INTERNATIONAL JOURNAL OF INFORMATION AND COMPUTING SCIENCE ISSN NO: 0972-1347

1 INTENDED JOURNAL CATEGORIES: Disease Notes, Phytopathology and Plant

2 protection, Plant diseases

3

4 Title:

5 First report of falcata parasitizing Thespesia populnea

6

7 Author:

8 Gaurav Mudgal*1, Gajendra Bahadur Singh2

9

10 Author Affiliation and address:

11 Department of Biotechnology, University Institute of Biotechnology, Chandigarh University,

12 Gharuan, Mohali, Punjab-140413. .

13 14 E-mail addresses: [email protected], [email protected]

15 Telephone No.: +91-9557519824

16 17 18 Abstract

19 20 This is the first incidence of Thespesia populnea as host parasitized by .

21 The incidence was recorded at Hyderabad city in the Andhra Pradesh state of India. The

22 hemiparasitic exhibited epicortical-roots type hasutoria, unusually hanging spread

23 of its foliage but absence of any floral resemblance to its new host. Associated bioresource

24 and conservation aspects have also been briefed.

25

26 Keywords: Hemiparasite, haustoria, , Malvaceae, Epicortical Root

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27 Main Text 28 29 Dendrophthoe falcata (L.f) Ettingsh is a hemiparasitic plant belonging to the mistletoe

30 family, Loranthaceae. India’s rich plant advocates an exclusive host range

31 numbering 345 susceptible to infection from this mistletoe which is a significant

32 number as it contributes to a comparatively recent global record for 401 hosts (Shaw III

33 1993). Two of varieties namely, var. falcata (Honey Suckled Mistletoe) and var. Coccinea

34 (Red Honey Suckled Mistletoe) are predominant in India and are characterized by white and

35 red flowers respectively (Kawale 2016). The epiphyte bears grey barks, thick coriaceous

36 leaves variable in shape with stout flowers. In the Indian subcontinent, infection from D.

37 falcata is commonly broad in extent especially on mango (Mangifera indica), neem

38 (), teak (Tectona grandis) and sugar apple () etc. As per

39 the available literature, this is the first report that adds Indian Tulip Tree, Thespesia populnea

40 (L.) Sol. ex Corrêa, a member of the Malvaceae (mallow family) to the list of susceptible

41 hosts parasitized by D. falcata var. falcata (Honey Suckled Mistletoe). The parasitic

42 relationship was recorded from the road sides of Miyapur locality in Hyderabad district of

43 Andhra Pradesh (India) wherein other common hosts viz., mango, guava, sugar apple, sapota,

44 neem, night jasmine, yellow cassia and also exhibit infestation from D. falcata.

45 The hemiparasite on this newly discovered host was identified as D. falcata var. falcata (Fig

46 1a-1d) on the basis of established floral characteristics (Kawale 2016) shown in the Table 1.

47 Due to an apparent lack of unique characters, high hybridization potential (both intraspecific

48 and inter-specific) it was formerly difficult to correctly circumscribe D. falcata as it

49 resembles very closely with other species in its . D. falcata thus itself was previously

50 known as Loranthus longiflorous and regarded as an extremely complex, polymorphic and

51 widespread taxon distributed from India to Australia. In floral and leaf characters it resembles

52 D. pentandra and D. praelonga in Malaysia, and D. vitellina in northern Australia. D.

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53 gjellerupii in New Guinea can only be distinguished from D. falcata based on measurements

54 of corolla which again is highly variable. Morphological distinctiveness among different

55 entities has been observed and exists in conformity with their geographic discontinuity. The

56 Indian entity though in particular is more or less glabrous and glaucous, with fine

57 longitudinal lenticels on the stems (Nickrent 2008). Ariel parasitic plants belonging to the

58 mistletoe families Loranthaceae and Viscaceae are characterized by the formation of

59 haustorial structures at the host parasite interface through which the mistletoe derives water,

60 and dissolved metabolites and nutrients from the host (Kuijt 1969; Wilson and Calvin 2006).

61 Haustorial structures have been classified into four distinct types namely, Epicortical-Roots

62 (ERs), solitary unions, wood roses, and bark strands (Calvin and Wilson 1998). We observed

63 D. falcata haustoria of the type ER that run along the Indian Tulip tree branches (Fig 1b and

64 1d). D. falcata foliage on this new host exhibited unusually hanging spread of long, leafy,

65 unbranched stems extending towards the ground which was also observed in case with a

66 pomegranate host but usually was not observed in other common hosts viz. sugar apple,

67 guava, night jasmine in the same locality. The mistletoe leaf morphology on this newly found

68 host was also distinct compared to that on other hosts and exhibits great variations in shape

69 and thickness. It is known that the mimic their corresponding hosts in terms of

70 floral structures probably to safeguard hosts’ individual fitness by signalling the birds to

71 expel mistletoe seeds on other uninfected hosts (Atsatt 1979). Our observations for D. falcata

72 on Indian Tulip Tree host do not fall in agreement with this view due to the absence of any

73 floral resemblance among them. We support that host-parasite resemblance may be

74 coincidental and thus the so called mimicry if apparent could be attributed to the influence by

75 a firm epigenetic hormonal control from the concurrent host plant (Atsatt 1979; Mudgal and

76 Mudgal 2011). Variations in shape of leaves of D. falcata from the same host indicate that the

77 epigenetic control may be insufficient for an explanation to mimicry. In addition, influence

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78 from other factors such as ageing in the host, the parasite and/or environmental constraints

79 should be considered. Increase in size and/or infective spread of mistletoe upon ageing would

80 require corresponding increment in sustainable photosynthetic apparatus. In order to seek

81 this, enhanced water and nutrient uptake would be facilitated by an increment in the

82 transpiration-efficient leaf surface area.

83 The new host Thespesia populnea evidenced here is valuable as of the most important forest

84 trees to Pacific Islands. For craftsmen, its dark wood proves as a source to make beautiful

85 bowls, tools, small canoes, and figures. Ropes can be twisted from the bark. It also provides

86 protection against wind, salt sprays, and hot sun (Friday and Okano 2006). Mother Nature has

87 attributed T. populnea with valuable medicinal properties such as antifertility, antibacterial,

88 anti-inflammatory, antioxidant, purgative and hepatoprotective activity (Vasudevan et al.

89 2007). Besides these, T. populnea bark extracts experimented on exteroceptive and

90 interoceptive behavioural models has indicated remarkable memory-enhancing activity and

91 has been suggested for use on Alzheimer patients (Vasudevan and Parle 2006; Vasudevan

92 and Parle 2007). The oil from its seeds constitutes 20% of semi-drying dark red coloured oil

93 and bears potentials for its use in industrial oils (Subbaram 1954). Many pharmacological

94 implications from T. populnea also match with those evidenced for D. falcata as shown in the

95 Table 2. Besdies, this mistletoe is known to offer comparatively different medicinal on

96 different hosts and ethno-medicinal assets (Mallavadhani et al. 2006). On T. populnea, the

97 newly found host, it is for sure that D. falcata would provide novel bioactive compounds with

98 value added pharmaceutical implications.

99 T. populnea is susceptible to several diseases viz. fungal leaf spot caused by Lophodermium

100 sp., fungal root and stem rot caused by Phellinus noxius, fungal heart rot caused Fomes

101 pachyphloeus; pests of cotton, viz. cotton stainer bug (Dysdercus sp.), the cotton boll weevil

102 (Anthonomus grandis), Pyroderces simplex, Indian dusky cotton bug (Oxycarenus laetus) etc.

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103 (Friday and Okano 2006). To add, overharvesting, increased urbanization and mass

104 eradication and including possibly as of now the reported incidence of by D.

105 falcata that prevalence of T. populnea has become nearing vulnerability.

106 In light of the above, the present article appeals both for pharmacological investigations on D.

107 falcata occurring on T. populnea, and also for strict conservation of the host. Albeit,

108 mistletoes are considered an important component of biodiversity (Watson 2001), and praised

109 due to their miraculous ethno-medicinal assets, but being backed by easy seed dispersal by

110 frugivorous birds, widespread and ever increasing host range particularly of D. falcata

111 continues to pose serious losses to economically valuable fruit trees, flowering plants and

112 those with medicinal properties whether growing in forests, orchards or gardens in India

113 (Sridhar and Rao 1978). Such an increment in the host range should also alarm

114 phytopathologists to devise effective control and management strategies particularly for this

115 hemiparasite (Mudgal et al. 2011). It is upsetting to note that amidst D. falcata and other

116 mistletoes pose heavy losses to forest trees, commercial fruit crops and ornamental plants, no

117 sincere efforts have been initiated and the possible biotechnological solutions are either

118 limited or have not yet seen the light of the day.

119

120 Acknowledgement

121 The author is thankful to the Department of Biotechnology, UIBT, Chandigarh University for

122 critical review of the manuscript. The views presented here do not reflect in part and/or as a

123 whole an outcome of any mandated research activity(s) of the institution(s) to which the

124 author is and/or had been affiliated to but in actual are products of author’s independent

125 observations.

126

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127 References

128 Anarthe SJ, Bhalke, R. D., Jadhav, R. B., & Surana, S. J. (2008) Antidiabetic activity of

129 stems of hemiparasite Dendrophthoe falcata Linn. parasitic growing on Mangifera indica.

130 Dhaka University Journal of Pharmaceutical Sciences 7:177-180

131 doi:http://dx.doi.org/10.3329/dujps.v7i2.2175

132 Atsatt PR (1979) On the evolution of leaf resemblance between mistletoes and their hosts. In:

133 Proceedings of the 2nd symposium on parasitic weeds. NC State University, Raleigh., pp 59–

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135 Belhekar SN, Chaudhari PD, Saryawanshi JS, Mali KK, Pandhare RB (2013) Antidiabetic

136 and antihyperlipidemic effects of Thespesia populnea fruit pulp extracts on alloxan-induced

137 diabetic rats Indian Journal of Pharmaceutical Sciences 75:217-221 doi:10.4103/0250-

138 474X.115491

139 Boonsri S, Karalai C, Ponglimanont C, Chantrapromma S, Kanjana-opas A (2008) Cytotoxic

140 and Antibacterial Sesquiterpenes from Thespesia populnea Journal of Natural Products

141 71:1173-1177 doi:10.1021/np800055q

142 Calvin CL, Wilson CA (1998) The haustorial system in African Loranthaceae. In: Polhill R

143 WD (ed) The mistletoes of . Kew, UK: Royal Botanic Gardens, pp 17-36

144 Friday JB, Okano D (2006) Thespesia populnea (Milo), Traditional Tree Initiative— Species

145 Profiles for Pacific Island Agroforestry. http://agroforestry.org/images/pdfs/Thespesia-

146 milo.pdf. Accessed 25 April 2016

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147 Hasan MS, Ahmed MI, Mondal S, Uddin SJ, Masud MM, Sadhu SK, Ishibashi M (2006)

148 Antioxidant, antinociceptive activity and general toxicity study of Dendrophthoe falcata and

149 isolation of quercitrin as the major component Opem 6:355-360

150 Ilavarasan R, Vasudevan M, Anbazhagan S, Venkataraman S (2003) Antioxidant activity of

151 Thespesia populnea bark extracts against carbon tetrachloride-induced liver injury in rats

152 Journal of Ethnopharmacology 87:227-230 doi:10.1016/S0378-8741(03)00147-8

153 Kawale P (2016) Honey Suckle Mistletoe. http://www.flowersofindia.net.

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156 Kuijt J (1969) The biology of parasitic flowering plants. University of California Press,

157 Berkeley The biology of parasitic flowering plants University of California Press, Berkeley

158 Mallavadhani UV, Narasimhan K, Sudhakar AVS, Mahapatra A, Li W, Breemen RBv (2006)

159 Three new pentacyclic triterpenes and some flavonoids from the fruits of an Indian

160 Ayurvedic plant Dendrophthoe falcata and their estrogen receptor binding activity Chemical

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162 Manandhar NP (2002) Plants and people of Nepal. Timber Press,

163 Mitra S, Mukherjee SK (2009) Some abortifacient plants used by the tribal people of West

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165 Mudgal G, Mudgal B (2011) Evidence for unusual choice of host and haustoria by

166 Dendrophthoe falcata (L.f) Ettingsh, a leafy mistletoe Archives of Phytopathology and Plant

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168 Mudgal G, Mudgal B, Gururani MA, Jelli V (2011) Pseudaulacaspis cockerelli (Cooley)

169 hyperparasitizing Dendrophthoe falcata (L.f) Ettingsh Archives of Phytopathology and Plant

170 Protection 44:282-286 doi:10.1080/03235408.2010.505368

171 Nagappa A, Cheriyan B (2001) Wound healing activity of the aqueous extract of Thespesia

172 populnea fruit Fitoterapia 72:503-506 doi:10.1016/S0367-326X(01)00275-1

173 Nickrent DL (2008) Loranthaceae of New Guinea: A Hypermedia Guide to the Loranthaceae

174 of Papua New Guinea, Irian Jaya and Surrounding. Nickrent, D.L., .

175 http://parasiticplants.siu.edu/NewGuineaLoranths/Index.html. Accessed 25 April 2016

176 Pattanayak S, Mazumder P (2009) Effect of Dendrophthoe falcata (Lf) Ettingsh on female

177 reproductive system in Wistar rats: a focus on antifertility efficacy Contraception 80:314-320

178 doi:10.1016/j.contraception.2009.03.001

179 Pattanayak S, Priyashree S (2008) Hepatoprotective activity of the leaf extracts from

180 Dendrophthoe falcata (Lf) Ettingsh against carbon tetrachloride–induced toxicity in wistar

181 albino rats Phcog Mag 4:218-222

182 Pattanayak S, Sunita P (2008) Wound healing, anti-microbial and antioxidant potential of

183 Dendrophthoe falcata (Lf) Ettingsh Journal of Ethnopharmacology 120:241-247

184 doi:10.1016/j.jep.2008.08.019

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185 Shaw III CG, & Phanichapol, D. (1993) First report of Dendrophthoe falcata on Pinus kesiya

186 Plant Disease 77:847

187 Shirwaikar A, Kumar AV, Krishnanand B, Sreenivasan K (1995) Chemical investigation and

188 antihepatotoxic activity of Thespesia populnea International Journal of Pharmacognosy

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190 Sridhar T, Rao V (1978) Dendrophthoe falcata, a menace to fruit orchards [India] Current

191 Science 38:908

192 Subbaram M Analysis and characterisation of the oil from the seeds of Thespesia Populnea.

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194 304. doi:10.1007/BF03048704

195 Vasudevan M, Gunnam K, Parle M (2007) Antinociceptive and anti-inflammatory effects of

196 Thespesia populnea bark extract Journal of Ethnopharmacology 109:264-270

197 doi:10.1016/j.jep.2006.07.025

198 Vasudevan M, Parle M (2006) Pharmacological actions of Thespesia populnea relevant to

199 Alzheimer's disease Phytomedicine 13:677-687 doi:10.1016/j.phymed.2006.01.007

200 Vasudevan M, Parle M (2007) Memory-Enhancing Activity of Thespesia populnea in Rats

201 Pharmaceutical Biology 45:267-273 doi:10.1080/13880200701214631

202 Watson DM (2001) Mistletoe-a keystone resource in forests and woodlands worldwide

203 Annual Review of Ecology and Systematics 32:219-249

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204 Wilson CA, Calvin CL (2006) An origin of aerial branch parasitism in the mistletoe family,

205 Loranthaceae American Journal of Botany 93:787-796 doi:10.3732/ajb.93.5.787

206

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207 FIGURE 1

a b

c d 208

209

210 Fig. 1 a D. falcata (=DF) infecting T. populnea branch (TPB) b Close view of haustorium at

211 the host parasite interface (HPI) emphasized with brace c Close view of a D. falcata flower

212 with scale d Epicortical root (ERs) of haustoria extending along the T. populnea branch with

213 intermittent attachment points (AP). DFL= D. falcata leaves; TPF= T. populnea fruits;

214 TPL=T. populnea leaves. Arrows have been used to distinguish structures.

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Parts identified Features Visual agreement Leaves alternate or sub-opposite  pinnately veined  axillary  sometimes at leafless node  racemes or spikes  Bract One subtending each flower  shorter than calyx  Flowers bisexual  5-merous  actinomorphic or zygomorphic  Calyx ovoid or urceolate  Flower bud tubular  Corolla White colored  sympetalous  tube inflated  tip clavate  lobes reflexed or twisted with  age Stamens inserted at base of corolla lobes  filaments short, flattened  Anthers 4-loculed  Pollen grain trilobate in polar view  Ovary 1-loculed  placentation basal  Style filiform , 5- angled  Stigma capitate  Berry ovoid 

Table 1.List of the floral features used while identification of the mistletoe as provided in the compendium, Flowers of India (Kawale 2016).

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Matching medicinal Referenced Evidences for Referenced Evidences for properties D. falcata T. populnea

Antifertility (Mitra and Mukherjee (2009); Vasudevan and Parle (2006)

Pattanayak and Mazumder (2009))

Antimicrobial Pattanayak and Sunita (2008) Boonsri et al. (2008)

Anti-inflammatory and Hasan et al. (2006) Vasudevan et al. (2007)

Antinociceptive

Antioxidant Pattanayak and Sunita (2008) Ilavarasan et al. (2003)

Hepatoprotective Pattanayak and Priyashree (2008) Shirwaikar et al. (1995)

Wound-healing (Manandhar (2002); Pattanayak and Nagappa and Cheriyan (2001)

Sunita (2008))

Antidiabetic Anarthe (2008) Belhekar et al. (2013)

Table 2. A tabulated match of ethno-medicinal properties of both the host and the parasite and the correspondingly cited references.

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