. 118 331 339

    • Search Google Scholar
    • Export Citation
  • Bhangale, J.O., Acharya, N.S. & Acharya, S.R. 2016 Protective effect of Ficus religiosa (L.) against 3-nitropropionic acid induced Huntington disease Orient. Pharm. Expt. Med. 16 165 174

    • Search Google Scholar
    • Export Citation
  • Cagno, V., Civra, A., Kumar, R., Pradhan, S., Donalisio, M., Sinha, B.N., Ghosh, M. & Lembo, D. 2015 Ficus religiosa L. bark extracts inhibit human rhinovirus and respiratory syncytial virus infection in vitro J. Ethnopharmacol. 176 252 257

    • Search Google Scholar
    • Export Citation
  • Chalak, L., Chehade, A. & Kadri, A. 2007 Morphological characterization of cultivated almonds in Lebanon Fruits 62 177 186

  • Cruse-Sanders, J.M., Hamrick, J. & Ahumada, J.A. 2005 Consequences of harvesting for genetic diversity in American ginseng (Panax quinquefolius L.): A simulation study Biodivers. Conserv. 14 493 504

    • Search Google Scholar
    • Export Citation
  • Dwivedi, P., Narvi, S.S. & Tewari, R.P. 2014 Phytofabrication characterization and comparative analysis of Ag nanoparticles by diverse biochemicals from Elaeocarpus ganitrus Roxb., Terminalia arjuna Roxb., Pseudotsuga menzietii, Prosopis spicigera, Ficus religiosa, Ocimum sanctum, Curcuma longa Ind. Crops Prod. 54 22 31

    • Search Google Scholar
    • Export Citation
  • Ebrahimi, M., Farajpour, M., Hadavand, H., Bahmani, K. & Khodaiyan, F. 2012a Essential oil variation among five Achillea millefolium ssp. elbursensis collected from different ecological regions of Iran Ann. Biol. Res. 3 3248 3253

    • Search Google Scholar
    • Export Citation
  • Ebrahimi, M., Farajpour, M. & Rahimmalek, M. 2012b Inter-and intra-specific genetic diversity of Iranian yarrow species Achillea santolina and Achillea tenuifolia based on ISSR and RAPD markers Genet. Mol. Res. 11 2855 2861

    • Search Google Scholar
    • Export Citation
  • Farajpour, M., Ebrahimi, M., Amiri, R., Noori, S., Sanjari, S. & Golzari, R. 2011 Study of genetic variation in yarrow using inter-simple sequence repeat (ISSR) and random amplified polymorphic DNA (RAPD) markers Afr. J. Biotechnol. 10 11137 11141

    • Search Google Scholar
    • Export Citation
  • Ferrer-Gallego, P.P., Boisset, F. & Upadhyay, G.K. 2016 Lectotypification of the name of the sacred tree Ficus religiosa (Moraceae) Taxon 65 158 162

  • Francisco-Ortega, J., Santos-Guerra, A., Kim, S.-C. & Crawford, D.J. 2000 Plant genetic diversity in the Canary Islands: A conservation perspective Amer. J. Bot. 87 909 919

    • Search Google Scholar
    • Export Citation
  • Ghosh, M., Civra, A., Rittà, M., Cagno, V., Mavuduru, S.G., Awasthi, P., Lembo, D. & Donalisio, M. 2016 Ficus religiosa L. bark extracts inhibit infection by herpes simplex virus type 2 in vitro Arch. Virol. 161 3509 3514

    • Search Google Scholar
    • Export Citation
  • Hesami, M. & Daneshvar, M.H. 2016a Development of a regeneration protocol through indirect organogenesis in Chenopodium quinoa Wild Indo-Amer. J. Agr. Vet. Sci. 4 25 32

    • Search Google Scholar
    • Export Citation
  • Hesami, M. & Daneshvar, M.H. 2016b Regeneration from callus which is produced from cotyledon of Antirrhinum majus Indo-Amer. J. Agr. Vet. Sci. 4 20 24

    • Search Google Scholar
    • Export Citation
  • Hesami, M. & Daneshvar, M.H. 2018 In vitro adventitious shoot regeneration through direct and indirect organogenesis from seedling-derived hypocotyl segments of Ficus religiosa L.: An important medicinal plant HortScience 53 55 61

    • Search Google Scholar
    • Export Citation
  • Hesami, M., Daneshvar, M.H. & Lotfi, A. 2017a In vitro shoot proliferation through cotyledonary node and shoot tip explants of Ficus religiosa L Plant Tissue Cult. Biotechnol. 27 85 88

    • Search Google Scholar
    • Export Citation
  • Hesami, M., Daneshvar, M.H. & Yoosefzadeh-Najafabadi, M. 2018a An efficient in vitro shoot regeneration through direct organogenesis from seedling-derived petiole and leaf segments and acclimatization of Ficus religiosa J. For. Res., doi: 10.1007/s11676-11018-10647-11670.

    • Search Google Scholar
    • Export Citation
  • Hesami, M., Daneshvar, M.H. & Yoosefzadeh-Najafabadi, M. 2018b Establishment of a protocol for in vitro seed germination and callus formation of Ficus religiosa L., an important medicinal plant Jundishapur J. Nat. Pharm. Prod. 13 e62682

    • Search Google Scholar
    • Export Citation
  • Hesami, M., Daneshvar, M.H., Yoosefzadeh-Najafabadi, M. & Alizadeh, M. 2017b Effect of plant growth regulators on indirect shoot organogenesis of Ficus religiosa through seedling derived petiole segments J. Gen. Eng. Biotech. 16 175 180

    • Search Google Scholar
    • Export Citation
  • Hesami, M., Naderi, R., Yoosefzadeh-Najafabadi, M. & Rahmati, M. 2017c Data-driven modeling in plant tissue culture J. Appl. Environ. Biol. Sci. 7 37 44

  • Keshari, A.K., Kumar, G., Kushwaha, P.S., Bhardwaj, M., Kumar, P., Rawat, A., Kumar, D., Prakash, A., Ghosh, B. & Saha, S. 2016 Isolated flavonoids from Ficus racemosa stem bark possess antidiabetic, hypolipidemic and protective effects in albino Wistar rats J. Ethnopharmacol. 181 252 262

    • Search Google Scholar
    • Export Citation
  • Khadivi-Khub, A., Zamani, Z. & Fatahi, M.R. 2012 Multivariate analysis of Prunus subgen. Cerasus germplasm in Iran using morphological variables Genet. Resources Crop Evol. 59 909 926

    • Search Google Scholar
    • Export Citation
  • Kirana, H., Agrawal, S. & Srinivasan, B. 2009 Aqueous extract of Ficus religiosa Linn. reduces oxidative stress in experimentally induced type 2 diabetic rats Indian J. Expt. Biol. 47 822 826

    • Search Google Scholar
    • Export Citation
  • Mallurwar, V. & Pathak, A. 2008 Studies on immunomodulatory activity of Ficus religiosa Indian J. Pharm. Educ. Res. 42 341 343

  • Milligan, B.G., Leebens-Mack, J. & Strand, A. 1994 Conservation genetics: Beyond the maintenance of marker diversity Mol. Ecol. 3 423 435

  • Pandit, R., Phadke, A. & Jagtap, A. 2010 Antidiabetic effect of Ficus religiosa extract in streptozotocin-induced diabetic rats J. Ethnopharmacol. 128 462 466

    • Search Google Scholar
    • Export Citation
  • Patil, M.S., Patil, C., Patil, S. & Jadhav, R. 2011 Anticonvulsant activity of aqueous root extract of Ficus religiosa J. Ethnopharmacol. 133 92 96

  • Pawar, P.L. & Nabar, B.M. 2010 Effect of plant extracts formulated in different ointment bases on MDR strains Indian J. Pharm. Sci. 72 397 401

  • Salmi, M.S. & Hesami, M. 2016 Time of collection, cutting ages, auxin types and concentrations influence rooting Ficus religiosa L. stem cuttings J. Appl. Environ. Biol. Sci. 6 124 132

    • Search Google Scholar
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  • Sankar, R., Maheswari, R., Karthik, S., Shivashangari, K.S. & Ravikumar, V. 2014 Anticancer activity of Ficus religiosa engineered copper oxide nanoparticles Mater. Sci. Eng. C Mater. Biol. Appl. 44 234 239

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