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CHAPTER

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Podophyllum hexandrum

Jagdish Singh, Joginder Singh, Swaran Lata

Himalayan Forest Research Institute (HFRI), Conifer Campus, Shimla, Himachal Pradesh, India

7.1 Introduction

North Western Himalayas harbors a large number of economically important plants, which includeseveral species of medicinal value. The ever-increasing demand, particularly in view of worldwide shift for the drugs of herbal origin over synthetic counterparts, has led to overexploitation of medicinal plants. Apart from healthcare, medicinal plants are mainly the alternate income generating source of underprivileged communities; therefore, strengthening this sector may beneﬁt and improve the living standard of poor people. Podophyllum hexandrum Royle belongs to family Berberidaceae, and it is a perennial herb bearing the common name Himalayan Mayapple. The genus Podophyllum is also called as Mayapple because its fruits ripen in spring. The name Podophyllum is taken from “podos” a foot and “phyllon” a leaf and refers to the resemblance of the leaves to a duck’s foot. The genus

Podophyllum is represented by three species P. hexandrum, P. peltatum, and P. sikkimensis in Himalayan zone of India. P. hexandrum Royle also known as the

Indian Podophyllum is a perennial herb, growing on the lower slopes of the Himalayas in scrub and forest from Afghanistan eastward to central China commonly distributed in Himalayan region of Asian continent and popularly known as Himalayan Mayapple, while P. peltatum, commonly distributed in Atlantic North America and popularly called as American Mayapple.

The rhizomes of P. hexandrum are known to contain several lignans. The lignans occurring in Podophyllum possess antitumor properties. Podophyllum being the most active cytotoxic herb contains 4.3% podophyllotoxin on a dry weight basis. The whole plant has also got great importance in traditional systems of medicines including Ayurveda, Unani, and Tibetan systems for curing several diseases. The rhizomes and roots of Podophyllum species have gained much importance throughout the world as being the main source or the starting material for the alkaloid podophyllotoxin and its semisynthetic compounds, the etoposide, teniposide, and etoposide phosphate since their use in treatment of speciﬁc type s of cancers. These compounds are useful in the treatment of refractory testicular carcinomas, nonlymphocytic leukemias and non-Hodgkin’s lymphomas and etoposide in the treatment of lung cancer in addition to its therapeutic value against the AIDS-associated Kaposi sarcoma. It has served as a commercial source of podophyllotoxin and related

Himalayan Medicinal Plants. https://doi.org/10.1016/B978-0-12-823151-7.00001-5

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aryltetralin lignans and several other bioactive constituents. It also has numerous applications in modern medicine by virtue of its free radical scavenging capacity. In United States Bristol Co. and in Switzerland Sandoz prepared hundreds of semisynthetic compounds. Out of these only above three are widely used as antitumor agents with minimal toxic or side effects. Destruction of plant populations due to overexploitation or natural calamities affects drug supply and the content of bioactive secondary metabolite in the plant. Therefore, immediate thrust has to be given for generating the reliable conventional protocols of mass cultivation of P. hexandrum. Moreover, wild populations may be represented by various genotypes growing under different environmental conditions which may affect drug proﬁle leading to problems in the purity of the ﬁnal product. Thus, cultivation of suitable clones would ensure a reliable supply of the material with consistent quality. Thus, there is a need to understand and conserve the genetic diversity of this important medicinal plant. At present two species of Podophyllum, viz. the American Podophyllum or Mayapple (P. peltatum) and the Himalayan Podophyllum (P. hexandrum), are the main sources of podophyllotoxin. Podophyllotoxin is an expensive starting compound for the chemical synt hesis of its derivatives. P. hexandrum is now being considered as a rare and threatened species mainly due to the large-scale removal of its underground parts that still continues at rates well over natural regeneration. Attempts have been made to conserve this plant through in vitro propagation and artiﬁcial breaking of seed dormancy.

P. hexandrum is native to the temperate region of Himalayan countries like Afghanistan, Pakistan, India, Nepal, Bhutan, and in Southwest China (Airi et al.,

1997; Gupta and Sethi, 1983; Giri and Narasu, 2000a,b; Chaudhary et al., 1998).

It is categorized as globally rare plant in IUCN red list and has endangered status in India (Chaudhary et al., 2014). It is distributed in very restricted pockets in the Himalayan zone at altitudes ranging from 2000 to 4000 m a.s.l (Bhadula et al.,

2000), mostly found in Alpine region. Extraction of the whole P. hexandrum plant

in order to harvest the roots and rhizome containing the useful drug has resulted into a decline of this species and even disappearance in some regions. The population of these plants throughout its range was observed to be very sparse, in decline, and receding toward higher elevations (Rao, 1998). It is variously considered as endangered (Bhadula et al., 2000) and critically endangered (CAMP, 1998). It has declined considerably as a result of exploitation to meet the increasing demands of the pharmaceutical industry (Bhadula et al., 2000). Export of this species from India has been prohibited, although illegal removal continues (Nadeem et al., 2000).

In recent years, the frequency of P. hexandrum in nature has declined because these plant species are collected in large quantities from wild to meet the everincreasing demand of pharmaceutical industry (Sultan et al., 2006).

P. hexandrum (Himalayan Mayapple) was known as Aindri (“a divine drug”) in ancient times. It has been reported to be used through the ages and in modern times as a cure for allergic and inﬂammatory conditions of the skin; biliary fever; burning sensation; cold; constipation; cancer of the brain, bladder, and lung; erysipelas; Hodgkin’s disease; insect bites; mental disorders; monocytoid leukemia non-Hodgkin’s lymphoma; rheumatism; septic wounds; plague; and venereal warts. However, currently the commercial source of podophyllotoxin is the rhizomes and

7.1 Introduction 87

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roots of P. hexandrum. Availability of podophyllotoxin isolated from plant has its limitations, due to scarce occurrence of the plant because of intense collection from nature and lack of organized cultivation (Gupta and Seth, 1983). Himalayan Mayapple is overexploited because the whole plant is uprooted for extraction of podophyllotoxin which is a serious issue from conservation point of view (Canel

et al., 2000). In view of overexploitation due to its medicinal importance, a conser-

vation strategy should be devised to increase its population number by propagating the plant through seed in a short period thereby compensating or reducing the harvesting pressure on rhizome. Exploitation of Podophyllum from the wild is prohibited for export from India under CITES (Convention on International Trade in Endangered Species of wild ﬂora and fauna). Only cultivated/artiﬁcially propagated plant species is allowed for export under cover of CITES export permit and Legal Procurement Certiﬁcates or certiﬁcate of cultivation from the designed authorities. P. hexandrum needs study of its variability and population under different locations

Mature plant of P . hexandrum.

Profuse rooting in P. hexandrum.

88 CHAPTER 7 Podophyllum hexandrum

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with scientiﬁc basis and its ex situ and in situ conservation. National Medicinal Plant Broad, India, has initiat ed efforts toward conservation of rare, endangered, and threatened medicinal plants throughout the country (Kaul et al., 1998).

7.2 Taxonomy

Flower of P. hexandrum.

P. hexandrum is believed to have originated in Himalayan regions. According to Bentham and Hooker’s System of Classiﬁcation, the genus Podophyllum is classiﬁed as follows:

Kingdom Plantae Subkingdom Phanerogamia Division Angiospermae Class Dicotyledons Subclass Polypetalae Order Ranunculales Family Berberidaceae Genus Podophyllum Species hexandrum Royle.

Vernacular Names:

Hindi Bakra, Chimara, Papra, Papri Himachali Ban-kakri, Kakariya Uttaranchal (Bhotia) Ghi-cupra Punjabi Bankakri Urdu Ban kakri Kashmiri Baruwangan, Nirbishi, Papra,

English Mayapple Ladakhi Ol-Mo-Se, Demo-khushu Kinnauri Ululu

Bhavanbakra

7.4 Geographical distribution and status 89

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7.3 Adulterant

The rhizomes in trade are also adulterated with the rhizome of wild growing Ainsliaea latifolia belonging to Asteraceae family (Puri and Jain, 1988).

7.4 Geographical distribution and status

It occur s in forests and on open slopes from 2400 to 4500 m (Polunin and Stainton,

1984). This species has been considered a rare and threatened species, and removal

rates exceed natural regeneration rates (Nadeem et al., 2000). Occurrence is reported in Uttarakhand (Rao, 1998), and more particularly in Kumaon (Airi et al., 1997), and Garhwal (Bhadula et al., 2000). It is also reported in Himachal Pradesh, where it is found sporadically in Rohru, Kullu, Kangra, Chamba, Nichar, and Lahaul and Spiti forest divisions (Chauhan, 1999). It is distributed in restricted pockets of the Himalayas ranging from 2000 to 4000 m (Bhadula et al., 2000). The population of these plants throughout its range was observed to be very sparse, in decline and receding toward higher elevations (Rao, 1998). It is variously considered as endangered (Bha-

dula et al., 2000) or critically endangered (CAMP, 1998). It has declined consider-

ably as a result of exploitation to meet the increasing demand of the pharmaceutical industry (Bhadula et al., 2000). Podophyllum takes years for establishment and lives long in a suitable habitat (Facciola, 1990). According to reports, about 37.3 tone s of rhizomes of P. hexandrum were uprooted during 1995e2000 in Himachal Pradesh (Ali and Sharma, 2013). P. hexandrum has been overharvested to meet the demands of pharmaceutical industries. The entire plant is harvested due to presence of podophyllotoxin in its rhizome. That is why the species has acquired the endangered status (Gupta and Sethi, 1983; Bhadula et al., 2000; Airi et al., 1997). Leaves of

P. hexandrum contain higher amounts of podophyllotoxin in comparison to P. peltatum.

Podophyllum hexandrum in Suru Valley, Ladakh.

90 CHAPTER 7 Podophyllum hexandrum

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Nag et al. (2013) reported that P. hexandrum has a wide region of distribution,

within it appears mostly in valleys with secondary vegetation. In any population, the plant shows a kind of clumped distribution pattern. Earlier, P. hexandrum was used in folk medicine by local healers in small quantities, but com mercialization of the plant for its medicinal attributes in recent years has increased demand and consequent exploitation. The size of the wild populations has been declining owing to overexploitation, habitat fragmentation, long dormancy, and low rate of natural regeneration. The population size of P. hexandrum in the Himalayas is very low (40e700 plants per location) and is declining rapidly each year. Some populations in certain pockets have virtually disappeared owing to anthropogenic activities and overexploitation (Bhadula et al., 2000). Therefore, P. hexandrum has been classiﬁed as an endangered species in India since 1987 (Nayar and Sastry, 1987).

Singh et al. (2018) reported that most of the identiﬁed habitat for P. hexandrum in

Himachal Pradesh and Ladakh (J&K) was moist and rocky moist having gentle to steep slope which shows habitat speciﬁcity of species. According to literature also the species prefers moist humid conditions and soils with rich in organic matter. Several species like Achillea millefolium, Bergenia ciliata, Dactylorhiza hatagirea,

Heracleum candicans, Salix spp., Rosa webbiana, Primula spp., Aconitum heterophyllum, Angelica glauca, etc., were commonly associated with P. hexandrum in different identiﬁed sites. Aesculus indica, Salix spp., Quercus semecarpifolia, Pinus wallichiana, Betula utilis, Abies pindrow, Juniperus spp., Rhododendron campanulatum, etc., were the prominent main tree species found in different identiﬁed sites.

They have further identiﬁed 41 different sites from Himachal Pradesh and Ladakh, UT, the details of sites are given in Table 7.1:

Table 7.1 Podophyllum hexandrum in different geographical locations of Himachal Pradesh (HP) and Ladakh.

https://t.me/med1917

Sr. No. State/UT District Forest division Source/Sites Latitude (N) Longitude (E) Altitude (m)

100

1. HP Kullu Naggar Bansherudhar 32

2. HP Lahaul and Spiti Keylong Chimrit 32

3. HP Chamba Killar Karyuni 33

4. HP Chamba Killar Hudanbhaturi 33

5. HP Chamba Killar Suralbhaturi 33

6. HP Kenner Yangapa Shelti (Yangapa) 31

7. HP Lahaul and Spiti Udaipur Trilokinath 32

8. HP Kinnaur Nichar Chotkhanda 31

9. HP Kinnaur Sangla Chitkul 31

10. HP Kullu Manali Kothi 32

11. HP Kangra Bir Palachak 32

430

030

050

080

390

060



200

190

080

12. HP Shimla Rampur Jurassi N 31

13. HP Kullu Sainj Khoruthach 31

14. HP Chamba Bhandal Thathidhar 32

450

490

15. HP Kullu Anni Jalorijot N 31

16. HP Chamba Bharmour Deol 32

17. HP Kullu Patlikul Shangchar 32

18. HP Kullu Naggar Parot 32

19. HP Kullu Naggar Kulri (Bansheru) 32

20. HP Kullu Manali Gulaba 32

21. HP Kullu Kullu Majhoni (Tirthan) 31

22. HP Kinnaur Sarahan Katgaon 31

23. HP Chamba Khajjiar Kalatop 32

24. HP Shimla Rohru Janglik 1

180

100

110

1006400

190

450

330

910

795

249

271

980

594

583

741

308077

422

206

076

180

5830077420092

976

905

320

2360077220391

210

502

654

114

640

061

052

4116

77120994 76400870 76260300 76290223 76270015 7707032 76410471 77580704 78260702 77120234 76450416

77260732 75580600

76330015 77080576 77170012 77130415 77120310 77270870 77580489 76010168 78000992

2866 2718 3064 3580 3320 2985 2951 3400 3450 3036 2760 2540 2580 2899 3140 3225 3056 3032 3079 3664 3460 2750 2356 2848

Continued

7.4 Geographical distribution and status 91

Table 7.1 Podophyllum hexandrum in different geographical locations of Himachal Pradesh (HP) and Ladakh.dcont’d

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Sr. No. State/UT District Forest division Source/Sites Latitude (N) Longitude (E) Altitude (m)

220

25. HP Shimla Rohru Maila (Diudi) 31

26. HP Chamba Bhandal Dharwal 32

27. HP Lahaul and Spiti Keylong Kangsar 32

28. HP Shimla Theog Deha 32

29. HP Lahaul and Spiti Lahaul Kardang 32

30. HP Kullu Sainj GHNP 31

31. HP Shimla Rampur Chottkanda (Panvi) 31

32. HP Kangra Bir Joardu forest 32

33. Ladakh Kargil Sankoo Prachik-2 34

34. Ladakh Kargil Sankoo Beemaputri 34

35. Ladakh Kargil Sankoo Panikher 34

36. Ladakh Kargil Sankoo Shangara 34

37. Ladakh Leh Sankoo Thangbu-1 34

38. Ladakh Leh Sankoo Thangbu-II 34

39. Ladakh Kargil Sankoo UMBA1 34

40. Ladakh Kargil Sankoo UMBA 2 34

41. Ladakh Kargil Sankoo Suru (Sangrol) 34

Source: Singh, J., Singh, J., Tewari, V.P., 2018. Screening and evaluation of superior chemotypes of Podophyllum hexandrum royle from different geographical locations of North-west Himalayas. J. Plant Chem. Ecophysiol. 3 (1), 1e7.

480

320

080

330

450

180

080

040

120

070

120

180

140

014 829 721 715 918 970 583 715 129 353 119 984 337 457 118 096 479

78010129 75560766 76580463 76450526 77010088 E77260728 77420092 77450526 75580667 75550699 75580002 750580219 75550743 75550748 75550709 75550677 75580466

2990 2810 3240 2675 3148

2582 2835 2675 3497 3231 3306

3148 3228 3235 3129 3142 3085

92 CHAPTER 7 Podophyllum hexandrum

7.5 Morphology 93

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7.5 Morphology

It is an erect, smooth, glabrous, somewhat ﬂeshy, 15e40 cm tall herb with perennial roots and rhizomes. Mostly found in aggregation, which gives the plant a shrubby look. It bears one to four reproductive and ﬁve to eight vegetative shoots that appear in AprileMay. Whereas the vegetative shoot bears a single leaf, the reproductive shoots generally bear two and sometimes three to four palmate, orbicular, and deeply lobed (three to ﬁve) leaves. A single white or pink supraaxillary ﬂower emerges at the middle of the ﬂower-bearing shoot. The cup-shaped bisexual, actinomorphic, and gamosepalous ﬂower (2e3 cm long) bears three deciduous petaloid sepals but six obovate/oblong polypetalous petals, six stamens with anthers opened as lateral slits, and a superior multilocular ovary with marginal placentation. The ovoid, pulpy, many seeded berry is borne on a pedicel is an erect, smooth, glabrous, somewhat ﬂeshy. Fruit a berry, 2.5e5 cm, oblong ovoid or oblong-ellipsoid, scarlet, or red when ripe and many seeded. Seeds small and light black embedded in the red pulp. Rhizome ﬂeshy, short, horizontally creeping with long dense ﬁbrous roots, the underground part is known as rhizomatus root. Each node has the tendency to develop into a new plant offshoot (Collet, 1921; Hooker, 1875; Airi et al., 1997). Its ﬂowering and fruiting period is MayeSeptember.

P. hexandrum in Lahaul Valley (Himachal Pradesh).

94 CHAPTER 7 Podophyllum hexandrum

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Bud initiation in P. hexandrum.

7.6 Chemical constituents

American Podophyllum contains 4%e5% podophyllum resin, whereas Indian spp. contains 7%e16%. The variation in percentage of resin is attributed to seasonal differences, different sites of growth, and age of the plant (Purohit et al., 1999).

Sharma et al. (2000a,b) demonstrated much higher podophyllotoxin content in

P. hexandrum collected from Jalori Pass (8000 ft) than in the Palampur (4000 ft) counterpart. Similarly active constituents of P. hexandrum (resin and podophyllo- toxin) and A. heterophyllum alkaloids and aconitine from both wild (alpine region) and cultivated (subalpine region) plants were analyzed. Active constituents of both the plant species were signiﬁcantly lower in cultivated plants than in wild plants. However, differences in actual amounts of each type of active constituent were small. These differences, which were consistent for all active constituents, could have resulted from moving the plants from an alpine to a subalpine environment or from growing wild rather than having been cultivated. Methanolic extracts of P. hexandrum were assessed for phytochemical components and results revealed that both the plant extracts contained glycosides, ﬂavonoids, saponins, and terpenes. Alkaloids were absent in P. hexandrum. The absences of carbohydrates were detected in P. hexandrum.

Chattopadhyay et al. (2001) reported that podophyllotoxin was produced by cell

culture of P. hexandrum under in vitro culture conditions. A maximum of 4.26 mg/L of podophyllotoxin was produced when P. hexandrum was cultivated in 3 liter stirred tank bioreactor. Woerdenbag et al. (1990) reported that cell suspension cultures, derived from roots of P. hexandrum, accumulate podophyllotoxin. Although some efforts have been done for production of podophyllotoxin by plant cell cultures using bioreactors, the quantity is not sufﬁcient to meet the demand (Saurabh et al., 2002).

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