An Approach to the Chemosystematics of the Genus Cucumis L.

Introduction

Cucurbitaceae is a family of about 120 genera and over 900 species, widely distributed in tropical and subtropical regions of Africa including Madagascar, South, Southeast and East Asia, Australia as well as Central and South America^1,2. The cucurbits are also among the most diverse plant families, cultivated and naturalised worldwide in a variety of environmental conditions. These include some of the earliest cultivated food plants in both the Old and the New World tropics and subtropics. Examples of some of the World’s most important vegetable crops are cucumber (Cucumis sativus), melon (Cucumis melo L.), West Indian Gherkin (Cucumis anguria), pumpkins and squashes (Cucurbita moschata and C. mixta), red pumpkin (Cucurbita maxima), water melon (Citrulus vulgaris), loofah (Luffa acutangula, L. cylindrica), bottle gourd (Lageneria siceraria), snake gourd (Trichosanthes cucumerina var. anguina), bitter gourd (Momordica charantia) and pepitos (Cucurbita pepo). A number of them are used since antiquity not only as food, but also in folk medicine, health-care and cosmetology.  Notable medicinal applications include their use in the treatment for diabetes, bronchial and respiratory ailments as well in the oral health care and as an abortifacient^3.4. Gourds also find use as containers and as resonators in musical instruments such as the sitar. The genus Cucumis (Cucurbitaceae) comprises of some 38 African/Indian Ocean species, 19 Asian, and six Australian/ New Guinean species. Most of the ca. 63 species of Cucumis, presently known are monoecious annuals, but dioecious mating systems and a perennial habit evolved several times within the genus⁵. Formerly, Cucumis L. was a more narrowly defined genus⁶. Based on the recent molecular-phylogenetic findings^7,8, the species of the genera Cucumella Chiov.,  Dicaelospermum C.B.Clarke,  Mukia Arn., Myrmecosicyos C.Jeffrey, and  Oreosyce Hook.f. are now transferred into a  more broadly defined Cucumis^9,10. In the context of the present nuclear and chloroplast DNA data-based recircumscribtion of Cucumis, an examination of the relevance of the chemotaxonomic significance of the marker phenolics has been attempted for the first time in this paper.

Biosystematics

In the traditional systems of taxonomy, morphological traits are commonly used for classifications. However, for delimiting those taxa that exhibit morphological/cytological similarities or whose morphological characters show reticulate relations, chemical data in conjunction with those drawn from other approaches (say, morphological, cytological, embryological, anatomical and molecular) are frequently resorted to resolve the issue and to establish phylogenetic relations at interspecific, intergeneric and family levels^11,12.

Chemical characters may be broadly categorized into visible traits, micromolecular, and macromolecular. Compared to the very few visible characters, such as starch grains, raphides, lapachols and silica that have limited usage in taxonomy, the micro- and macro-molecules prove to be important taxonomic tools¹³. Micromolecular characters relate to the low molecular weight secondary metabolites belonging to various chemical classes, such as phenolic, alkaloid, terpenoid, cyanogenic, free amino acid, lipid and others. Examples of macromolecules offering such informations include certain proteins, DNA and RNA. Though chemical characters offer themselves as important taxonomic tools, some of them, for instance, alkaloids and proteins are susceptible to change with regard to changing environmental conditions or ontogeny. Plant parts of the same physiological age should, therefore, be used for comparative analysis.

Phytophenols

Phytophenols are the ubiquitous class of bioactive constituents of the human diet, manifesting both nutritional and health benefits, mediated largely by their redox property, reactive species-scavenging and metal chelating capacities¹⁴. They are thus capable of mitigating oxidative stress-induced tissue damage associated with chronic diseases. Structurally, plant phenolics are a diversified group of plant-derived molecules, originated from the pentose phosphate, shikimate and phenylpropanoid pathways. This class of secondary metabolites are produced by the plant kingdom, including certain algae and specific insects. In plants, they are distributed throughout most tissues, including the flowers, roots, seeds and leaves, with the foliar phenolics expressing greater stability¹⁵. Plant phenolics are characterized by the presence of at least one aromatic ring with one or more hydroxyl groups directly bonded to the ring. They range from the naturally occurring simple, low molecular weight, single-aromatic-ring compounds to the large and complex tannins and derived-polyphenols. The most productive plant metabolic route, in terms of the number of phenolic substances it produces, is the one that leads to the flava-/flavo-noids, a C₆‒C₃‒C₆ framework with close to 10,000 structures characterised to date¹⁴. Flavonoids, because of their easy isolation, identification, stability and occurrence in different structural forms, have been used extensively for differentiating various species, establishing relationships at inter-generic and sub-familial levels and solving taxonomic problems¹³.

Phylogenetic systematics of Cucumis

Phylogenetic relationships in the order Cucurbitales as well as the phylogeny and classification of its taxonomically most problematic family, Cucurbitaceae, have been the focus of several studies of the recent past^16-19. Taxonomists over the years have differed on the delimitation of Cucumis, which was first described by Linnaeus in Species plantarum (1753). Numerous taxonomic treatments of Cucumis have been proposed since the pioneering work of Linnaeus⁸. Using maximum parsimony, maximum likelihood, and Bayesian inference analyses of sequence data from both the nuclear and chloroplast genomes, Ghebretinsae, Thulin and Barber have provided a comprehensive phylogeny of Cucumis and the traditionally related genera, Cucumella Chiovenda, Dicaelospermum C.B. Clarke, Mukia Arnott,  Myrmecosicyos C. Jeffrey and Oreosyce Hooker f.^8,9. Accordingly, the genus Cucumis from its erstwhile paraphyletic circumscription is recircumscribed by including the five genera of the subtribe cucumerinae Pax in compliance with the monophyly of Cucumis^8-10.

Foliar phenolics of Cucumis

Two major chemical classes, viz., cucurbitacins and flavonoids dominate the phytochemistry of cucurbits. Cucurbitacins are bitter-tasting triterpenoids that are present in high concentrations in root tissue and are toxic to mammals. In contrast, the fruits of many species in this family are edible and used as foods, including pumpkin, watermelon, melon and cucumber²⁰. Since the foliar phenolics generally contribute significantly to chemosystematics of both, angiosperms and gymnosperms, it is felt that an evaluation of the data available on the foliar flavonoid constitution of the recently defined Cucumis would be relevant. Survey of the flavonoid constitution of Cucumis has probably originated from the U.S. Vegetable Breeding Laboratory in 1969 during the screening for nematode resistance by Brown et al.²¹. Twenty six compounds have been identification by paper chromatography from 15 Cucumis species. Based on the similarities in the distribution of flavonoids, they had grouped the studied species into two large complexes. The first consisted of C. africanus, C. heptadactylus, C. melo and C. myriocarpus and the second one composed of C. anguria, C. dipsaceus, C. ficifolius, C. prophetarum, C. pustulatus, and C. zeyheri. Cucumis hirsutus, C. humifructus, C. metuliferus, C. sagittatus, and C. sativus were each considered to be distinct from all the other species studied as they possessed distinct patterns unlike any other sp.

Table 1: Natural distribution of flavonoids in species and cultivar varieties of the genus Cucumis

Species/ cultivar varieties

Compound*

1

2

3

4

5

6

7

8

9

10

11

12

13

14

15

16

17

C. maderaspatanus22,23

+

+

+

+

+

+

C. melo var. Doublon24

+

+

+

+

C. metuliferus25

+

C. myriocarpus25

+

+

+

C. sativus25,26

+

+

+

+

+

+

+

+

+

+

+

C. sativus Mustang27

+

+

+

+

C. sativus Cezar25

+

+

+

+

+

C. sativus Hela25

+

+

+

C. sativus Monastyrski25

+

+

C. sativus Olimp25

+

C. sativus Polan25

+

+

+

C. sativus Delicius25

+

+

+

+

+

 

Foliar phenolics of Cucumis

Two major chemical classes, viz., cucurbitacins and flavonoids dominate the phytochemistry of cucurbits. Cucurbitacins are bitter-tasting triterpenoids that are present in high concentrations in root tissue and are toxic to mammals. In contrast, the fruits of many species in this family are edible and used as foods, including pumpkin, watermelon, melon and cucumber²⁰. Since the foliar phenolics generally contribute significantly to chemosystematics of both, angiosperms and gymnosperms, it is felt that an evaluation of the data available on the foliar flavonoid constitution of the recently defined Cucumis would be relevant. Survey of the flavonoid constitution of Cucumis has probably originated from the U.S. Vegetable Breeding Laboratory in 1969 during the screening for nematode resistance by Brown et al.²¹. Twenty six compounds have been identification by paper chromatography from 15 Cucumis species. Based on the similarities in the distribution of flavonoids, they had grouped the studied species into two large complexes. The first consisted of C. africanus, C. heptadactylus, C. melo and C. myriocarpus and the second one composed of C. anguria, C. dipsaceus, C. ficifolius, C. prophetarum, C. pustulatus, and C. zeyheri. Cucumis hirsutus, C. humifructus, C. metuliferus, C. sagittatus, and C. sativus were each considered to be distinct from all the other species studied as they possessed distinct patterns unlike any other sp.

Conclusions:

The occurrence of 3 and 12 in C. maderaspatanus L. is chemosystematically in harmony with the recent revision of the genus Cucumis L. The present study is however subject to the limitations that the flavonoid profile available in literature to date is only limited and requires more study reports to gain larger sample size. Further, the reports of partially/incompletely characterized compounds 14 – 16 as well as those reported from eight other species by Brown et al.²¹ has restricted the specificity of the marker compound.

References

1. Crase B, In: Short P.S., Cowie, I.D. (eds), Flora of the Darwin Region. (Northern Territory Herbarium, Department of Natural Resources, Environment, the Arts and Sport). Vol. 1, pp. 1–17 (2011).
2. Petrus A.J.A., Asian J Chem, 24, 2361 (2012).
3. Petrus A.J.A., Indian J. Nat. Prod. Resour., 4, 9 (2013).
4. Petrus A.J.A., Phcog. J., 4 (34), 1 (2012).
5. Sebastian P., Schaefer H., Telford I.R.H., Renner S.S., PNAS, 107, 14269 (2010).
6. Jeffrey C., In: Milne-Redhead, E., Polhill, R.M. (eds), Flora of Tropical East Africa, Crown Agents for Overseas Governments and Administrations: London, (1967).
7. Renner S.S., Schaefer H., Kocyan A. BMC Evolutionary Biol., 7, 58 (2007).
8. Ghebretinsae A.G., Thulin M., Barber J.C., Amer. J. Bot., 94, 1256 (2007).
9. Ghebretinsae A.G., Thulin M., Barber J.C. Novon 17, 176 (2007)
10. Schaefer H., Blumea, 52, 165 (2007).
11. Hutchinson J., The families of flowering plants, 2nd edn. Oxford University Press, Oxford (1959).
12. Davis P.H., Heywood V.H. Principles of angiosperm taxonomy. Robert E Kreiger Publishing Company, New York (1973).
13. Sharma G., Proc. Natl. Acad. Sci., India, Sect. B Biol. Sci. 83, 141 (2013).
14. Petrus A.J.A., Asian J Chem, Article communicated.
15. Cronquist A., Plant Syst. Evol. Suppl. 1, 179 (1977).
16. Jeffrey C., Bot. Zhurn., 90, 332 (2005).
17. Zhang L.-B., Simmons M.P., Kocyan A., Renner S.S., Molec. Phylog. Evol., 39: 305 (2006).
18. Schaefer H., Heibl C., Renner S.S., Proc. Roy. Soc. London, Ser. B, Biol. Sci. 276, 843 (2009).
19. Schaefer H., Renner S.S., TAXON 60, 122 (2011).
20. P.K. Mukherjee, N.K. Nema, N. Maity and B.K. Sarkar, Fitoterapia 84, 227 (2013).
21. Brown G.B., Deakin J. R., Wood M.B., J. Amer. Soc. Hort. Sci., 94, 231 (1969).
22. Petrus A.J.A., Bhuvaneshwari N., Alain J.A.L., Indian J. Nat. Prod. Resour., 2, 34 (2011).
23. Petrus A.J.A., Bhuvaneshwari N., Asian J. Chem., 24, 1261 (2012).
24. Monties B., Bouillan M.L., Chopin J., Phytochemistry,15, 1053 (1976).
25. Krauze-Baranowska M., Cisowski W., Biochem. Systemat. Ecol., 29, 321 (2001).
26. McNally D.J., Wurms K.V., Labbé C., Quideau S., Bélanger R.R., J. Nat. Prod., 66, 1280 (2003).
27. Abou-Zaid M.M., Lombardo D.A., Kite G.C., Grayer R.J., Veitch N.C., Phytochemistry 58, 167 (2001).
28. Petrus A.J.A., Bhuvaneshwari N., UGC-SAP, DST and CSIR sponsored National Seminar on New Frontiers in Chemistry, Annamalai University, Annamalai Nagar, India, (2010).
29. Chopin J., Bouillant M.L., In: Harborne J.B, Mabry T.J., Mabry H., (eds.) The Flavonoids. Chapman & Hall Ltd., London pp. 650-667 (1975).
30. Osawa T., Katsuzaki H., Hagiwara Y., Hagiwara H., Shibamoto T., J. Agric. Food Chem. 40, 1135 (1992).
31. Kitta K., Hagiwara Y. and Shibamoto T., J. Agric. Food Chem. 40, 1843 (1992).
32. Nishiyama T., Hagiwara Y., Hagiwara H. and Shibamoto T., J. Amer. Oil Chemists Soc., 70, 911 (1993).
33. Miyake T., Hagiwara Y., Hagiwara H. and Shibamoto T., Symposium of Functional Foods, 213^th ACS National Meeting 1997.
34. Miyake T., Shibamoto T., J. Agric. Food Chem. 45, 1819 (1997).
35. Miyake T., Shibamoto T., J. Agric. Food Chem. 46, 3694 (1998).
36. Markham K.R., Mitchell K.A., Z. Naturforsch., 58c, 53 (2003).
37. Cogniaux A., In A.L.P.P. de Candolle and A.C.P. de Candolle [eds.], Monographiae phanerogamarum, vol. 3, pp. 325–951, 953–954. G. Mason, Paris, France (1881).
38. Cho Y.H., Kim J.H., Sim G.S.  Lee B.C., Pyo  H.B.,  Park  H.D.,  J.  Cosmet.  Sci.  57, 279 (2006).
39. Mondal A., Maity T.K., Pal D.K., Pharm. Biol., 50, 1151 (2012).
40. Lalhriatpuii T.C., Ghosh S.K., Achari B., Lalawmpuii P.C., Vanlalruata R, J. Pharm. Res., 1,15 (2013).
41. Langoljam R.D., Kongbrailatpam B.D., Laitonjam W.S., Indian J. Chem., 44B, 1291 (2005).
42. Jeffrey C., Kew Bulletin 15, 337 (1962). Renner S.S., Pandey A.K. PhytoKeys 20, 53 (2013).

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