Abstract
The phenolic content of Spartina maritima was investigated using chromatographic and spectroscopic techniques. Aqueous methanolic extracts were prepared from plant collected in different seasons in the Bay of Arcachon (French Atlantic coast). High performance liquid chromatography (HPLC) with diode array detection (DAD) coupled with mass spectrometry allowed identification of four major phenolics in the aerial tissue, all belonging to the C-glycosidic-flavonoid class. They were isolated from the crude extracts, and their structures were assigned to isovitexin, isoscoparin and their respective 2″-O-glucosides on the basis of NMR, mass and UV spectroscopies. The seasonal variation of the flavonoid content was quantified over the period January 2013 to May 2015. The total concentration found ranged from 1.73 to 4.60 mg g−1 dry wt for isovitexin derivatives, and 0.88–2.66 mg g−1 dry wt for isoscoparin derivatives. The phenolic content of the rhizomes was very low and mainly dominated by coumaric acid (0.03–0.08 mg g−1), along with ferulic acid (≤0.06 mg g−1). The lack of significant concentrations of flavonoids in the rhizome contrasts with the aerial tissue. This work constitutes the first phenolic profiling of S. maritima and should provide a foundation for further studies, considering the reported biological activities of C-glycosidic flavonoids, and the lack of knowledge of the phenolic chemistry of the genus Spartina.
About the authors
Micheline Grignon-Dubois was awarded a PhD and a Doctorate of Chemical Sciences in organosilicon chemistry by the University of Bordeaux (France). Since 1995, she has held a position as director of research at the CNRS, where she has specialized in phytochemistry and metabolomics profiling. Her main research interests are applied to polyphenols and how these compounds are produced in response to stress and changing environments. Most of her recent work focuses on the isolation and structural elucidation of secondary metabolites from marine plants, seagrass chemosystematics, commercial and environmental applications of seagrass and algae detrital material as a source of high value-added natural marine products.
Bernadette Rezzonico is currently a research technician in the field of natural marine products at the University of Bordeaux. She received her advanced technical diploma (French DUT) in Chemistry from the University of Rouen. She is mainly interested in the application of environmentally friendly extraction and purification techniques and the development of qualitative and quantitative methods with analytical techniques, mainly HPLC.
Acknowledgments
This work is dedicated to Professor Jean-Marie Géhu in acknowledgment of his important contributions to botany and phytosociology, and his kind assistance in the identification of the Spartina species. We are grateful to the Service Central d’Analyse (SCA), CNRS, F69360 Solaize, for recording the LC/MS spectra.
References
Akiyama, K., H. Matsuoka and H. Hayashi. 2002. Isolation and identification of a phosphate deficiency-induced C-glycosylflavonoid that stimulates arbuscular mycorrhiza formation in melon roots. Mol. Plant-Microbe Interact. 15: 334–340.10.1094/MPMI.2002.15.4.334Search in Google Scholar PubMed
Arnold, T. and N.M. Targett. 2002. Marine tannins: the importance of a mechanistic framework for predicting ecological roles. J. Chem. Ecol. 28: 1919–1934.10.1023/A:1020737609151Search in Google Scholar
Baerlocher, F. and S.Y. Newell. 1994. Phenolics and proteins affecting palatability of Spartina leaves to the gastropod Littoraria irrorata. Mar. Ecol. 15: 65–75.10.1111/j.1439-0485.1994.tb00042.xSearch in Google Scholar
Balasundram, N., K. Sundram and S. Samman. 2006. Phenolic compounds in plants and agri-industrial by-products: antioxidant activity, occurrence, and potential uses. Food Chem. 99: 191–203.10.1016/j.foodchem.2005.07.042Search in Google Scholar
Bertrand, F. 2014. The Arcachon Bay estuary: a “collage” of landscapes. In: (F.M. Fort and M.F. André, eds.) Landscapes and Landforms of France. World Geomorphological Landscapes, Springer, Dordrecht. pp. 71–80.10.1007/978-94-007-7022-5_8Search in Google Scholar
Bhattacharya, A., P. Sood and V. Citovsky. 2010. The roles of plant phenolics in defence and communication during Agrobacterium and Rhizobium infection. Mol. Plant Pathol. 11: 705–719.10.1111/j.1364-3703.2010.00625.xSearch in Google Scholar PubMed PubMed Central
Boudet, A. 2007. Evolution and current status of research in phenolic compounds. Phytochemistry 68: 2722–2735.10.1016/j.phytochem.2007.06.012Search in Google Scholar PubMed
Brazier-Hicks, M., K.M. Evans, M.C. Gershater, H. Puschmann, P.G. Steel and R. Edwards. 2009. The C-Glycosylation of Flavonoids in Cereals. J. Biol. Chem. 284: 17926–17934.10.1074/jbc.M109.009258Search in Google Scholar PubMed PubMed Central
Cardoso, C.A.L., R.G. Coelho, N.K. Honda, A. Pott, F.R. Pavan and C.Q.F. Leite. 2013. Phenolic compounds and antioxidant, antimicrobial and antimycobacterial activities of Serjania erecta Radlk. (Sapindaceae). Braz. J. Pharma. Sci. 49: 775–782.10.1590/S1984-82502013000400017Search in Google Scholar
Castillo, J.M. and E. Figueroa. 2009a. Effects of abiotic factors on the life span of the invasive cordgrass Spartina densiflora and the native Spartina maritima at low salt marshes. Aquat. Ecol. 43: 51–60.10.1007/s10452-007-9159-2Search in Google Scholar
Castillo, J.M. and E. Figueroa. 2009b. Restoring salt marshes using small cordgrass, Spartina maritima. Rest. Ecol. 17: 324–326.10.1111/j.1526-100X.2008.00465.xSearch in Google Scholar
Castillo, J.M., L. Fernández-Baco, E.M. Castellanos, C.J. Luque, M.E. Figueroa and A.J. Davy. 2000. Lower limits of Spartina densiflora and S. maritima in a Mediterranean salt marsh determined by different ecophysiological tolerances. J. Ecol. 88: 801–812.10.1046/j.1365-2745.2000.00492.xSearch in Google Scholar
CBNSA (Conservatoire Botanique National Sud-Atlantique). 2014. Guide d’identification des spartines du Bassin d’Arcachon. http://www.cbnsa.fr/delta/fichiers/envahissantes/pdf/guide_d_identifications_spartines_bassin.pdf.Search in Google Scholar
Chandra, Y., A. Rana and J. Li. 2001. Separation, identification, quantification, and method validation of anthocyanins in botanical supplement raw materials by HPLC and HPLC-MS. J. Agric. Food Chem. 49: 3515–3521.10.1021/jf010389pSearch in Google Scholar PubMed
Chevalier, A. 1953. La distribution géographique et la nomenclature des Spartina des vases salées dans l’Ancien et dans le Nouveau- Monde. Dernière opinion. In: Revue internationale de botanique appliquée et d’agriculture tropicale, 33ᵉ année, bulletin n°371–372, Septembre-octobre 1953. pp. 403–408.10.3406/jatba.1953.6622Search in Google Scholar
Cheynier, V., G. Comte, K.M. Davies, V. Lattanzio and S. Martens. 2013. Plant phenolics: recent advances on their biosynthesis, genetics, and ecophysiology. Plant Physiol. Biochem. 72: 1–20.10.1016/j.plaphy.2013.05.009Search in Google Scholar PubMed
Courts, F.L. and G. Williamson. 2015. The Occurrence, Fate and Biological Activities of C-glycosyl Flavonoids in the Human Diet. Crit. Rev. Food Sci. 55: 1352–1367.10.1080/10408398.2012.694497Search in Google Scholar PubMed
Curado, G., A.E. Rubio-Casal, E. Figueroa and J.M. Castillo. 2014. Potential of Spartina maritima in restored salt marshes for phytoremediation of metals in a highly polluted estuary. Int. J. Phytoremediation 16: 1209–1220.10.1080/15226514.2013.821451Search in Google Scholar PubMed
De Bertoldi, C., M. de Leo, A. Braca and L. Ercoli. 2009. Bioassay-guided isolation of allelochemicals from Avena sativa L.: allelopathic potential of flavone C-glycosides. Chemoecology 19: 169–176.10.1007/s00049-009-0019-5Search in Google Scholar
Delazar, A., S. Gibbons, A. Kosari, H. Nazemiyeh, M. Modarresi, L. Nahar and S. Sarker. 2006. Flavone C-glycosides and cucurbitacin glycosides from Citrullus colocynthis. DARU 14: 109–114.Search in Google Scholar
Duarte, B., D. Santos and I. Caçador. 2013. Halophyte anti-oxidant feedback seasonality in two salt marshes with different degrees of metal contamination: search for an efficient biomarker. Funct. Plant Biol. 40: 922–930.10.1071/FP12315Search in Google Scholar PubMed
Duarte, B., J. Carreiras, J. Alberto Pérez-Romero, E. Mateos-Naranjo, S. Redondo-Gómez, A.R. Matos, J.C. Marques and I. Caçador. 2018. Halophyte fatty acids as biomarkers of anthropogenic-driven contamination in Mediterranean marshes: sentinel species survey and development of an integrated biomarker response (IBR) index. Ecol. Indic. 87: 86–96.10.1016/j.ecolind.2017.12.050Search in Google Scholar
Falcone Ferreyra, M.L., S.P. Rius and P. Casati. 2012. Flavonoids: Biosynthesis, Biological functions and Biotechnological applications. Front. Plant Sci. 3: 222.10.3389/fpls.2012.00222Search in Google Scholar PubMed PubMed Central
Ferreira de Carvalho, J., H. Chelaifa, J. Boutte, J. Poulain, A. Couloux, P. Wincker, A. Bellec, J. Fourment, H. Berges, A. Salmon and M. Ainouche. 2013a. Exploring the genome of the salt-marsh Spartina maritima (Poaceae, Chloridoideae) through BAC end sequence analysis. Plant Mol. Biol. 83: 591–606.10.1007/s11103-013-0111-7Search in Google Scholar
Ferreira de Carvalho, J., J. Poulain, C. Da Silva, P. Wincker, S. Michon-Coudouel, A. Dheilly, D. Naquin, J. Boutte, A. Salmon and M. Ainouche. 2013b. Transcriptome de novo assembly from next-generation sequencing and comparative analyses in the hexaploid salt marsh species Spartina maritima and Spartina alterniflora (Poaceae). Heredity 110: 181–193.10.1038/hdy.2012.76Search in Google Scholar
Ferreira de Carvalho, J., J. Boutte, P. Bourdaud, H. Chelaifa, K. Ainouche, A. Salmon and M. Ainouche. 2017. Gene expression variation in natural populations of hexaploid and allododecaploid Spartina species (Poaceae). Plant Syst. Evol. 303: 1061–1079.10.1007/s00606-017-1446-3Search in Google Scholar
Franz, G. and M. Grun. 1983. Chemistry, occurrence and biosynthesis of C-Glycosyl compounds in plants. Planta Med. 47: 131–140.10.1055/s-2007-969972Search in Google Scholar
Géhu, J.-M. 1973. Premiers compléments chorologiques au fascicule 1 Spartinetea maritimae du prodrome des groupements végétaux d’Europe. Documents Phytosociologiques 4: 47–49.Search in Google Scholar
Géhu, J.-M. 2008. Les Spartines des côtes de France et d’Europe. Phytogéographie et socioécologie. Aestuaria 13. Les plantes envahissantes du littoral atlantique. Le cas de la Spartine anglaise: 13–33.Search in Google Scholar
Grignon-Dubois, M. and C. Echmak. 2013. First evaluation of the marine invasive species Spartina anglica as a potential renewable source of glycine betaine. J. Appl. Pharmaceut. Sci. 3: 029–034.Search in Google Scholar
Harborne, J.B. 1980. Plant phenolics. In: (E.A. Bell and B.V. Charlwood, eds.) Encyclopedia of plant physiology. Springer-Verlag Berlin, Heidelberg, New York. pp. 329–395.Search in Google Scholar
Harborne, J.B. and C.A. Williams. 1976. Flavonoid patterns in leaves of the gramineae. Biochem. Syst. Ecol. 4: 267–280.10.1016/0305-1978(76)90051-XSearch in Google Scholar
Haribal, M. and J.A.A. Renwick. 1998. Isovitexin 6″-O-β-D-glucopyranoside: a feeding deterrent to Pieris nupi oleracea from Alliaria petiolata. Phytochemistry 47: 1237–1240.10.1016/S0031-9422(97)00740-1Search in Google Scholar
IPNI (International plant name index). 2018. Sporobolus maritimus (Curtis) P.M.Peterson & Saarela http://www.ipni.org/ipni/plantNameByVersion.do?id=77144701-1&version=1.3&output_format=lsid-metadata&show_history=true.Search in Google Scholar
Kern, V.G., N.J. Guarise and A.C. Vegetti. 2008. Inflorescence structure in species of Spartina Schreb. (Poaceae: Chloridoideae: Cynodonteae). Plant Syst. Evol. 273: 51–61.10.1007/s00606-008-0009-zSearch in Google Scholar
Kim, M., H.S. Koh and H. Fukmai. 1985. Isolation of C-glucosylflavones as probing stimulant of plant hoppers in rice plant. J. Chem. Ecol. 11: 441–452.10.1007/BF00989555Search in Google Scholar PubMed
Kim, B., S. Woo, M-J. Kim, S-W. Kwon, J. Lee, S. Hyun Sung and H.-J. Koh. 2018. Identification and quantification of flavonoids in yellow grain mutant of rice (Oryza sativa L.). Food Chem. 241: 154–162.10.1016/j.foodchem.2017.08.089Search in Google Scholar PubMed
Kitta, K., Y. Hagiwara and T. Shibamoto. 1992. Antioxidative activity of an isoflavonoid, 2″-O-Glycosylisovitexin isolated from green barley leaves. J. Agric. Food Chem. 40: 1843–1845.10.1021/jf00022a023Search in Google Scholar
Kulbat, K. 2016. The role of phenolic compounds in plant resistance. Biotechnol. Food Sci. 80: 97–108.Search in Google Scholar
Kumarasamy, Y., M. Byres, P.J. Cox, A. Delazar, M. Jaspars, L. Nahar, M. Shoeb and S.D. Sarker. 2004. Isolation, structure elucidation and biological activity of flavone 6 C-glycosides from Alliaria petiolate. Chem. Nat. Comp. 40: 122–128.10.1023/B:CONC.0000033926.72396.41Search in Google Scholar
Lattanzio, V., V. Lattanzio and A. Cardinali. 2006. Role of phenolics in the resistance mechanisms of plants against fungal pathogens and insects. In: (F. Imperato, ed) Phytochemistry: advances in research. Research Signpost, Trivandrum, Kerala. pp. 23–67.Search in Google Scholar
Les, D. and D.J. Sheridan. 1990. Biochemical heterophylly and flavonoid evolution in North American Potamogeton (Potamogenoceae). Am. J. Bot. 77: 453–465.10.1002/j.1537-2197.1990.tb13576.xSearch in Google Scholar
Li, S.-H., Q. Zhao, Y. Cheng and F. Liu. 2013. Antimicrobial activities of vitexin from Alsophila spinutosa. Food Res. Develop. 34: 4–6.Search in Google Scholar
Mabry, T.J., K.R. Markham and M.B. Thomas. 1970. The aglycone and sugar analysis of flavonoid glycosides. In: The systematic identification of flavonoids. Springer, Berlin, Heidelberg. pp. 23–32.10.1007/978-3-642-88458-0_3Search in Google Scholar
Manan, F.A., D.D. Mamat, A.A. Samad, Y.S. Ong, K.F. Ooh and T.T. Chai. 2015. Heavy metal accumulation and antioxidant properties of Nephrolepis biserrata growing in heavy metal-contaminated soil. Global NEST J. 17: 544–554.10.30955/gnj.001463Search in Google Scholar
Mateos-Naranjo, E., S. Redondo-Gómez, L. Andrades-Moreno and A.J. Davy. 2010. Growth and photosynthetic responses of the cordgrass Spartina maritima to CO2 enrichment and salinity. Chemosphere 81: 725–731.10.1016/j.chemosphere.2010.07.047Search in Google Scholar
McNally, D.J., K.V. Wurms, C. Labbé, S. Quideau and R.R. Bélanger. 2003. Complex C-Glycosyl Flavonoid Phytoalexins from Cucumis sativus. J. Nat. Prod. 66: 1280–1283.10.1021/np030150ySearch in Google Scholar
Moreira da Silva, M., J. Anibal, D. Duarte and L. Chicharo. 2015. Sarcocornia fruticosa and Spartina maritima as heavy metals remediators in southwestern European salt marsh (Ria Formosa, Portugal). J. Environ. Prot. Ecol. 16: 1468–1477.Search in Google Scholar
Naidoo, G., Y. Naidoo and P. Achar. 2012. Ecophysiological responses of the salt marsh grass Spartina maritima to salinity. Afri. J. Aquat. Sci. 37: 81–88.10.2989/16085914.2012.666377Search in Google Scholar
Negrin, V.L., B. Teixeira, R. Godinho, R. Mendes and C. Vale. 2017. Phytochelatins and monothiols in salt marsh plants and their relation with metal tolerance. Mar. Pollut. Bull. 121: 78–84.10.1016/j.marpolbul.2017.05.045Search in Google Scholar
Otte, M.L. and J.T. Morris. 1994. Dimethylsulphoniopropionate (DMSP) in Spartina alterniflora Loisel. Aquat. Bot. 48: 239–259.10.1016/0304-3770(94)90018-3Search in Google Scholar
Peterson, P.M, K. Romaschenko and G. Johnson. 2010. A classification of the Chloridoideae (Poaceae) based on multi-gene phylogenetic trees. Mol. Phylogenet. Evol. 55: 580–598.10.1016/j.ympev.2010.01.018Search in Google Scholar PubMed
Peterson, P.M., K. Romaschenko, Y.H. Arrieta and J.M. Saarela. 2014a. A molecular phylogeny and new subgeneric classification of Sporobolus (Poaceae: Chloridoideae: Sporobolinae). Taxon 63: 1212–1243.10.12705/636.19Search in Google Scholar
Peterson, P.M., K. Romaschenko, Y. Herrera Arrieta and J.M. Saarela. 2014b. Proposal to conserve Sporobolus against Spartina, Crypsis, Ponceletia, and Heleochloa (Poaceae: Chloridoideae: Sporobolinae). Taxon 63: 1373–1374.10.12705/636.23Search in Google Scholar
Peterson, P.M., J.M. Saarela and K. Romaschenko. 2015. New combinations in Sporobolus (Poaceae: Chloridoideae). Phytoneuron 20: 1–2.Search in Google Scholar
Peterson, P.M., K. Romaschenko, Y. Herrera Arrieta and J.M. Saarela. 2017. A molecular phylogeny of the subtribe Sporobolinae and a classification of the subfamily Chloridoideae (Poaceae). Memoirs of the New York Botanical Garden 118: 127–151.10.21135/893275341.003Search in Google Scholar
Rabelo, A.S., I.D. Oliveira, A.G. Guimaraes, J.S.S. Quintans, A.P.N. Prata, D.P. Gelain, E.M. Venceslau, J.P.A. Santos, L.J. Quintans-Junior, L.R. Bonjardim, A. Barison, F.R. Campos, A.D.C. Santos, P.C.L. Nogueira, E.V. Costa, V.R.S. Moraes and A.A.S. Araujoan. 2013. Antinociceptive, anti-inflammatory and antioxidant activities of aqueous extract from Remirea maritima (Cyperaceae). J. Ethnopharmacol. 145: 11–17.10.1016/j.jep.2012.10.020Search in Google Scholar
Rahman, K., L. Krenn, B. Kopp, M. Schubert-Zsilavecz, K.K. Mayer and W. Kubelka. 1997. Isoscoparin-2″-O-glucoside from Passiflora incarnata. Phytochemistry 45: 1093–1094.10.1016/S0031-9422(97)00100-3Search in Google Scholar
Ramarathnam, N., T. Osawa, M. Namiki and S. Kawakishi. 1989. Chemical studies on novel rice hull antioxidants: 2. identification of isovitexin, a C-glycosylflavonoid. J. Agric. Food. Chem. 37: 316–319.10.1021/jf00086a009Search in Google Scholar
Ravisé, A. and J. Chopin. 1981. Influence de la structure de composés Phénoliques sur l’inhibition du Phytophthora parasitica et d’enzymes participant aux processus parasitaires V. Flavones, O- et C-glycosides. J. Phytopath. 100: 257–269.10.1111/j.1439-0434.1981.tb03299.xSearch in Google Scholar
Rayyan, S., T. Fossen, H.S. Nateland and O.M. Andersen. 2005. Isolation and identification of flavonoids, including flavone rotamers, from the herbal drug ‘Crataegi folium cum flore’ (Hawthorn). Phytochem. Anal. 16: 334–341.10.1002/pca.853Search in Google Scholar PubMed
Redondo-Gomez, S. 2013. Bioaccumulation of heavy metals in Spartina. Funct. Plant Biol. 40: 913–921.10.1071/FP12271Search in Google Scholar PubMed
Rietsma, C.S., I. Valiela and R. Buschsbaum. 1988. Detrital chemistry, growth, and food choice in the salt-marsh snail (Melampus bidentatus). Ecology 69: 261–266.10.2307/1943181Search in Google Scholar
Roberts, M.L. and R.R. Haynes. 1986. Flavonoid systematics of Potamogeton subsections Perfoliati and Praelongi (Potamogetonaceae). Nord. J. Bot. 6: 291–294.10.1111/j.1756-1051.1986.tb00881.xSearch in Google Scholar
Rousseau-Gueutin, M., S. Bellot, G.E. Martin, J. Boutte, H. Chelaifa, O. Lima, S. Michon-Coudouel, D. Naquin, A. Salmon, K. Ainouche and M. Ainouche. 2015. The chloroplast genome of the hexaploid Spartina maritima (Poaceae, Chloridoideae): comparative analyses and molecular dating. Mol. Phylogenet. Evol. 93: 5–16.10.1016/j.ympev.2015.06.013Search in Google Scholar
Saarela, J.M., S.V. Burke, W.P. Wysocki, M.D. Barrett, L.G. Clark, J. M. Craine, P.M. Peterson, R.J. Soreng, M.S. Vorontsova and M.R. Duvall. 2018. A 250 plastome phylogeny of the grass family (Poaceae): topological support under different data partitions. PeerJ 6: e4299.10.7717/peerj.4299Search in Google Scholar
Senatore, F., M. D’Agostino and I. Dini. 2000. Flavonoid Glycosides of Barbarea vulgaris L. (Brassicaceae). J. Agric. Food Chem. 48: 2659–2662.10.1021/jf990625kSearch in Google Scholar
Sieg, R.D. and J. Kubanek. 2013. Chemical ecology of marine angiosperms: opportunities at the interface of marine and terrestrial systems. J. Chem. Ecol. 39: 687–711.10.1007/s10886-013-0297-9Search in Google Scholar
Sieg, R.D., D. Willey, K. Wolfe and J. Kubanek. 2013. Multiple chemical defenses produced by Spartina alterniflora deter farming snails and their fungal crop. Mar. Ecol.- Prog. Ser. 488: 35–49.10.3354/meps10415Search in Google Scholar
Siska, E.L., S.C. Pennings, T.L. Buck and M.D. Hanisak. 2002. Latitudinal variation in palatability of salt-marsh plants: which traits are responsible? Ecology 83: 3369–3381.10.1890/0012-9658(2002)083[3369:LVIPOS]2.0.CO;2Search in Google Scholar
Soriano, I.R., R.E. Asenstorfer, O. Schmidt and I.T. Riley. 2004. Inducible flavone in oats (Avena sativa) is a novel defense against plant-parasitic nematodes. Nematology 94: 07–1214.10.1094/PHYTO.2004.94.11.1207Search in Google Scholar
Sun, X., J. Tang, W. Hu and N. Xu. 2013. Antioxidant flavonol compounds from the marine cordgrass Spartina anglica. Food Sci. Technol. Res. 19: 1093–1097.10.3136/fstr.19.1093Search in Google Scholar
Symonowicz, M. and M. Kolanek. 2012. Flavonoids and their properties to form chelate complexes. Biotechnol. Food Sci. 76: 35–41.Search in Google Scholar
Valiela, I. and C.S. Rietsma. 1984. Nitrogen, phenolic acids, and other feeding cues for salt marsh detritivores. Oecologia 63: 350–356.10.1007/BF00390664Search in Google Scholar
Valiela, I., L. Koumjian, T. Swain, J.M. Teal and J.E. Hobbie. 1979. Cinnamic acid inhibition of detritus feeding. Nature 280: 55–57.10.1038/280055a0Search in Google Scholar
Wallace, J.W. and T.J. Mabry. 1970. The conversion of the 8-C-glycosylflavone vitexin to the 6-isomer, isovitexin, in Lemna minor. Phytochemistry 9: 2133–2135.10.1016/S0031-9422(00)85378-9Search in Google Scholar
Wiseman, B.R. and J.E. Carpenter. 1995. Growth inhibition of corn earworm (Lepidoptera Noctuidae) larvae reared on resistant corn silk diets. J. Econ. Entom. 88: 1037–1043.10.1093/jee/88.4.1037Search in Google Scholar
WoRMS (World register of Marine Species). 2018. Spartina maritima (Curt.) Fernald. http://www.marinespecies.org/aphia.php?p=taxdetails&id=234038 on 2018-04–10.Search in Google Scholar
Xiao, J., E. Capanoglu, A. Reza Jassbi and A. Miron. 2016. Advance on the Flavonoid C-glycosides and Health Benefits. Crit. Rev. Food Sci. 56: sup1, S29–S45.10.1080/10408398.2015.1067595Search in Google Scholar PubMed
Yang, B., H. Liua, J. Yanga, V. K. Gupta and Y. Jianga. 2018. New insights on bioactivities and biosynthesis of flavonoid glycosides. Trends Food Sci. Technol. 79: 116–124.10.1016/j.tifs.2018.07.006Search in Google Scholar
Supplementary Material
The online version of this article offers supplementary material (https://doi.org/10.1515/bot-2018-0063).
© 2019 Walter de Gruyter GmbH, Berlin/Boston
