Dear Editor-in-Chief
Modern agriculture faces pressing problems, such as salinization that is a very common, but difficult to control and ameliorate process. Non-enzymatic compounds such as polyphenols and flavonoids are generally stimulated in response to biotic/abiotic stresses such as salinity (1). Halophytes are naturally salt-tolerant plants that may be potentially useful for economical (oilseed, forage, production of metabolites) purposes (2). Recent data suggest that halophytes can serve as a source of valuable secondary metabolites with assumed economic value (3). Total phenolics and flavonoids were attributed as antioxidants with use in food, cosmetic, pharmacognosy, functional foods and nutraceuticals (4).
In this context, due to increased interest in maximize the economic potential of plants growing in saline environments, this papers aims at revealing new findings about Romanian halophytes as possible candidates for economic or medicinal purposes.
Plant material has been collected from salt areas from Valea Ilenei (Leţcani) nature reserve. Yet it is a small nature reserve, several species are included in the Red Book of Iaşi district.
Plant material was collected from 4–5 individuals of each species. Leaves and shoots (in the case of articulated succulent species) were sampled in the summer of 2011.
The following species were collected for subsequent analysis: Salicornia europaea L., Halimione verrucifera (M. Bieb.) Aellen, Suaeda maritima (L.) Dumort., Petrosimonia triandra (Pall.) Simonk., Atriplex prostrata Boucher ex DC. (Chenopodiaceae), Juncus gerardii Loisel. (Juncaceae), Boloboschoenus maritimus (L.) Palla (Cyperaceae), Limonium gmelinii (Willd.) Kuntze (Plumbaginaceae), Plantago schwarzenbergiana Schur (Plantaginaceae), Lepidium cartilagineum (J. C. Mayer) Thell. spp. crassifolium (Waldst. et Kit.) Thell. (Brassicaceae), Inula britannica L., Artemisia santonica L., Aster linosyris (L.) Bernh. (Asteraceae).
Several of these species were explicitly recognized in Romanian traditional medicine (Aster linosyris, Salicornia europaea, Artemisia santonica, Limonium gmelinii, Inula britannica), while other genera have related-species with proved medicinal properties: Plantago and Lepidium (5).
Total polyphenols content was determined using a modified Folin-Ciocalteau method (6). Flavonoids content was measured following a spectrophotometric method (7). The obtained results show a different behavior of halophytes in terms of flavonoids biosynthesis (Table 1). All halophytes from Chenopodiaceae (Halimione, Salicornia, Atriplex, Suaeda, Petrosimonia) accumulate the lowest amount of flavonoids, with values ranged from 0.72 mg CE g−1 DW (S. europaea) to 2.80±0.27 mg CE g−1 DW (A. prostrata). Interestingly, these species might be included in a distinct, well defined cluster within investigated halophytes. Juncus gerardii and Bolboschoenus maritimus, two euryhaline species that vegetates only in wet, even flooded saline environments are very similar in flavonoids biosynthesis. Limonium, Plantago and Lepidium show generally only a slightly increased value of accumulated flavonoids, as compared to chenopods species. The highest values of registered flavonoids occur in Asteraceae species, with huge value recorded for Aster linosyris, followed by Artemisia santonica and Inula britannica. This small group of halophytes might be regarded as a distinct cluster; nevertheless, these species have also in common the fact that they are xero-halophytes that could also suggest that the large accumulation of flavonoids is related to drought stress natural conditions.
Table 1:
Total polyphenols and flavonoids content in several halophytes collected from Valea Ilenei nature reserve
| Botanical name | Family | Flavonoids (mg CE g−1 DW) | Polyphenol (mg GAE g−1 DW) |
|---|---|---|---|
| Salicornia europaea | Chenopodiaceae | 0.72±0.04 | 1.04±0.070 |
| Halimione verrucifera | Chenopodiaceae | 1.35±0.09 | 2.96±0.11 |
| Suaeda maritima | Chenopodiaceae | 1.89±0.14 | 4.57±0.93 |
| Petrosimonia triandra | Chenopodiaceae | 2.41±0.07 | 4.06±0.15 |
| Atriplex prostrata | Chenopodiaceae | 2.80±0.27 | 5.04±0.45 |
| Juncus gerardii | Juncaceae | 2.12±0.20 | 3.39±0.27 |
| Boloboschoenus maritimus | Cyperaceae | 2.21±0.13 | 4.28±0.13 |
| Limonium gmelinii | Plumbaginaceae | 1.57±0.10 | 5.60±0.45 |
| Plantago schwarzenbergiana | Plantaginaceae | 3.83±0.49 | 3.50±0.35 |
| Lepidium crassifolium | Brassicaceae | 2.37±0.55 | 6.73±0.29 |
| Inula britannica | Asteraceae | 3.64±0.34 | 4.07±0.10 |
| Artemisia santonica | Asteraceae | 7.86±0.54 | 8.54±0.52 |
| Aster linosyris | Asteraceae | 15.38±2.19 | 14.93±1.34 |
Polyphenols biosynthesis is generally slightly higher (Table 1). Chenopods species show relatively lower values within other species; yet, there seems not to be a clear correlation between halophytes type and polyphenols accumulation. For instance, Suaeda accumulates 4-fold higher amount of phenolics than Salicornia, even both of them have more or less the same ecological spectra. Salicornia records the smallest value from all chenopods. Regarding other species, there is no clear correlation between profile species and polyphenols accumulation; Juncus and Bolboschoenus, two halophytes from marshy environments show similar pattern accumulation. Limonium, Plantago, and Lepidium (different taxonomically) species synthesize polyphenols in a higher amount than flavonoids. A quite different cluster seems to be also maintained in the case of Asteraceae halophytes: Inula, Artemisia, and Aster, who register the highest value within all investigated species. As in the case of flavonoids, this large polyphenols biosynthesis could be rather related to drought conditions and affiliation to botanical family.
Nevertheless, in halophytes vegetating in their habitats, the polyphenols content varies among large limits. For instance, in the case of a man-grove associate species, Suaeda maritima, Banerjee et al. (8) found out similar values (4.72 GAE mg/g) as in the case of Romanian investigated species. In the same study, other mangrove species accumulate polyphenols in the range of species investigated by us; thus, Ceriops decandra, Bruguiera gymnorrhiza, Sesuvium portulacastrum, Acanthus illicifolius, and Avicennia alba show values of total phenolic content ranging from 5.14 to 11.73 GAE mg/g. Halophytes collected from a different geographical area of Romania (Dobrogea, SE of Romania) synthesize higher values of total phenolics (9) than our investigated species, here including S. maritima and S. europaea.
Flavonoid content largely varies in different halophytes species; for instance, in three halophytes from Libya, Mesembryanthemum crystallinum, Limoniastrum guyonianum, Anabasis articulata huge amount of flavonoids have been recorded (10), as compared to our investigated species. The same species of Limonium collected from other geographical area of Romania (Dobrogea region) display approximately the same value of flavonoid content (9). The same is true for S. maritima and S. europaea, but other species of Plantago (P. maritima, P. coronopus, P. lanceolata) generally synthesize higher values of flavonoids.
Our study revealed a high diversity of flavonoids and total phenolic in investigated halophytes. Generally, the content of phenols is higher than flavonoids, but there are no significant differences between species, although they are very heterogeneous from taxonomical and ecological point of view.
Competing interests
The authors declare that there is no conflict of interests.
References
- 1. Navarro JM, Flores P, Garrido C, Martinez V. (2006). Changes in the contents of antioxidant compounds in pepper fruits at ripening stages, as affected by salinity. Food Chem, 96: 66–73. [Google Scholar]
- 2. Parvaiz A, Satyawati S. (2008). Salt stress and phyto-biochemical responses of plants. A review. Plant Soil Environ, 54: 89–99. [Google Scholar]
- 3. Ksouri R, Ksouri WM, Jallali I, Debez A, Magné C, Hiroko I, Abdelly C. (2012). Medicinal halophytes: potent source of health promoting biomolecules with medical, nutraceutical and food applications. Crit Rev in Biotechnol, 32: 289–32. [DOI] [PubMed] [Google Scholar]
- 4. Macheix JJ, Fleuriet A, Jay-Allemand C. (2005). Les composés phénoliques des végétaux, un exemple de métabolites secondaires d’importance économique, édition. Lausanne: Presses Polytechniques et Universitaires Romandes. [Google Scholar]
- 5. Toma C, Grigore MN, Afemei M, Stănescu I. (2010). Histo-anatomical considerations on some Romanian Inula L. species, with pharmacological action. An Şt Univ Al. I. Cuza”, s. II.a. Biol Veget, 56 ( 1): 5–16. [Google Scholar]
- 6. Singleton VL, Orthofer R, Lamuela-Raventos RM. (1999). Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Methods Enzymol, 299: 152–178. [Google Scholar]
- 7. Dewanto V, Wu X, Adom KK, Liu RH. (2002). Thermal processing enhances the nutritional value of tomatoes by increasing total antioxidant activity. J Agr Food Chem, 50: 3010–3014. [DOI] [PubMed] [Google Scholar]
- 8. Banerjee D, Chakrabarti S, Hazra AK, Banerjee S, Ray J, Mukherjee B. (2008). Antioxidant activity and total phenolics of some mangroves in Sundarbans. Afr J Biotechnol, 7 ( 6): 805–810. [Google Scholar]
- 9. Ivan M, Oprica L. (2013). Study of polyphenols and flavonoids contents of some halophytes species collected from Dobrogea region. Bull of the Transilv Univ of Brasov Series II. Forestry, Wood Industry. Agric Food Engin, 6 ( 55): 121–128. [Google Scholar]
- 10. Mohammed HA, Alshalmani SK, Abdellatif AG. (2013). Antioxidant and Quantitative Estimation of Phenolic and Flavonoids of Three Halophytic Plants Growing in Libya. J Pharm Phytochem, 2 ( 3): 89–94. [Google Scholar]