Chemistry and Biology of Industrial Crop Tagetes Species: a Review

See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/283038100

Chemistry and biology of industrial crop Tagetes Species: A review

Article in Journal of Essential Oil Research · October 2015 DOI: 10.1080/10412905.2015.1076740

CITATIONS READS 24 1,864

7 authors, including:

Alok Krishna Madhuri Gupta Central Institute of Medicinal and Aromatic Plants Central Institute of Medicinal and Aromatic Plants

13 PUBLICATIONS 145 CITATIONS 10 PUBLICATIONS 66 CITATIONS

SEE PROFILE SEE PROFILE

Some of the authors of this publication are also working on these related projects:

Skill development and deployment of rural population through employing S&T intervention of economically viable aromatic and medicinal crops for income generation and job creation in rural sector of Bundelkhand and adjoining areas. View project

All content following this page was uploaded by Madhuri Gupta on 23 June 2016.

The user has requested enhancement of the downloaded file. Journal of Essential Oil Research

ISSN: 1041-2905 (Print) 2163-8152 (Online) Journal homepage: http://www.tandfonline.com/loi/tjeo20

Chemistry and biology of industrial crop Tagetes Species: a review

Priyambada Singh, Alok Krishna, Vinod Kumar, Swadhinta Krishna, Kuldip Singh, Madhuri Gupta & Sohan Singh

To cite this article: Priyambada Singh, Alok Krishna, Vinod Kumar, Swadhinta Krishna, Kuldip Singh, Madhuri Gupta & Sohan Singh (2015): Chemistry and biology of industrial crop Tagetes Species: a review, Journal of Essential Oil Research, DOI: 10.1080/10412905.2015.1076740

To link to this article: http://dx.doi.org/10.1080/10412905.2015.1076740

Published online: 05 Oct 2015.

Submit your article to this journal

Article views: 8

View related articles

View Crossmark data

Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=tjeo20

Download by: [CIMAP Central Institute of Medicinal & Aromatic Plants] Date: 13 October 2015, At: 22:22 Journal of Essential Oil Research, 2015 http://dx.doi.org/10.1080/10412905.2015.1076740

Chemistry and biology of industrial crop Tagetes Species: a review

Priyambada Singha, Alok Krishnaa, Vinod Kumara, Swadhinta Krishnab, Kuldip Singha, Madhuri Guptaa and Sohan Singha

aCSIR-Central Institute of Medicinal and Aromatic Crops, Lucknow, India; bDr. Ram Manohar Lohia Avadh University, Faizabad, Lucknow, India

ABSTRACT ARTICLE HISTORY In this review, different research works related to Taxonomy, cytogenetics, tissue culture, Received 20 February 2014 Biotechnology, Agronomy, phytochemistry, pharmacology and biological activity as well as its Accepted 21 July 2015 commercial uses of Tagetes species including all the biological and chemical activities mainly KEYWORDS T. minuta, T. patula and T. erecta have been compiled. The review also highlights the chemical Tagetes; taxonomy; structures and commercial uses of essential oil and its components of its unique biological activity cytogenetics; being used as agrochemical, food and colorants and nutritional supplement and cosmetic industry. phytochemistry; commercial This review work also focus on commercial cultivation of T. minuta for its oil and T. patula and T. erecta find floriculture use and also raw material for commercial production of several kinds of compounds.

Introduction are: T. minuta, also known as southern cone marigold Tagetes is a genus of annual and perennial, mostly herba- and black mint (Stinking roger), T. petula (French mari- ceous plants in the sunflower family (Asteraceae or Com- gold) and T. erecta (African marigold) the Mexican mar- positae). It was described as a genus by Linnaeus in 1753 it igold, also called Aztec marigold, (Figures 1-4). Of these, is also known for its horticultural and essential oil-yielding T. minuta is mainly cultivated for its essential oil, where species that are cultivated or occur naturally in many parts as T. petula and T. erecta find floricultural use, as well as of world. Commonly called marigolds, there are thirty-six provide raw material for commercial production of several species of Tagetes, most widely known being T. erecta, kinds of useful compounds. This review aims at compila- T. petula and T. minuta (1). The genus Tagetes is native tion of information on various aspects of these species. The to the area extending from south-western United State of Tagetes plants have typical features of family Asteraceae. America (USA) to Argentina, with maximum variation The leaves are alternate and pinnate lobed. The primary occurring in Mexico. Several-to-many marigolds species inflorescence is a racemose head or capitulum. Each head are now naturalized in Europe, Africa, Asia and Australia is subtended by involucres of green bracts which are pro- (2). In Mexico several marigold species are traditional tective in function. The capitula open in acropetal fashion. medicines, used as analgesics, antiseptics, carminative, In bisexual flowers five epipetalous stamens are present. diuretic, worm expellants, stimulants and vermin repel- The filaments are free but anthers are usually connate in lents. In southern USA, marigold material is used in food a tube around the style. The anthers are ditheous, introrse seasoning and for insect repellence (1). Marigold is used and open by longitudinal slits. The gynaecium is bi-capil- for ceremonial purposes, as offering to Gods in India and lary and syncarpous. The ovary is inferior and unilocular in ceremonies for the dead in Mexico and Guatemala (2). with single anatropous ovule. The style is bifid. The fruit In recent years, marigolds are proving to be commercial is achene with pappus and seeds are non endospermic (3). resources of essential oils and compounds of unique bio- The distinguishing features of the three commercially Downloaded by [CIMAP Central Institute of Medicinal & Aromatic Plants] at 22:22 13 October 2015 logical activities for use as agrochemicals, foods and color- important Tagetes species namely T. minuta, T. erecta and ants and nutritional supplements and in cosmetic industry T. petula are briefly summarized in the Table 1. (3). Cytogenetics, genetics and genetic variability: The chro- Plant description and taxonomy: The three species of mosome numbers of T. erecta and T. petula have been Tagetes which have been domesticated independently in determined as 2n = 24 and 48, respectively (4, 5). Triploid several countries and are now widely used world over inter specific hybrids of the two species which have double

CONTACT Alok Krishna [email protected]

inter-varietal crosses in T.erecta (7). Drought tolerant clones could be generated as somaclones from the callus cultures of T. minuta (8). The genetic variability of nine parents of marigold and evaluated that highest range of variation was reported in no of leaves/plant followed by leaf biomass exhibited highest of variation. High heritabil- ity with high genetic advance was found with number of flower /plant, number of petals/flower yield /plant (9). Tissue culture and biotechnology: Media explants and culture conditions have been worked out to regenerate shoots and then root them in T. erecta (10, 11). It was found that whereas callus as well as suspension cultures could be raised from leaf explants, only the callus cultures regenerated shoots (12). Immature unpollinated disc florets could also be regenerated into shoots (10). In another study with T. erecta, the suspension cultures were observed to syn- thesize pyrethrins (13). Random amplified polymorphic DNA (RAPD) analysis was carried out to assess the extent of genetic diversity in six accessions each of Tagetes minuta Figure 1. (a) Tagetes minuta single plant. and patula collected from different geographical parts of India. A set of twenty decem random primers was used to amplify the genomic DNA from different accessions through Polymerase chain reaction (PCR). Among these primers, fifteen responded positively to yield amplification products as discreet bands in both the cases. In case of T. minuta, only 7% polymorphism was observed and all the six accessions showed 95–100% similarity. While in case of T. patula, more than ninety bands were produced out of which 70% were polymorphic. Biological activity of their essential oils was also studied against bacterial and fungal strains (14). In vitro anti-tick properties of the essential oil of T. minuta L. (Asteraceae) on Hyalomma have been observed, we obtained the essential oil of T. minuta by hydro-distillation of a combination of fresh flowers, leaves and soft stems, and analyzed these by using gas chromatography (GC) and gas chromatography-linked mass spectrometry (GC-MS). The oil had a high percentage of monoterpenes and the major compounds identified were cis-ocimene (28.5%),β -ocimene (16.83%) and 3-methyl-2 (2-methyl -2-butenyl) – furan Figure 2. (b) Tagetes patula single plant. (11.94%). Hyaloma rufipes adults displayed a significant (p

Downloaded by [CIMAP Central Institute of Medicinal & Aromatic Plants] at 22:22 13 October 2015 < 0.05) repellent response to the essential oil of T. minuta. The oil also significantly (p < 0.05) delayed molting of 60% flowers and dwarf habit having thirty-six chromosomes of H. rufipes (15). have been produced. Towner and Bolze have suggested that T. petula is amphidiploid hybrid of T. erecta and Use of Tagetes for soil health improvement: A number T. tenuifolia or a related species. Amphidiploid of the of studies have been carried out in which T. minuta and T. erecta and T. petula hybrid have been also produced. T. erecta were inter-cultured with other crops susceptible The genetic resources of T. erecta and T. petula have been to different species of nematodes. It has been generally investigated earlier in India. Heterotic combinations have found that intercropping with Tagetes species helped in been identified in T petula (5). Many strains of T. erecta the control of different species of soil nematodes (16). and T. petula were found to be nematode resistant (6). Aluminum culture concentration of 0, 1, and 4 mg/L Transgressive segregation was recovered from certain increased root length and weight. In T. erecta studies also Journal of Essential Oil Research 3

North Indian Plains. CSIR-Central Institute of Medic- inal & Aromatic Plants, Lucknow, India has developed and registered a new T. minuta variety called ‘Vanphool’ which is being cultivated by the growers of North Indian Plains. Variety produces maximum oil yield (48 kg/ha) at full bloom stage. In the second year, the open pollinated bulk progeny was again evaluated for oil yielding, potential where it produced 61 Kg/ha oil yield at full bloom stage. The variety oil contained seven major constituents with dihydrotagetone as the predominant monoterpenoid and moderate (Z)-tagetone and (Z)- β-Ocimene. The crop can be grown during October to March through seeds or seedling transplanting with lesser input in North Indian Plains (117). Suitable agro climates: Successful cultivation of marigolds Figure 3. (c) Tagetes erecta single plant. has been reported from most parts of the country (20). Marigold can be cultivated in almost all the states of India. It is planted between March and September in different geographical locations. First a nursery is raised and the seedlings are transplanted, often layered cuttings can also be used to plant marigolds. The yields ofT. erecta and T. petula flowers reported from different areas vary considerable from a few tons to 25 tons/ha (21). T. minuta variety Vanphool is being cultivated commercially between October and March in North Indian Plains (117). Physiology and biosynthesis: Gibberellic acid, its antag- onists and micro-nutrient sprays have been found to enhance flower yield (22-25). Two flavones patuletin from T. patula and quercetagetin from T. erecta have been found aldose reductase inhibitor activity (26). T. erecta flower containing seven compounds also exhibited electrophysiological activity in Helicoverpa armigera (27). Figure 4. (d) Tagetes minuta crop; Mature crop (Left) Ratoon Crop Root extract of T. erecta also reported as light activated (Right). metabolite bioactivity (28). Seventy percent essential oil yield was found to be increased by introduction of Pseu- domonas fluoresce or its co-inoculation in the plants (29). revealed that it has no effect on stem and leaf weight (17). The infection-specific phosphatase (ISPase) is detected in Allelopathic effects of Tagetes species on the growth of the mycorrhizal root of T. patula. It is demonstrative that other plant species have been demonstrated (18). The con- ISPase activity can be used as indicator for growth of the centration of sodium in shoot tissues of all the Tagetes mycorrizal plants (30). species increased and that of potassium and magnesium decreased with increase in soil ESP. The calcium concen- Fertilizer application: Deficiency of N and P in the soil Downloaded by [CIMAP Central Institute of Medicinal & Aromatic Plants] at 22:22 13 October 2015 tration in shoot tissues of Tagetes species did not change has been shown to decrease herbage and flower yield (31). with sodic levels, except that it was lowest in T. minuta at The effect of mineral fertilization o the composition of the the soil ESP 40 (19). essential oil from the leaves and flowers of Tagetes patula from Bulgaria during the flowering period was investi- Cultivation and variety of Tagetes: A number of stud- gated by GC/MS, The N, P, and K doses recommended ies have been carried out on marigold in many parts of for high flower yields are 60 to 120 kg N/ha, 60 to 90 kg India to standardize the time of planting, fertilizer appli- P/ha and 30 kg/ha K (32–35). cation schedule, physiological treatments for improvement of flowering and disease control, especially on Germination and plant spacing: Tagetes minuta L. is an T. erecta and T. petula (34–36). Considering the application important medicinal plant, known as South African Mar- potential of T. minuta oil. It was desirable to introduced igold used for extraction of essential oil, which is known new high-yielding variety and practice in cultivation in for its potent antimicrobial and pesticidal activities, first 4 P. Singh et al.

Table 1. Taxonomical features of the Tagetes species.

Characters Tagetes minuta T. patula (French African marigold) T. erecta (African marigold) (A) Key to species Head many, in corymbs, few flow- Head, 3–4 cm across; involucres 1–2cm Head, 6–8cm across; involucres 1.5–2.5 ered , involucres cylindrical long; bracts 5–7 cm long; bract 8–3 (B) Morphological features Herb 30 cm to more than 1m height, 60cm to more than 1m height, strongly Erect, 25–75 cm height, sparingly branched, strongly scented scented, much branched strongly aromatic, branches angular, ribbed Leaf Pinnate, leaflet linear-lanceolate, Opposite, upper one sometimes Opposite, decussate or upper one alter- sharply serrate, 2–4.5cm long, con- alternate, leaflets lanceolate oblong, nate, pinnate; leaflet lanceolate- oblong, spicuously gland-dotted, glabrous sharply serrate with awed teeth, acute, remotely dentate, glandular near glandular along the margins below the the base of teeth, petiole up to 5cm long serrations Head Numerous, in crowded cymes at the Solitary or cymose, 2–3cm across, Heterogamous, radiate, solitary terminal end of branches, 0.3–0.5cm across. peduncle, peduncles 3–15cm, slightly on 4–5cm long peduncle, 6–8cm across; Involucres Ca 10x3mm swollen below the head, involucres peduncle swollen below the head. Invo- campanulate, 1–2cm with 5–7, acute lucres 2–2.5cm, glabrous bract 1seriate, linear teeth, glands dotted glandular Flower Florets only little exceeding the Ligules of marginal flower yellow or Floret orange yellow, ray floret female, involucres, ray florets yellow, 3–4; orange colored with brownish red 1.5–2.5 cm long; disc floret bisexual tubular, ligules 2-toothed, disc florets yellow, marking, 1–1.5 cm long, emarginated 5 toothed; stamen 5, included; anther linear, tubular-5 toothed flat, shortly 2-fid, stigma hairy Seed (Achenes) Achenes black, sub compressed Achenes angled, somewhat com- Achenes blackish, 8–10 mm long, angular, 6–7 mm long, densely shiny pressed, hairy; pappus of 1–2 long scabrous on angles, pappus scales united, hair, pappus scales 5, unequal, with awed scales and 2–3, shorter, blunt 4–4.5 mm long, unequal. one much larger than the others ones Chemotaxonomy Sabinene, myrcene, (z)- B-ocimene, Limonene, (z)- B- ocimene, linalool, (z)- Limonene, (z)- B-ocimene, terpenolene, dihydrotagetone, (E) and (z)-tage- myroxide, piperitenone, piperiteone (z)- tagetone and (E)- tagetone, (E)- tone, linalool and (E)- (z)- tagetones. oxide, B-caryophyllene, terpenolene, tagetone and (z)- tagetone, piperitone, carvacrol and E-(anethole). piperitenone and caryophyllene oxide. Note: a = Source (Flora of India, 1995) Vol. 13: 326–330.

and final count of seed germination and associated ger- commercial importance due to several of its biological mination parameters of Tagetes minuta accessions (36). activities. T. minuta oil inhibits bacterial growth (54). The A large number of spacing trials have been conducted in thiophenes and SE-ocimenene present in the oil render flower bearing T. erecta and T. petula cultivars. Spacing it insecticidal against the larvae and adults of mosquitoes of 20 × 50, 30 × 30, 40 × 30, 40 × 40 cm have been recom- (55–59). The essential oil of Tagetes L. also exhibits poten- mended. (37–41). However, effect of planting dates and tial as info chemical agents on insects’ behavior, this study spacing of Tagetes minuta in mid October planting with highlights the chemical variability of essential oils as a source closer spacing (45 cm × 45 cm) resulted in maximum oil of variation of anti-insect properties (60). The T. minuta oil yield (38, 42). Cultivation of marigold for loose flower has compounds that mimic insect juvenile hormone activ- trade requires standardization of agro techniques, Orissa ity (61) and inhibits growth of many species of insects and state has quite favorable agro climatic condition and there efficacious against cattle tick infestation (62, 63). T. minuta is tremendous potential for taking up commercial culti- essential oil containing 119 hydrocarbon compounds and vation of this flower crop (43). richer in monoterpenes (47.90%) are found to be mosquitoes repellant (Anopheles arabiensis) in southern part of western Diseases and pests: Few pests have been reported to cause Kenya. It is reported as new practical and economic way damage in Tagetes crops. However, several diseases do and readily available and applicable malaria vector control cause losses, especially viral diseases (44). Mosaic disease tool for incorporation into integrated vector management has been reported in T. erecta (45, 46). Root rot caused strategies (64). T. minuta has also been reported to possess by Rhizoctonia bataticola has been reported in T. erecta hypotensive, spasomolytic, anti-inflammatory, antidepres- (47). Flower bud rot caused by Alternaria dianthi has been Downloaded by [CIMAP Central Institute of Medicinal & Aromatic Plants] at 22:22 13 October 2015 sant, antimicrobial activities and antibacterial activities noted on T. erecta (48). Another species A. tagetica causes (65–67). The T. minuta, T. petula and T. erecta leaf oils are leaf spots in T. erecta (49). Phyllody disease also appears highly active against a wide spectrum of fungi (68). Essential to be common in T. erecta (50, 51). The essential oil of oil of T. petula is used as acricide and antioxidant activity T. minuta is efficacious against cattle tick infestation (52). against engorged adult female of Rhipicephalus sanguineus Number of disease like damping off caused by a ceratoba- (69, 70). The essential oil extracted from capitula of T. patula. sidium species and begomovirus found in T. erecta and T. It is evaluated for its antifungal properties, thirty compounds patula, respectively (53). were identified representing 89.1% of the total detected. The Biological activities: Marigold essential oils: The entire main components were piperitone (24.74%), piperitetone shoot of T. minuta and leaves of T. erecta and T. petula (22.93%), terpinolene (7.8%) dihydrotagetone (4.91%), upon hydro distillation yield essential oils, which have been cis-tagetone (4.62%) and allo-ocimne (3.66%).The oil exerted chemically characterized. T. minuta oil is of considerable a good antifungal activity against two phytopathogenic fungi, Journal of Essential Oil Research 5

CH 2 OPP CH 2 OH OH

Geraniol GPP Linalool

CH2

CH 2 OPP CH2 Neryl pyrosphate Myrcene

O O CH2 Dihydrotagetone (Z)- Tagetenone ( Z ) -β-ocimene

(Z)-Tagetone

O CH2 O O (E)-Tagetenone (Z)-β-Ocimene epoxide (E)-β-ocimene (Z) - myroxide ) (E)-Tagetone

Scheme I. Biosynthetic pathways for the formation of acyclic monoterpenes. Downloaded by [CIMAP Central Institute of Medicinal & Aromatic Plants] at 22:22 13 October 2015

Botrytis cinerea and Penicillium digitatum, providing com- of T. minuta has been observed against gram positive and plete growth inhibition at 10 µL/mL and 1.25 µL/mL, respec- gram negative microorganisms (54). tively (71, 72). T. minuta contain Ocimene and Ocimenone rich exhibited mycelia inhibition at 5000 ppm, 3000 ppm, Thiophenes: The T. erecta root thiophenes exhibit nemat- and 2000 ppm, respectively (73). Essential oil of T. minuta icidal, antiviral, antifungal and antibacterial activities has been found 95% efficacious against four species of ticks (75–77). Marigolds are therefore sometimes co-culti- at concentration of 20%. It also suggests that the oil could vated with vegetable crops that are highly susceptible to be used as an environmentally friendly acaricide (74). The rhizosphere borne diseases, including nematodal attack. antimicrobial activity of flavonoids containing in the leaves Thiophenes, steroidal and terpenoidal type of constituents 6 P. Singh et al.

+ CH 2 -OPP CH2

Neryle pyrophosphate

+ +

(B) (A) α - β- Phellandrens

Sabinene Limonene γ - Terpinene

O OH β-pinene α-pinene + OH

Carvone Thymol Carvacrol OH

+ OH O Terpinolene (A) O Thymol hydroquinon Piperitenone O O Piperitenone oxide Piperitone

Scheme II. Biosynthetic pathways for the formation of cyclic monoterpene.

found in different parts of T. patula (roots, leaves and processes for producing marigold powder, there are three flower). Their structures were characterized by different different drying processes, namely freeze drying (FD), hot spectroscopic. Among the thiophenes triterpens and ster- air drying (HA) and combined far-infrared radiation with oids are two thiophenes, one triterpene and one steroid hot air convection (FIR-HA), on the color, carotenoids

Downloaded by [CIMAP Central Institute of Medicinal & Aromatic Plants] at 22:22 13 October 2015 first time isolated from the genes T. petula (78). (lycopene, beta-carotene and lutein) and phenolic compou nds of marigold flowers were evaluated. FIR-HA should Capitula carotenoids: Lutein (chemical structure dia- be considered as a suitable drying method for marigold grammed below) di-esters extracted from petals of with respect to preserving its color, antioxidant properties T. erecta are used as nutritional supplements in poultry and bioactive compounds and provided useful informa- feed (79, 80). Marigold (Tagetes erecta L.) flower has long tion for industrial production of marigold powder (81). been used as a food colorant and ingredient in human These have been shown to possess antimutagenic activity food and animal feed. Drying is one of the most important (54, 82). Journal of Essential Oil Research 7

2 R 5 ' 3 ' ' 1 13 9 ' ' 9 1 13 3 5 1 R

β-carotene R1 = R2 = H Lutein R1 =R2 = OH ( Tagetes )

(d) Flavanoids: Flavanoids from the leaves of T. minuta flower (capitulum) and/or whole plant oils examined are known to possess antimicrobial activity (54). from twelve locations. In five types (Z)-β-ocimene was pre-eminent and in three the preponderant constituent Chemical profiles of the domesticated marigolds: The was dihydrotagetone : oil compositions of T. minuta, T. erecta and T. petula of (a) Oils produced in Brazil, France and Hungary, different geographical origins have been studied in consid- (Z)- -ocimene > (Z)- and (E)-tagetenone > (Z)- erable detail. The available information is briefly reviewed β and (E)-tagetone and dihydrotagetone; below. T. minuta essential oil: The essential oil ofT. minuta Table 2. Basic skeleton species foe the formation of monoter is commercially produced in Argentina, Australia, penes of Tagetes essential oils. Brazil, France, Spain, Venezuela, Iran and other coun- Myrcene, (Z)- and (E)-ocimenenes; (Z)- and tries. The oils having origin in many countries have been (E)- tagetenones; (Z)- and (E) tagetenones; (Z)-β - ocimene epoxide analyzed, The main components of the whole shoot oils + were identified as (Z)-β-ocimene, dihydro-tagetone, (Z)- and (E)-tagetones and (Z)- and (E)-tagetenones (also known as ocimenones). Differences have been observed in profiles of leaf, flower and whole plant oils of T. minuta Geranial and geranyl acetate produced in Brazil, North America, France, Hungary, Tur- CH2 key, Rwanda, Zambia, Bhutan and India. Five types can be recognized from the observations on leaf oils of these origins (83, 84, 86–99). (a) Oils from six locations in Rwanda, dihydrotagetone > (Z)-tagetone > (Z)-tagetenone > (E)- Limonene; α -terpinolene; carvone tagetone > (Z)-β-ocimene > (E)-tagetenone; (b) Hyderabad (Andhra Pradesh, India) oil, dihydrotagetone > (Z)-β-ocimene and (Z)-tagetone; (c) Mukoni (Rwanda) oil, (E)-tagetenone > (Z)- tagetone > dihydrotagetone, (E)-tagetone and (Z)-β-ocimene; + (d) Lucknow (Uttar Pradesh, India) oil, (Z)-tagetone γ terpinolene; terpinolene; sabenene Downloaded by [CIMAP Central Institute of Medicinal & Aromatic Plants] at 22:22 13 October 2015 terpinolene-4ol; α abd β phellandrenes pip- > (Z)-tagetenone > dihydrotagetone, (E)- eritone; piperitenone; piperitenone oxide tagetone and (Z)-β-ocimene > (E)- tagetone; and thymol; carvacrol. (e) French oil, (Z)-tagetenone > (Z)-β-ocimene > + (Z)-tagetone > dihydrotagetone. It will be seen that leaf oil of T. minuta investigated were generally rich in the distal compound(s) α and β pinenes of the dihydrotagetone biosynthetic pathway which proceeds in the direction of (Z)-β-ocimene (E)- and (Z)-tagetenone (E)-and (Z)-tagetone dihydrotagetone (100–103). Eight types could be recognized among the 8 P. Singh et al.

Table 3. Basic structural species of compounds for the formation of sesquiterpenes of Tagetes oils.

β-caryophyllene; α -humulene

β-endesmol

+ + +

β-and γ -elemenes

+ γ- cadinene germcrene D α-cadinol

+ +

(E)-nerolidol +

(b) North American oil, (Z)-β-ocimene > (Z)- and (h) Lucknow oil, dihydrotagetone > (Z)- and (E)- (E)-tagetenone > dihydrotagetone > (Z)- and tagetone > (Z)- and (E)-tagetenone and (E)-tagetone; (Z)-β-ocimene. (c) Rwandan oils, (Z)-β-ocimene > (Z)- and (E)- The above observed variability in the flower oils of tagetone > (Z)- and (E)-tagetenones > T. minuta produced at geographically diverse locations is dihydrotagetone; indicative of wide genetic differences in the expression of (d) Kashmir and Himachal Pradesh (India) oils, (Z)- the different steps of the dihydro tagetone biosynthetic -ocimene > (Z)- and (E)- tagetenone > dihydro- pathway. On the whole it appears that in T. minuta (Z)- -

Downloaded by [CIMAP Central Institute of Medicinal & Aromatic Plants] at 22:22 13 October 2015 β β tagetone > (Z)- and (E)-tagetone; ocimene, (Z)- and (E)-tagetenones, (Z)- and (E)-tagetones (e) Bhutanese oil, (Z)-β-ocimene > dihydrotagetone and dihydro tagetone are programmed to accumulate in > (Z)- and (E)-tagetone and tagetenone; the oil in about 2:1:1:1 proportion. The allelic differences (f) Zambia and Andhra Pradesh oils, dihydrotage- in the genes concerned with the oil synthesis pathway dis- tone > (Z)-β-ocimene > (Z)- and (E)-tagetone > tributed in different populations are responsible for the (Z)- and (E)- tagetenone; observed deviations from the average of oil types. Leaves (g) Turkey oil, dihydrotagetone > (Z)-β-ocimene > and inflorescences of five species of Tagetes have been (Z)- and (E)- tagetenone> (Z)- and (E)-tagetone; found with major components like T. caracasana were and trans-ocienone (64.3%) and cis-tagetone (13.7%) and for Journal of Essential Oil Research 9

T. credo piperitone (35.9%) and terpinolene (22.2%). In the effect of mineral fertilization on composition of the oils T. filifolia trans-anethole (87.5%) and estragole (10.7%) from the leaves and flowers of four variants of T. petula of were observed in high amount. For T. patula two samples Bulgarian origin. Limonene, (Z)-β-ocimene, (Z, Z)- alloo- were analyzed, leaves (TPL) and inflorescences (TPI), TPL cimene, (Z)-β-ocimene epoxide, (Z)- and (E)-tagetones, oil showed terpinolene (20.9%) and piperitenone (14.0%) (Z)- and (E)- tagetenones, piperitone and piperitenone as main components and the TPI oil composed beta- were found as the major constituents of the leaves and caryophyllene (23.7%), terpinolene (15.6%) and cis-beta- flowers of these variants. Tagetes have been found with ocimene (15.5%) (104). major components like T. caracasana were trans-ocienone (64.3%) and cis-tagetone (13.7%) and for T. credo piperi- Tagetes erecta essential oil: This marigold is weakly tone (35.9%) and terpinolene (22.2%). In T. filifolia trans- aromatic and the leaves and flowers contain essential anethole (87.5%) and estragole (10.7%) were observed in oil in low concentrations. The composition of the oil of high amount. For T. patula two samples were analyzed, T. erecta has been a subject of several investigations (86, leaves (TPL) and inflorescences (TPI), TPL oil showed 105, 106). Very early investigation of the oil of the flow- terpinolene (20.9%) and piperitenone (14.0%) as main ering plants reported limonene, ocimene, linalyl acetate, components and the TPI oil composed beta-caryophyl- linalool and n-nonyl aldehyde as the major constituents. lene (23.7%), terpinolene (15.6%) and cis-beta-ocimene Later investigations (86, 87) on the oil reported the iso- (15.5%) (113, 116). lation of limonene, β-ocimene, β-phellandrene, linalool and linalyl acetate. In addition, 1,8-cineole, tagetone, α- Biosynthesis of the compounds of Tagetes oils: Most of and β-pinenes and menthol were also reported as minor the chemical compounds encountered in the essential oils constituents. The oil ofT. erecta from Hungary was found of T. minuta, T. erecta and T. petula belong to the terpenoid to contain limonene, β-ocimene, piperitone and β-car- class-mainly monoterpenes. A few compounds belonging yophyllene as the major constituents (106, 107). Subse- to sesquiterpene group are also found. These compounds quently the oil of T. erecta from Brazil was reported to are not the direct products of the secondary metabolism. contain terpinolene, (E)- β-ocimene, limonene, piperitone, The relative concentration of these secondary metabolites thymol, carvacrol, indole, β-caryophyllene and nerolidol depends upon the presence and availability of the various in amounts more than 2%. T. erecta leaves are subjected to precursors and also on the presence and activity of the steam distillation and simultaneous distillation method. various enzymes in the plants. Further the sites of accu- Which related 0.094% and 1.005% recovery and contain- mulation of the metabolites in the plant facilitate their ing twenty-nine type of in steam distillation and fifty are isolation and enable one to characterize them. kind of compound in simultaneous distillation oil (108). Terpenoids are compounds derived from mevalonic acid which itself is biosynthesized in the plant from three T. petula essential oil: The aerial parts of the plant (capit- molecules of acetyl coenzyme A. Earlier works of Ruzika, ula, leaves and shoots) are weakly aromatic and contain Folkers, Lyren and others have enabled the understanding essential oil, which has fruity top note similar to that of of the biosynthetic path ways of various terpenoid com- green apples (3).The oils of different parts of T. petula have pounds. This work was reviewed in several treatises (87). been the subject of several investigations (35, 85, 86, 106, The transformation of mevalonic acid to terpenoid 109–115). Earlier studies on the oil of the flowers, leaves molecule involves several reactions like phosphorylation, and stems of T. petula from India reported limonene, hydrolysis, condensation, oxidation, reduction, cyclization, ocimene, linalool, linalyl acetate and tagetone as the main etc. These reactions are catalyzed by enzymes present in the constituents of the oils (109, 110). Later, methyl heptenol plants which are referred to as oxidases, reductases, cyclases, was also reported as a major constituent of the oil obtained etc. The first step in the transformation of mevalonic Downloaded by [CIMAP Central Institute of Medicinal & Aromatic Plants] at 22:22 13 October 2015 from full flowering plants of T. petula (110, 115). The oil of acid to terpenoid is its conversion to isopentenyl pyroph- the flowering plants from Hungary was reported to contain osphate. Phosphorylation of mevalonic acid with adenyl limonene, β-ocimene, tagetone, (Z)- and (E)-ocimenones triphosphate (ATP) gives pyrophosphate (2) which again (tagetenones) and β-caryophyllene as the major constitu- undergoes phosphorylation to give the intermediate ents (87). Recently Garg et al.1999 investigated the oil of phospho-3-pyrophospho-5-mevolonate (3) which was capitula and found that the oil contained limonene, (Z)-β- not isolated. Subsequent steps involved are decarboxyl- ocimene, terpinolene, (E)-tagetone, (Z)-tagetone, carvone, ation, hydrolysis and dehydration leading to the forma- carvacrol and piperitone as the major constituents. They tion of isopentanyl pyrophosphate (4). Isomerization of found leaf oil to contain limonene, (ZZ)-allo ocimene, isopentenyl pyrophosphate gives dimethyl allyl pyroph- (Z)-β-ocimene epoxide, (E)-tagetone, (Z)-tagetenone, pip- osphate (5). Condensation of isopentenyl pyrophospahte eritone and piperitenone. Stojanova et al. (2000) studied (IPP) with dimethyl allyl pyrophosphate (DMAPP) gives 10 P. Singh et al.

the monoterpenoid compound geranyl pyrophosphate many of the sesquiterpenes found in the Tagetes oils are (GPP) (6). GPP is the main precursor for the synthesis of found as minor constituents. The minor sesquiterpenes various monoterpenoid and sesquiterpenoids. found in these oils are β- and γ-elemenes, germacrene -D, -cadinene, -humulene, -cadinol and -eudesmol. As Conversion of GPP to monoterpenes: Tagetes oils con- δ α α β there are several biosynthetic pathways for the formation tain both acyclic and cyclic monoterpenes. Acyclic mono- of sesquiterpenes, it is rather difficult to present them in terpenes include (Z)- β- and (E)-β-ocimene, (Z)- and one scheme. The basic skeletal species for the formation (E)-tagetone and (Z)- and (E)-tagetenone (also known of both monoterpenes and sesquiterpenes are shown in by the name ocimenones). The cyclic monoterpenes of Tables 2 and 3. Tagetes oils are limonene, piperitone, piperitenone, etc. The above review gives the background for the present In addition, there are a few bicyclic monoterpenes like investigation which aimed at the collection and character- pinenes and sabinene in these oils. The main constituents ization of yield and quality of flowers and/or essential oils of T. minuta oils are (Z)-β-ocimene, dihydrotagetone, (Z)- yielded by T. erecta, T. petula and T. minuta. and (E)-tagetone and (Z)- and (E)-tagetenones. The cyclic monoterpenes limonene, sabinene and piperitenone are the minor constituents of T. minuta oil. The main con- Conclusion stituents of T. minuta oil are (Z)-β-ocimene, limonene, Tagetes genus is known for its horticulture and essen- terpinolene, piperitenone and the sesquiterpene β-car- tial oil- and dye-yielding species. All these three spe- yophyllene. The cyclic monoterpenoids, piperitone and cies, minuta, patula and erecta have been domesticated piperitenone are dominant in T. erecta oil. independently in several countries including India. The acyclic monoterpenes (Scheme-I) are formed by Tagetes genus is considered for its chemical and biolog- chemical modification of either GPP or neryl pyrophos- ical activity and also used as raw material for commer- phate (NPP) which is obtained by isomerization of GPP. cial exploitation of various compounds. Tagetes species The cyclic monoterpenes are formed from NPP or less are known for its potent antimicrobial and pesticidal probably from the isomeric linalyl pyrophosphate (LPP). activity and also as a source of nutritional supplements The biosynthesis of acyclic monoterpenes proceeds as additive of chicken feed to give color to egg yolks in through the simple reactions such as hydrolysis, dehy- poultry industry. dration, oxidation and reduction which are catalyzed by specific enzymes. The proposed pathways for the formation of the acyclic monoterpenes, such as myrcene, (Z)-β- Disclosure statement ocimene, (Z)- -ocimene epoxide, (Z)- and (E)-tagetone, β No potential conflict of interest was reported by the authors. (Z)- and (E)-tagetenone, dihydrotagetone, linalool and geranial, are shown in Scheme-II. The biosynthesis of cyclic monoterpenes involves References cyclization reaction of NPP catalyzed by the enzymes 1. R.T. Neher, The ethnobotany of Tagetes. Eco. Bot., 22 (4), cyclases. There are numerous cyclases in plants which 317–325 (1968). are capable of producing different types of compounds. 2. L. Kaplan, Historical and ethno botanical aspects of The first step in this biosynthesis is the formation of the domestication Tagetes. Eco. Bot., 14, 200 (1960). species (A). This species (A) undergoes hydride shift to 3. Annoymus, Raw Materials: Wealth of India. NISCOM, Council of Scientific and Industrial Research, New Delhi, form the species (B). The cyclic monoterpenesα - and India (1976). β-pinenes, limonene, and α-terpineol are formed from 4. A.M. Singh and S.S. Achahia, Meiotic studies in Tagetes the species (A), whereas the compounds γ-terpinene, ter- erecta and Tagetes petula from munger. J. Mendel., 10 (2–4), 127–129 (1993). Downloaded by [CIMAP Central Institute of Medicinal & Aromatic Plants] at 22:22 13 October 2015 pinolene, sabinene, α- and β-thujones, piperitenone and piperitone are formed from the species (B). The forma- 5. J. Rehana, T.N. Khoshoo and M. Pal, Origin, nature and limit of polyploidy in marigolds. Curr. Sci., 43 (24), 777– tion of these monoterpenes from NPP is summarized in 779 (1974). Scheme-II. The sequence of reactions shown in schemes 6. D. Prasad and M.M. Haque, Reaction on varieties of is common for the biosynthesis of monoterpenoid con- marigold against Root Knot nematode, Meloidogyne stituents of other essential oils. incognita. Indian J. Nematol., 12 (2), 418–419 (1982). There are numerous skeletons of sesquiterpenes pro- 7. B. Singh and V. Swaroop, Inheritance of flowering, flower duced in higher plants. The biosynthesis of sesquiterpenes weight and flower number in African marigold. Indian J. Genet. Pl. Br., 32 (2), 172–175 (1973). proceeds through the precursor farnesyl pyrophosphate 8. M.A. Mohamed, P.J. Harris and J. Henderson, In Vitro (FPP) which is formed by condensation of GPP with one selection and characterization of a drought tolerant clone molecule of IPP. With the exception of β-caryophyllene, of Tagetes minuta. Plant Sci., 159 (2), 213–222 (2000). Journal of Essential Oil Research 11

9. D. Singh and K.K. Misra, Genetic variability in 27. T.J. Bruce and A. Cork, Electrophysiological and quantitative characters of marigold Indian. J. Hortic., 65 behavioral responses of female Helicoverpa armigera to (2), 187–192 (2008). compounds identified in flowers of African marigold, 10. S.L. Kothari and N. Chandra, In vitro propagation of Tagetes erecta. J. Chem. Ecol. Jun, 27 (6), 1119–1131 African marigold. Hort. Sci., 19 (5), 703–705 (1984). (2001). 11. H.Y.M. Ram and G. Mehta, Regeneration of plantlets 28. G.L. Shi, Y.N. Wang, H.L. Wang, L.L. Zhao, S.Q. Liu, H. from cultured morphactin induced bearer capitula of Cao, T.Q. Yu and P. Lu, Effects of Tagetes erecta extracts African marigold (Tagetes erecta L.). Plant Sci. Let., 26 on glutathione S-transferase and protease activities and (2/3), 227–232 (1982). protein content in Tetranychus viennensis. Ying Yong 12. S.L. Kothari and N. Chandra, History of rhizogenesis and Sheng Tai Xue Bao, 18 (2), 400–404 (2007). shoot bud formation in cultures of Tagetes erecta. Curr. 29. L. del Rosario Cappellari, M. Valeria Santoro, Sci., 55 (7), 354–356 (1986). F. Nievas, W. Giordano and E. Banchio, Increase of 13. P. Khanna, R. Sharma and R. Khanna, Pyrethrins from in secondary metabolite content in marigold by inoculation vivo and in vitro tissue culture of Tagetes erecta L. Indian with plant growth-promoting rhizobacteria. Appl. Soil J. Exp. Biol., 13 (5), 508–509 (1975). Ecol., 70, 16–22 (2013). 14. M.P. Darokar, M.S. Khan, A.K. Shasany, A. Krishna 30. T. Ezawa and T. Yoshida, Characterization of Phosphatase and S.P.S. Khanuja, Molecular diversity analysis in in marigold roots infected with vesicular arbuscular the Germplasm collection of Tagetes species. J. Med. Mycorrhizal fungi soil science. Plant Nutr., 40 (2), 255– Aromatic Plant Sci., 22, 536–539 (2000). 264 (1994). 15. F. Nchu, R. Solomon Mangano and N. Jacobus Eloff, 31. E.H. Graven, L. Webber, G. Benians, M. Venter and J.B. In vitro anti-tick properties of the essential oil of Tagetes Gardner, Effect of soil type and nutrient status on yield minuta L. (Asteraceae) on Hyalomma rufipes (Acari: and composition of Tagetes oil Tagetes minuta. J. Essent. Ixodidae) Onderstepoort. J. Vet. Res., 79, 5 (2012). Oil Res., 3 (5), 303–307 (1991). 16. D. Prasad, D.K. Magla, S. Kumar and M.L. Saini, Marigold 32. R. Arulmozhiyan and C.M. Pappaiah, Studies on the plants for management of nematode populations in field. effect of nitrogen, phosphorus and ascorbic acid on the Curr. Nematol., 3 (1), 15–18 (1992). growth and yield of Tagetes erecta. S. Indian Hort., 37 17. T.J. Smalley, F.T. Lasseigne, H.A. Mills and G.G. (3), 169–172 (1989). Hussey, Effect of aluminum on growth and chemical 33. K. Anuradha, K. Pampapathy and N. Narayana, Effect of composition of marigolds. J. Plant Nutr., 16 (8), 1375– N and P2 O5 on the nutrient composition and uptake by 1384 (1993). marigold (Tagetes erecta L.). S. Indian Hort., 36 (1, 2), 18. K. Kaul and Y.S. Bedi, Allelopathic influence of 51–61 (1988). Tagetes species on germination and seedling growth 34. P. Ram, B. Kumar, A. Singh, M. Yaseen and S.K. Kothari, of reddish and lettuce. Indian J. Agr. Sci., 65 (8), Response of marigold (Tagetes minuta) to irrigation and 599–601 (1995). nitrogen fertilization under Himalyan foot hills of Tarai 19. A. Prasad, A. Krishna, S.N. Garg, S. Bhasney and D.V. region of Uttar Pradesh. J. Med. Aromatic Plant Sci., 21, Singh, Growth, yield and cation accumulation in Tagetes 361–366 (1999). species under sodic soils. J. Med. Aromatic Plant Sci., 25 35. A. Stojanova, T. Primova and C.H. Anastassov, Effect of (2), 408–413 (2003). mineral fertilization on the essential oil composition of 20. S.H. Mehta, H.R. Nadkarni and A.D. Rangawala, Tagetes patula L. from Bulgaria. J. Essent. Oil Res., 12, Performance of African marigold (Tagetes erecta) in 609–612 (2000). Konkan region of Maharashtra. Indian J. Agr. Sci., 65 36. B. Kumar, A.K. Gupta, A.K. Verma and A. Dubey, (11), 810–812 (1995). Comparative germinination behavior of Tagetes minuta 21. R. Batti and S.D. Chitkara, A note on comparative L. J. Trop. Med. Plants, 9, 149–151 (2008). performance of three cultivars of marigold at Hissar. 37. J.V.N. Gowda and R. Jayanti, Studies on the effect of Haryana J. Hort. Sci., 18 (3–4), 230–232 (1989). spacing and season of planting on growth and yield of 22. A.S. Parmar and S.N. Singh, Effect of plant growth marigold (Tagetes erecta L.). J. Plant Physiol., 122 (3), regulators on growth and flowering of marigold (Tagetes 235–241 (1986). erecta). S. Indian Hort., 31 (1), 53–54 (1983). 38. D.V.L. Ravindran, R.R. Rao and E.N. Reddy, Effect of 23. A. Girwani, R.S. Babu and R. Chandrasekhar, Response spacing and nitrogen levels on growth, flowering and yield of marigold (Tagetes erecta L.) to growth regulators and of African marigold (Tagetes erecta L.). S. Indian Hort., Downloaded by [CIMAP Central Institute of Medicinal & Aromatic Plants] at 22:22 13 October 2015 zinc. Indian J. Agr. Res., 60 (3), 220–222 (1990). 34 (5), 320–323 (1986). 24. B. Singh, R.P. Sood and V. Singh, Chemical composition 39. R.S. Bhati and S.D. Chitkara, Effect of pinching and of Tagetes minuta L. oil from Himanchal Pradesh (India). planting distance on the growth and yield of marigold J. Essent. Oil Res., 4, 525–526 (1992). Tagetes erecta. Res. Dev. Reporter, 4 (2), 159–164 (1987). 25. D.K. Bandhopadhyay, D.K. Das and T.K. Chattopadhayay, 40. S. Chanda and N. Roychoudhury, The effect of time of Effect of micronutrients on flower character and yield of planting and spacing on growth, flowering and yield of marigold (Tagetes erecta L.) seeds. Crop. Res., 7 (1), 13– African marigold (Tagetes erecta L.) cv. Siracole. Hort. J., 16 (1994). 4 (2), 53–56 (1991). 26. S. Li, W. Mao, X. Cao, S. Liang, Z. Ding and N. Li, 41. C.R. Mohanty, T.K. Behra and D. Samantary, Effect Inhibition of rat lens aldose reductase by quercetagetin of planting time and planting density on growth and and patuletin. Yan Ke Xue Bao Mar, 7 (1), 29–30, 33 flowering in African marigold (Tagetes erecta L.) J. (1991). Ornam. Hort., 1 (2), 55–60 (1993). 12 P. Singh et al.

42. P. Ram, B. Kumar, N.K. Patra, S.N. Garg and M.S. Negi, 57. P.N. Kaul, K. Singh, B.R. Rajeswara Rao, G.R. Tagetes minuta L. Effect of post harvest storage of herb Mallavarapu and S. Ramesh, Analyse desetherischen Ols on oil under tarai condition of Uttarakhand. Indian Perf., Tagetes minuta L. Perf. Cosmetic., 79 (3), 36–38 (1998). 45, 153–158 (2001). 58. V.S. Dharmagadda, S.N. Naik, P.K. Mittal and P. 43. D. Samantaray, C.R. Mohanty and T.K. Behera, Effect Vasudevan, Larvicidal activity of Tagetes patula essential of planting and spacing on growth and flower yield of oil against three mosquito species. Bioresour. Technol., 96 marigold (Tagetes erecta L.) cv. Afr. Yellow Indian J. (11), 1235–1240 (2005). Hortic., 56 (4), 382–385 (1999). 59. W.P. Lima, F. Neto Chiaravalloti, L. Mde Macoris, D.A. 44. B.D. Suteri, G.C. Joshi and S. Bala, Some of the Zuccari and M.R. Dibo, Establishment of the feeding ornamental and weeds as reservoirs of potato virus Y and methodology of Aedes aegypti (Diptera-Culicidae in Swiss cucumber mosaic virus in Kumaon. Indian Phytopathol., mice and evaluation of the toxicity and residual effect 32 (4), 640 (1979). of essential oil from Tagetes minuta L (Asteraceae), in 45. R.D. Joshi and L.N. Dubey, Studies on a mosaic disease of populations of Aedes aegypti. Rev. Soc. Bras. Med. Trop., marigold (Tagetes erecta L.) in Uttar Pradesh. Sci. Cult., 42 (6), 638–641 (2009). 38 (3), 147–148 (1972). 60. S.B. López, M.L. López, L.M. Aragón, M.L. 46. K.M. Usman, G. Ramkrishnan and T.K. Kandaswamy, Tereschuk, A.C. Slanis, G.E. Feresin, J.A. Zygadlo A note on the occurrence of mosaic disease on marigold. and A.A. Tapia, Composition and anti-insect activity Tagetes erecta L. Sci. Cult., 38 (11), 489 (1972). of essential oils from Tagetes L. species (Asteraceae, 47. V.C. Saxena and R. Singh, A new root knot disease of Helenieae) on Ceratitis capitata Wiedemann and marigold. Indian J. Mycol. Plant Pathol., 21 (3), 293 Triatoma infestans Klug. J. Agr. Food Chem., 25, 59 (10), (1991). 5286–5292 (2011). 48. N. Mandal and S. Chaudhuri, Flower bud rot of marigold 61. B.P. Saxena and J.B. Srivastava, Tagetes minuta oil. New (Tagetes erecta L.) caused by Alternaria dianthi in West source of juvenile hormone mimicking substances. Indian Bengal. Curr. Sci., 45 (2), 75 (1976). J. Exp. Biol., 11, 56–58 (1973). 49. J.S. Diman and J.S. Arora, Occurrence of leaf spot and 62. A.M. Broussalis, G.E. Ferraro, V.S. Martino, R. Pinzon, flower blight of marigold (Tagetes erecta L.) in Punjab. J. J.D. Coussio and J.C. Alvarej, Argentine plants as potential Res., 27 (2), 231–236 (1990). source of insecticidal compounds. J. Ethnopharmacol., 67 50. A.K. Sharma, S. Mishra, S.P. Roychaudhari and (2), 219–223 (1999). N. Parameswaran, Phyllody of marigold, a disease 63. R. Andreotti, M.V. Garcia, R.C. Cunha and J.C. Barros, associated with mycoplasma: Like organism. Int. Protective action of Tagetes minuta (Asteraceae) J. Tropical Disease., 3 (1), 45–49 (1985). essential oil in the control of Rhipicephalus microplus 51. B.R. Singh, P.N. Singh and S.K. Garg, Natural occurrence (Canestrini, 1887) (Acari: Ixodidae) in a cattle pen trial. of phyllody disease on marigold. Farm-Sci. J., 1 (1–2), Vet. Parasitol., 18, 197 (1–2), 341–345 (2013). 77–78 (1986). 64. W. Wanzala and S.B. Ogoma, Chemical composition and 52. R. Andreotti, M. Valério Garcia, R. Casquero Cunha mosquito repellency of essential oil of Tagetes minuta from and J. Cavalcante Barros, Protective action of Tagetes the southern slopes of Mount Elgon in Western Kenya. J. minuta (Asteraceae) essential oil in the control Essent. Oil Bearing Plants, 16 (2), 216–232 (2013). of Rhipicephalus microplus (Canestrini, 1887) (Acari: 65. R.N. Martin, D.A. Garcia and I.D. Martijina, J.A. Ixodidae) in a cattle pen trial. Vet. Parasitol., 18, 197 Zygadlo and Perillo Ar Ce A, Anxiogenic like effect (1–2), 341–345 (1887). of Tagetes minuta L. essential oil on T-maze and toxic 53. A. Saroj, Department of Plant Pathology, CSIR - Central immobility behavior in domestic chicks. Fundam. Clin. Institute of Medicinal and Aromatic Plants (CIMAP), Pharmacol., 12 (4), 426–432 (1998). Lucknow 226015, India; A. Kumar, Department of 66. E. Hethelyi, I. Koczka and P. Tetenyi, Phytochemical and Biotechnology, CSIR - Central Institute of Medicinal antimicrobial analysis of essential oils. Herb. Hung., 28 and Aromatic Plants (CIMAP), Lucknow 226015, India; (1–2), 99–115 (1989). and S.T. Saeed, A. Samad and M. Alam, Department of 67. F, Senatore and V.D. Feo, Chemical composition of Plant Pathology, CSIR - Central Institute of Medicinal essential oil from Tagetes mandonii Sch. Bip. (Asteraceae). and Aromatic Plants (CIMAP), Lucknow 226015, India, Flavour Frag. J., 14, 32–34 (1999). First Report of Tagetes erecta Damping Off Caused 68. N. Kishore and R.S. Dwivedi, Fungi toxicity of the essential by Ceratobasidium sp. from India. APS J., 97, 1251 of Tagetes erecta against Pythium aphanidermatum of Downloaded by [CIMAP Central Institute of Medicinal & Aromatic Plants] at 22:22 13 October 2015 (2013). damping off pathogen. Flavour Frag. J., 6 (4), 291–294 54. M.L. Tereschuk, M.V. Riera, G.R. Castro and L.R. (1991). Abdala, Antimicrobial activity of flavonoids from leaves 69. F.A. Politi, T.M. de Souza-Moreira, E.R. Rodrigues, G.M. of Tagetes minuta. J. Ethnopharmacol., 56 (3), 227–232 de Queiroz, G.M. Figueira, A.H. Januário, J.M. Berenger, (1997). C. Socolovschi, R.C. Parola and P. Pietro, Chemical 55. M.M. Green, J.M. Singer, D.J. Sutherland and C.R. characterization and acaricide potential of essential oil Hibben, Larvicidal activity of Tagetes minuta (Marigold) from aerial parts of Tagetes patula L. (Asteraceae) against towards Aedes aegypti. J. Am. Mosq. Control Assoc., engorged adult females of Rhipicephalus sanguineus 7 (2), 282–286 (1991). (Latreille, 1806). Parasitol Res., 112 (6), 2261–2268 (2013). 56. M.J. Perich, C. Wells, W. Bertsch and K.E. Tredway, 70. J.S. Negi, V.K. Bisht, A.K. Bhandari and R.C. Sundriyal, Isolation of the insecticidal components of Tagetes minuta Essential oil contents and antioxidant activity of Tagetes (Compositae) against mosquito larvae and adults. J. Am. patula L. J. Essent. Oil Bearing Plants, 16 (3), 364–367 Mosq. Control Assoc., 11 (3), 307–310 (1995). (2013). Journal of Essential Oil Research 13

71. C. Romagnoli, R. Bruni, E. Andreotti, M.K. Rai, C.B. 88. A.A. Craveiro, F.J.A. Matos, M.I.L. Machado and J.W. Vicentini and D. Mares, Chemical characterization and Alencar, Essential oil of Tagetes minuta from Brazil. Perf. antifungal activity of essential oil of capitula from wild Flav., 13 (5), 35–36 (1988). Indian Tagetes patula L. Protoplasma., 225 (1–2), 57–65 89. E. Hethelyi, B. Danos, P. Tetenyi and I. Kockza, (2005). GC/ MS analysis of essential oils of some Tagetes 72. F. Sefidkon, S. Salehyar, M. Mirza and M. Dabiri Article species. In: Progress in Essential Oil Research. Edit., first published online, The essential oil of Tagetes E.J. Brunke, pp. 131–137, Walter de Gruyter & Co., erecta L. occurring in Iran. Flavour Frag. J., 19 (6), 579 Berlin (1986). –581 (2004). 90. E. Hethelyi, B. Danos, P. Tetenyi and G. Juhasz, 73. J.A. Zygadlo and C.A. Guzman, Antifungal properties of Phytochemical studies on Tagetes species infraspect the leaf oils of Tagetes minuta L. and T. filifolia Lag. J. differences of the essential oil in T. minuta and Essent. Oil Res., 6, 617–621 (1994). T. tenuifolia. Herb. Hung., 26, 145–158 (1987). 74. M.V. Garcia, J. Matias, J.C. Barros, D.P. de Lima, 91. B. Singh, R.P. Sood and Virendra Singh, Chemical S. Lopes Rda and R. Andreotti, Chemical identification composition of Tagetes minuta L. oil from Himanchal of Tagetes minuta Linnaeus (Asteraceae) essential oil and Pradesh (India). J. Essent. Oil Res., 4, 525–526 its acaricidal effect on ticks. Rev. Bras. Parasitol. Vet., 21 (1992). (4), 405–411 (2012). 92. R.P. Adams, Identification of Essential Oil Components 75. J.J.M.R. Jacob, A. Engelberts, A.F. Croes and G.J. by Gas Chromatography/Mass Spectroscopy., Allured Wullems, Thiophenes synthesis and distribution in young Publ. Corp, Carol Stream, IL (2007). developing plants of Tagetes petula and Tagetes erecta. J. 93. J.C. Chalchat, R.P. Garry and A. Muhayimana, Essential Exp. Bot., 45 (279), 1459–1466 (1994). oil of Tagetes minuta from Rwanda and France: Chemical 76. R. Randolph Arroo, J.M.R. John Jacobs, A.H. Edward, composition according to harvesting, location, growth D.E. Koning, Mirjam de Waard, Els van de Westerlo, stage and part of plant extracted. J. Essent. Oil Res., 7, M. Peter, A.D. Galen Van, E.M. Swolfs, F. Anton Croest 375–386 (1995). and G. Wullems, Thiophene Inter conversions in Tagetes 94. S.N. Garg and V.K. Mehta, Acyclic monoterpenes from Patula Hairy Root Culture. Phytochem., 38, 1193, 1197, the essential oil of Tagetes minuta flowers. Phytochem., 1195 (1994). 48, 395–396 (1998). 77. J.M.R. John Jacobs, M. Stalman, A.F. Croes and J. 95. P.N. Kaul, K. Singh, B.R.R. Rao, G.R. Mallavarapu and S. George Wullems, Thophene bioconversions in Tagetes Ramesh, Analysis des etherischon oils Tagetes minuta L. protoplasts. Plant Sci., 104, 139–145 (1995). perfum. Kosmet., 79, 36–38 (1998). 78. H. Bano, S.W. Ahmed, I. Azhar, M.S. Ali and N. Alam, 96. L. Graven, G. Webber, Venter M. Benians and J.B. Chemical constituents of Tagetes patula L. Pak J. Pharm. Gardener, Effect of soil type and nutrient status on the Sci., 15 (2), 1–12 (2002). yield and composition of Tagetes oil (Tagetes minuta L.). 79. R. Gomez, F.M. Goni and J.M. Macarulla, Carotenoids J. Essent. Oil Res., 3, 303–307 (1991). from marigold (Tagetes erecta) petals and their esterified 97. R.K. Thappa, S.G. Agrawal, N.K. Kalia and R. Kapoor, fatty acids. Rev. Esp. Fisiol., 34 (3), 253–256 (1978). Changes in chemical composition of Tagetes minuta oil 80. W.L. Hadden, R.H. Watkins, L.W. Levy, E. Regalado, at various stages of flowering and fruiting. J. Essent. Oil D.M. Rivadeneira, R.B. Breemen and S.J. Schwatz, Res., 5, 375–379 (1993). Carotenoid composition of marigold (Tagetes erecta) 98. B.M. Lawrence, Progress in essential oils. Perf. Flav., 21 flower extract used as nutritional supplement. J. Agr. (5), 57–68 (1996). Food Chem., 47 (10), 4189–4194 (1999). 99. R.P. Bansal, J.R. Bahl, S.N. Garg, A.A. Naqvi, S. Sharma, 81. S. Siriamornpun, O. Kaisoon and N. Meeso, Changes in M. Ram and S. Kumar, Variation in quality of essential color, antioxidant activities and carotenoids (lycopene, oil distilled from vegetative and reproductive stages of beta-carotene, lutein) of marigold flower (Tagetes erecta Tagetes minuta grown in North Indian plains. J. Essent. L.) resulting from different drying processes. J. Funct. Oil Res., 11, 747–752 (1999). Foods, 4 (4), 757–766 (2012). 100. E. Héthélyi, B. Dános, P. Tétényi and I. Koezka, GC/ MS 82. E. Mejia de Gonzalez, M. Ramos-Gomez and G. Pina analysis of the essential oils of four Tagetes species and the Loarca, Ant mutagenic activity of natural xanthophylls microbial activity of Tagetes erecta L. Flavour Frag. J., 1, against alfa toxin B1 in salmonella typhimurium. 169–173 (1986). Environ Mol. Mutagen., 30 (3), 346–353 (1997). 101. B.M. Lawrence, Essential oils of the Tagetes genus. Perf. Downloaded by [CIMAP Central Institute of Medicinal & Aromatic Plants] at 22:22 13 October 2015 83. I.C. Chopra, M.C. Nigam and L.D. Kapoor, Indian Flav., 10 (5), 73–82 (1985). Tagetes oils. Soap Perfum. Cosm., 36, 686–689 (1963). 102. B.M. Lawrence, R.H. Powel, T.W. Smith and S.W. 84. K.L. Handa, M.M. Chopra and M.C. Nigam, The Kramer, Chemical composition of Tagetes oil. Perf. Flav., essential oil of Tagetes minuta L. Perfum. Essent. Oil 10 (6), 56–58 (1985). Res., 54 (6), 372–374 (1963). 103. B.M. Lawrence, Progress in essential oils. Perf. Flav., 17 85. Y.N. Gupta, K.S. Bhandari and C.S. Khanna, Chemical (5), 131–146 (1992). examination of essential oil from the leaves of Tagetes 104. K. Armas, J. Rojas, L. Rojas and A. Morales, Comparative patula. Indian Perfum., 17, 24–27 (1973). study of the chemical composition of essential oils of 86. R.K. Bansal and A.K. Singh, Chemical examination of five Tagetes species collected in Venezuela. Nat. Prod. the essential oil of Tagetes erecta L. J. Indian Chem. Soc., Commun., 7 (9), 1225–1226 (2012). 58, 422–423 (1981). 105. M.L. Sharma, M.C. Nigam and I.C. Chopra, Essential oil 87. B.M. Lawrence and R.H. Powell, Chemical composition of Tagetes erecta. Perfum. Essent. Oil Res., 52, 561–562 of Tagetes oil. Perfum Flav., 10 (6), 82 (1985). (1961). 14 P. Singh et al.

106. E. Hethelyi, B. Danos, P. Tetenyi and I. Koezka, GC / MS 113. C. Romagnoli, R. Bruni, E. Andreotti, M.K. Rai, C.B. analysis of the essential oils of four Tagetes sp. and the Vicentini and D. Mares, Chemical characterization and antimicrobial activity of Tagetes minuta. Herb. Hung., antifungal activity of essential oil of capitula from wild Indian 25 (1), 49–61 (1986). Tagetes patula L. Protoplasma., 225 (1–2), 57–65 (2005). 107. A. Krishna, M.G. Rao, S. Ramesh and S. Kumar, 114. R.D. Prasad, S. Srivastava and R.P. Singh, Gas Composition of essential oil of leaves and flowers of chromatographic-mass spectrometric (GC-MS) Tagetes erecta L. J. Essent. Oil Res., 16, 520–522 (2004). analysis of marigold (Tagetes erecta L.) flower oil India 108. J. Li, S.D. Song, R.N. Zhang, N. Liu and C.C. Li, Chemical International. J. Agr. Envir. Biotechnol., 5 (3), 215–218 components and nitrite cleaning activity of essential oil (2012). from Tagetes erecta L. Leaf. Adv. Mater. Res., 183–185, 115. A. Krishna, R. Gopal Mallavarapu and Sushil Kumar, 1168–1172, (2011). Volatile oil constituents of the capitula, leaves and shoots 109. S.N. Dhingra and D.R. Dhingra, Essential oil of Tagetes of Tagetes patula L. J. Essent. Oil Res., 14, 433–436 patula. Perfum. Essent. Oil. Res., 47, 391–394 (1956). (2002). 110. Y.N. Gupta, K.S. Bhandari and C.S. Khanna, Chemical 116. K. Armas, J. Rojas, L. Rojas and A. Morales, Comparative examination of essential oil from the leaves of Tagetes study of the chemical composition of essential oils of patula. Indian Perfum., 17, 24–27 (1973). five Tagetes species collected in Venezuela. Nat. Prod. 111. F. Bohlmann and C. Zdero, Uber dimere Terpenketone Commun., 7 (9), 1225–1226 (2012). aus Tagetus gracilus. Phytochem., 18, 341–343 (1979). 117. S. Kumar, R.P. Bansal, J.R. Bahl, M. Ram, S.P.S. Khanuja, 112. S.N. Garg, S.K. Verma and S. Kumar, Identification of the A.K. Shashny, M.P. Darokar, S.N. Garg, A.A. Naqvi volatile constituents of the capitula oil of Tagetes patula and S. Sharma, Registration of Tagetes minuta variety grown in North Indian plains. J. Essent. Oil Res., 11, Vanphool for north Indian plains. J. Med. Aromatic Plant 688–690 (1999). Sci., 21, 52–53 (1999). Downloaded by [CIMAP Central Institute of Medicinal & Aromatic Plants] at 22:22 13 October 2015

View publication stats