Effects of secondary metabolites on pollination in legume forage crops

Year 2023, Volume: 60 Issue: 3 - Journal of Agriculture Faculty of Ege University Volume: 60 Issue: 3, 539 - 552, 13.10.2023

Mehmet Arif Özyazıcı

https://doi.org/10.20289/zfdergi.1338227

Abstract

Plants have developed a number of defense strategies against herbivores, including the synthesis of secondary metabolites with toxic, repellent, and/or anti-nutritional effects. The ecological function of these secondary metabolites, which are generally classified as flavonoids, alkaloids and terpenoids, in plant defense is well known; however, their role in plant-pollinator interactions is not yet clear enough. According to available information, secondary metabolites found in flower nectar and pollen are effective in pollination like mediating pollination with the help of its attractive odour and color, protecting flowers and nectar from insects that do not contribute much in pollination, and reducing the level of disease factors in pollinators thanks to their microbial activities. In this review study, the effects of secondary metabolites in forage legumes on pollination were emphasized.

Keywords

Alkaloid, flavonoid, pollinator, polyphenol, secondary metabolite

Baklagil yem bitkilerinde sekonder metabolitlerin tozlaşmadaki etkileri

Abstract

Bitkiler, otoburlara karşı toksik, itici ve/veya beslenme karşıtı etkileri olan sekonder metabolitlerin sentezini içeren bir dizi savunma stratejisi geliştirmişlerdir. Genel olarak flavonoidler, alkaloidler ve terpenoidler sınıfında yer alan bu sekonder metabolitlerin, bitki savunmasındaki ekolojik işlevi iyi bilinmekte; ancak, bitki-tozlayıcı etkileşimlerindeki rolleri henüz yeterince açık değildir. Mevcut bilgilere göre, çiçeğin nektar ve poleninde bulunan sekonder metabolitler; renk ve koku gibi cezbedici özellikleri ile tozlaşmada aracılık etme, tozlaşmada çok fazla katkısı olmayan böceklerden çiçeği ve nektarı koruma ve mikrobiyal aktiviteleri sayesinde tozlayıcılardaki hastalık etmenlerinin seviyesini azaltma gibi faydaları özellikleri ile tozlaşmada etkili olmaktadır. Bu derleme çalışmasında, baklagil yem bitkilerindeki sekonder metabolitlerin tozlaşmadaki etkileri üzerinde durulmuştur.

Keywords

Alkaloid, flavonoid, polifenol, sekonder metabolit, tozlayıcı

References

• Abdallah, R.M., H.M. Hammoda, M.M. Radwan, N.S. El-Gazzar, A.S. Wanas, M.A. ElSohly, M.A. El-Demellawy, N.M. Abdel-Rahman & S.M. Sallam, 2021. Phytochemical and pharmacological appraisal of the aerial parts of Lotus corniculatus L. growing in Egypt. Natural Product Research, 35 (24): 5914-5917.
• Abdel-alim, M.E., M.S. Serag, H.R. Moussa, M.A. Elgendy, M.T. Mohesien & N.S. Salim, 2023. Phytochemical screening and antioxidant potential of Lotus corniculatus and Amaranthus viridis. Egyptian Journal of Botany, 63 (2): 665-681.
• Abdel-lateif, K., D. Bogusz & V. Hocher, 2012. The role of flavonoids in the establishment of plant roots endosymbioses with arbuscular mycorrhiza fungi, rhizobia and Frankia bacteria. Plant Signaling & Behavior, 7: 636-641.
• Abouzeid, S., U. Beutling, E. Elekhnawy & D. Selmar, 2023. Antibacterial and antibiofilm effects of allelopathic compounds identified in Medicago sativa L. seedling exudate against Escherichia coli. Molecules, 28: 2645.
• Adler, L.S., 2000. The ecological significance of toxic nectar. Oikos, 91 (3): 409-420.
• Ahmad, S., A. Zeb, M. Ayaz, & M. Murkovic, 2020. Characterization of phenolic compounds using UPLC–HRMS and HPLC–DAD and anti-cholinesterase and anti-oxidant activities of Trifolium repens L. leaves. European Food Research and Technology, 246: 485-496.
• Aniszewski, T., 2015. Alkaloids: Chemistry, Biology, Ecology, and Applications. 2nd Ed., Elsevier, Amsterdam, The Netherlands, 496pp.
• Arnold, S.E.J., M.E.P. Idrovo, L.J.L. Arias, S.R. Belmain & P.C. Stevenson, 2014. Herbivore defence compounds occur in pollen and reduce bumblebee colony fitness. Journal of Chemical Ecology, 40: 878-881.
• Ayadi, M., M.L. Bennani, A. Aarab, J. Brigui & M. Benicha, 2021. “Content of polyphenolic compounds in Melilotus officinalis ecotypes from Morocco, 559-563”. In: Efficiency and Resilience of Forage Resources and Small Ruminant Production to Cope with Global Challenges in Mediterranean Areas. (Eds. A. López-Francos, M. Jouven, C. Porqueddu, H. Ben Salem, A. Keli, A. Araba, & M. Chentouf), Zaragoza, CIHEAM, 716 pp.
• Baali, N., A. Mezrag, M. Bouheroum, F. Benayache, S. Benayache & A. Souad, 2020. Anti-inflammatory and antioxidant effects of Lotus corniculatus on paracetamol-induced hepatitis in rats. Anti-Inflammatory & Anti-Allergy Agents in Medicinal Chemistry, 19: 128-139.
• Bajkacz, S., I. Baranowska, B. Buszewski, B. Kowalski & M. Ligor, 2018. Determination of flavonoids and phenolic acids in plant materials using SLE-SPE-UHPLC-MS/MS method. Food Analytical Methods, 11: 3563-3575.
• Baker, H.G., 1977. Non-sugar chemical constituents of nectar. Apidologie, 8: 349-356.
• Bakır, Ö., 2020. Sekonder metabolitler ve rolleri. Uluslararası Anadolu Ziraat Mühendisliği Bilimleri Dergisi, 2 (4): 39-45.
• Bandana, C., P. Khanin, D. Priyanka, B.A. Ranjan, K. Hemen & B. Samindra, 2022. Nutritional evaluation of few grass pea (Lathyrus sativus L.) genotypes of Assam. Indian Journal of Agricultural Biochemistry, 35 (2): 155-158.
• Barberis, M., D. Calabrese, M. Galloni, & M. Nepi, 2023. Secondary metabolites in nectar-mediated plant-pollinator relationships. Plants, 12: 550.
• Barlow, S.E., G.A. Wright, C. Ma, M. Barberis, I.W. Farrell, E.C. Marr, A. Brankin, B.M. Pavlik & P.C. Stevenson, 2017. Distasteful nectar deters floral robbery. Current Biology, 27 (16): 2552-2558.e3.
• Benchadi, W., H. Haba, C. Lavaud, D. Harakat & M. Benkhaled, 2013. Secondary metabolites of Astragalus cruciatus Link. and their chemotaxonomic significance. Records of Natural Products, 7 (2): 105-113.
• Bhattacharjee, S., A. Waqar, K. Barua, A. Das, S. Bhowmik & S.R. Debi, 2018. Phytochemical and pharmacological evaluation of methanolic extract of Lathyrus sativus L. seeds. Clinical Phytoscience, 4: 20a.
• Boukid, F. & A. Pasqualone, 2022. Lupine (Lupinus spp.) proteins: characteristics, safety and food applications. European Food Research and Technology, 248: 345-356.
• Boussaha, S., M. Bramucci, K. Rebbas, L. Quassinti, R. Mekkiou & F. Maggi, 2023. Chemical composition and anticancer activity of the essential oil from Vicia ochroleuca Ten., quite rare plant in Kabylia (Algeria). Natural Product Research, DOI: 10.1080/14786419.2023.2176492.
• Bozek, M., B. Denisow, M. Strzałkowska-Abramek, E. Chrzanowska & K. Winiarczyk, 2023. Non-forest woody vegetation: A critical resource for pollinators in agricultural landscapes-A review. Sustainability, 15: 8751.
• Böttger, A., U. Vothknecht, C. Bolle & A. Wolf, 2018. “Plant secondary metabolites and their general function in plants, 3-17”. In: Lessons on Caffeine, Cannabis & Co. (Eds. A. Böttger, U. Vothknecht, C. Bolle & A. Wolf), Learning Materials in Biosciences, Springer, Cham, 217pp.
• Brun, G., L. Braem, S. Thoiron, K. Gevaert, S. Goormachtig & P. Delavault, 2018. Seed germination in parasitic plants: What insights can we expect from strigolactone research? Journal of Experimental Botany, 69 (9): 2265-2280.
• Butkutė, B., A. Padarauskas, J. Cesevičienė, A. Pavilonis, L. Taujenis & N. Lemežienė, 2017. Perennial legumes as a source of ingredients for healthy food: proximate, mineral and phytoestrogen composition and antibacterial activity. Journal of Food Science and Technology, 54 (9): 2661-2669.
• Byers, K.J.R.P., H.D. Bradshaw & J.A. Riffell, 2013. Three floral volatiles contribute to differential pollinator attraction in monkeyflowers (Mimulus). The Journal of Experimental Biology, jeb.092213.
• Chiocchio, I., M. Mandrone, P. Tomasi, L. Marincich & F. Poli, 2021. Plant secondary metabolites: an opportunity for circular economy. Molecules, 26: 495.
• Chomel, M., M. Guittonny‐Larchevêque, C. Fernandez, C. Gallet, A. DesRochers, D. Paré, B.G. Jackson & V. Baldy, 2016. Plant secondary metabolites: a key driver of litter decomposition and soil nutrient cycling. Journal of Ecology, 104 (6): 1527-1541.
• Clemensen, A.K., F.D. Provenza, S.T. Lee, D.R. Gardner, G.E. Rottinghaus & J.J. Villalba, 2017. Plant secondary metabolites in alfalfa, birdsfoot trefoil, reed canarygrass, and tall fescue unaffected by two different nitrogen sources. Crop Science, 57 (2): 964-970.
• Cook, D., J.S. Manson, D.R. Gardner, K.D. Welch & R.E. Irwin, 2013. Norditerpene alkaloid concentrations in tissues and floral rewards of larkspurs and impacts on pollinators. Biochemical Systematics and Ecology, 48: 123-131.
• Cortés-Avendaño, P., M. Tarvainen, J.P. Suomela, P. Glorio-Paulet, B. Yang & R. Repo-Carrasco-Valencia, 2020. Profle and content of residual alkaloids in ten ecotypes of Lupinus mutabilis sweet after aqueous debittering process. Plant Foods for Human Nutrition, 75: 184-191.
• Couvillon, M.J., H. Al Toufailia, T.M. Butterfield, F. Schrell, F.L.W. Ratnieks & R. Schürch, 2015. Caffeinated forage tricks honeybees into increasing foraging and recruitment behaviours. Current Biology, 25 (21): 2815-2818.
• Cronk, Q. & I. Ojeda, 2008. Bird-pollinated flowers in an evolutionary and molecular context. Journal of Experimental Botany, 59: 715-727.
• Çölgeçen, H., U. Koca & H.N. Büyükkartal, 2020. “Use of red clover (Trifolium pratense L.) seeds in human therapeutics, 421-427”. In: Nuts and Seeds in Health and Disease Prevention. (Eds. V.R. Preedy & R.R. Watson), Academic Press, Elsevier.
• Esmaeili, A.K., R.M. Taha, S. Mohajer & B. Banisalam, 2015. antioxidant activity and total phenolic and flavonoid content of various solvent extracts from in vivo and in vitro grown Trifolium pratense L. (Red clover). BioMed Research International, 643285.
• Faegri, K. & L. Van Der Pijl, 2013. Principles of Pollination Ecology; Pergamon Press: Oxford, UK.
• Faehnrich, B., C. Franz, P. Nemaz & H.P. Kaul, 2021. Medicinal plants and their secondary metabolites-State of the art and trends in breeding, analytics and use in feed supplementation-with special focus on German chamomile. Journal of Applied Botany and Food Quality, 94: 61-74.
• Farré-Armengol, G., I. Filella, J. Llusià & J. Peñuelas, 2017. βOcimene, a key floral and foliar volatile involved in multiple interactions between plants and other organisms. Molecules, 22: 1148.
• Farré-Armengol, G., M. Fernández-Martínez, I. Filella, R.R. Junker & J. Peñuelas, 2020. Deciphering the biotic and climatic factors that influence floral scents: a systematic review of floral volatile emissions. Frontiers in Plant Science, 11: 1154.
• Fazly Bazzaz, B.S., G. Haririzadeh, S.A. Imami & M.H. Rashed, 1997. Survey of Iranian plants for alkaloids, flavonoids, saponins, and tannins [Khorasan Province]. International Journal of Pharmacognosy, 35 (1): 17-30.
• Ferchichi, N., W. Toukabri, U. Vrhovsek, I. Nouairi, A. Angeli, D. Masuero, R. Mhamdi & D. Trabelsi, 2021. Proximate composition, lipid and phenolic profiles, and antioxidant activity of different ecotypes of Lupinus albus, Lupinus luteus and Lupinus angustifolius. Journal of Food Measurement and Characterization, 15: 1241-1257.
• Fumić, B., M. Jug & M. Zovko Končić, 2019. Optimization of ultrasound-assisted extraction of phenolic antioxidants from Lotus corniculatus. Croatica Chemica Acta, 92 (3): 369-377.
• Gamal-Eldeen, A.M., S.A. Kawashty, L.F. Ibrahim, M.M. Shabana & S.I. El-Negoumy, 2004. Evaluation of antioxidant, anti-inflammatory, and antinociceptive properties of aerial parts of Vicia sativa and its flavonoids. Journal of Natural Remedies, 4 (1): 81-96.
• Guerrieri, A., L. Dong & H.J. Bouwmeester, 2019. Role and exploitation of underground chemical signaling in plants. Pest Management Science, 75: 2455-2463.
• Gupta, Y.P., 1987. Anti-nutritional and toxic factors in food legumes: a review. Plant Foods for Human Nutrition, 37: 201-228.
• Güzel, Y. & G. Özyazıcı, 2021. Adoption of promising fenugreek (Trigonella foenum-graceum L.) genotypes for yield and quality characteristics in the semiarid climate of Turkey. Atmosphere, 12: 1199.
• Hagler, J. & L.S. Buchmann, 1993. Honeybee (Hymenoptera: Apidae) foraging responses to phenolic-rich nectars. Journal of the Kansas Entomological Society, 66: 223-230.
• Hama, J.R., D.B.G. Jorgensen, E. Diamantopoulos, T.D. Bucheli, H.C.B. Hansen & B.W. Strobel, 2022. Indole and quinolizidine alkaloids from blue lupin leach to agricultural drainage water. Science of The Total Environment, 834: 155283.
• Harborne, J.B., 1989. “Methods in plant biochemistry: 1- General procedures and measurement of total phenolics, 1-28”. In: Plant Phenolics. (Ed. J.B. Harborne), Academic Press Limited, Cambridge, MA, USA.
• Harborne, J.B., 2001. Secondary Metabolites: Attracting Pollinators. Encyclopedia of Life Sciences, John Wiley & Sons, Ltd, 5pp.
• Hashemzaei, M., A. Delarami Far, A. Yari, R.E. Heravi, K. Tabrizian, S.M. Taghdisi, S.E. Sadegh, K. Tsarouhas, D. Kouretas, G. Tzanakakis, D. Nikitovic, N.Y. Anisimov, D.A. Spandidos, A.M. Tsatsakis & R. Rezaee, 2017. Anticancer and apoptosis-inducing effects of quercetin in vitro and in vivo. Oncology Reports, 38 (2): 819-828.
• Hatzold, T., I. Elmadfa, R. Gross, M. Wink, T. Hartmann & L. Witte, 1983. Quinolizidine alkaloids in seeds of Lupinus mutabilis. Journal of Agricultural and Food Chemistry, 31 (5): 934-938.
• He, Q., Y. Shen, M. Wang, M. Huang, R. Yang, S. Zhu, L. Wang, Y. Xu & R. Wu, 2011. Natural variation in petal color in Lycoris longituba revealed by anthocyanin components. PLoS One, 6: e22098.
• Horvat, D., M. Viljevac Vuletic, L. Andric, R. Balicevic, M. Kovacevic Babic & M. Tucak, 2022. Characterization of forage quality, phenolic profiles, and antioxidant activity in alfalfa (Medicago sativa L.). Plants, 11: 2735.
• Iqbal, Y., E.N. Ponnampalam, H.A.R. Suleria, J.J. Cottrell & F.R. Dunshea, 2021. LC-ESI/QTOF-MS profiling of chicory and lucerne polyphenols and their antioxidant activities. Antioxidants, 10: 932.
• Isah, T., 2019. Stress and defense responses in plant secondary metabolites production. Biological Research, 52: 39.
• Jamieson, M.A., L.A. Burkle, J.S. Manson, J.B. Runyon, A.M. Trowbridge & J. Zientek, 2017. Global change effects on plant–insect interactions: the role of phytochemistry. Current Opinion in Insect Science, 23: 70-80.
• Jia, K., L. Baz & S. Al-babili, 2018. From carotenoids to strigolactones. Journal of Experimental Botany, 69: 2189-2204.
• Joshi, A.S., P. Nagda, S. Bugade & S.S. Barve, 2022. Investigation of anti-inflammatory and immunomodulatory effects of methanolic extracts of fenugreek leaves and seeds to justify its use in topical creams for preventing inflammation and joint-pain. International Journal of Agro Nutrifood Practices, 2 (3): 9-15.
• Kazlauskaite, J.A., I. Matulyte, M. Marksa, R. Lelesius, A. Pavilonis & J. Bernatoniene, 2023. Application of antiviral, antioxidant and antibacterial Glycyrrhiza glabra L., Trifolium pratense L. extracts and Myristica fragrans Houtt. essential oil in microcapsules. Pharmaceutics, 15 (2): 464.
• Kekillioğlu, A. & Ö.E. Bostan, 2023. Polinatör Hymenopterler (Arthropoda: Insecta). Uluslararası İleri Doğa Bilimleri ve Mühendislik Araştırmaları Dergisi, 7 (6): 402-409.
• Kessler, D., S. Bhattacharya, C. Diezel, E. Rothe, K. Gase, M. Schöttner & I.T. Baldwin, 2012. Unpredictability of nectar nicotine promotes outcrossing by hummingbirds in Nicotiana attenuata. Plant Journal, 71 (4): 529-538.
• Koch, H. & P.C. Stevenson, 2017. Do linden trees kill bees? Reviewing the causes of bee deaths on silver linden (Tilia tomentosa). Biology Letters, 13: 20170484.
• Koch, H., J. Woodward, M.K. Langat, M.J.F. Brown & P.C. Stevenson, 2019. Flagellum removal by a nectar metabolite inhibits infectivity of a bumblebee parasite. Current Biology, 29 (20): 3494-3500.
• Kordan, B., K. Dancewicz, A. Wroblewska & B. Gabrys, 2012. Intraspecific variation in alkaloid profile of four lupine species with implications for the pea aphid probing behaviour. Phytochemistry Letters, 5 (1): 71-77.
• Ku, Y.S., C.A. Contador, M.S. Ng, J. Yu, G. Chung & H.M. Lam, 2020. The effects of domestication on secondary metabolite composition in legumes. Frontiers in Genetics, 11: 581357.
• Lampart-Szczapa, E., J. Korczak, M. Nogala-Kalucka & R. Zawirska-Wojtasiak, 2003. Antioxidant properties of lupin seed products. Food Chemistry, 83: 279-285.
• Lane, G.A., O.R.W. Sutherland & R.A. Skipp, 1987. Isoflavonoids as insect feeding deterrents and antifungal components from root of Lupinus angustifolius. Journal of Chemical Ecology, 13: 771-783.
• Lee, K.J., J.R. Lee, H.J. Kim, S. Raveendar, G.A. Lee, Y.A. Jeon, E. Park, K.H. Ma, S.K. Lee & J.W. Chung, 2017. Comparison of flavonoid contents and antioxidant activities of Vicia species. Plant Genetic Resources, 15 (2): 119-126.
• Liu, D.L. & J.V. Lovett, 1993. Biologically active secondary metabolites of barley. II. Phytotoxicity of barley allelochemicals. Journal of Chemical Ecology, 19: 2231-2244.
• Liu, Q., J. Li, M. Gu, W. Kong, Z. Lin, J. Mao, M. Zhang, L. Jiang, C. Liu, Y. Wang & J. Liu, 2023. High-throughput phytochemical unscrambling of flowers originating from Astragalus membranaceus (Fisch.) Bge. var. mongholicus (Bge.) P. K. Hsiao and Astragalus membranaceus (Fisch.) Bug. by applying the intagretive plant metabolomics method using UHPLC−Q−TOF− MS/MS. Molecules, 28: 6115.
• London-Shafir, I., S. Shafir & D. Eisikowitch, 2003. Amygdalin in almond nectar and pollen-facts and possible roles. Plant Systematics and Evolution, 238: 87-95.
• Luo, K., M.Z.Z. Jahufer, F. Wu, H. Di, D. Zhang, X. Meng, J. Zhang & Y. Wang, 2016. Genotypic variation in a breeding population of yellow sweet clover (Melilotus officinalis). Frontiers in Plant Science, 7: 972.
• Mardani-Korrani, H., M. Nakayasu, S. Yamazaki, Y. Aoki, R. Kaida, T. Motobayashi, M. Kobayashi, N. Ohkama-Ohtsu, Y. Oikawa, A. Sugiyama & Y. Fujii, 2021. L-canavanine, a root exudate from hairy vetch (Vicia villosa) drastically affecting the soil microbial community and metabolite pathways. Frontiers in Microbiology, 12: 701796.
• Mavromatis, A., I. Nianiou-Obeidat, A. Polidoros, Z. Parissi, E. Tani, M. Irakli, K.A. Aliferis, I. Zafeiriou, P.V. Mylona, E. Sarri, E.A. Papadopoulou, R. Tagiakas, L. Kougiteas, S. Kostoula & E.M. Abraham, 2023. Characterization of lupin cultivars based on phenotypical, molecular and metabolomic analyses. Agronomy, 13: 370.
• Medina, C.M.M., 2022. Effect of arbuscular mycorrhizal fungi inoculation and p-fertilization on terpene emitted from red clover (Trifolium pratense L.) leaf. Doctoral Dissertation, Universidad De La Frontera, Facultad de Ingeniería y Ciencias Doctorado en Ciencias de Recursos Naturales, 108 pp.
• Meena, R., 2020. Secondary metabolites in organic chemistry. International Journal of Multidisciplinary Research in Science, Engineering and Technology, 3 (1): 78-83.
• Megías, C., I. Cortés-Giraldo, J. Girón-Calle, M. Aliaz & J. Vioque, 2018. Characterization of Vicia (Fabaceae) seed water extracts with potential immunomodulatory and cell antiproliferative activities. Journal of Food Biochemistry, 42: e12578.
• Mittall, M., V. Pandey, B. Rathi, H.C. Verma, B.K. Singh, R. Chauhan & S. Kumar, 2023. The nutraceutical nexus: unveiling the complete nutrient solution in one place. European Chemical Bulletin, 12 (Special Issue 5): 6788-6796.
• Modzelewska, A., S. Sur, S.K. Kumar & S.R. Khan, 2005. Sesquiterpenes: natural products that decrease cancer growth. Current Medicinal Chemistry-Anti-Cancer Agents, 5 (5): 477-499.
• Molinu, M.G., L. Sulas, G. Campesi, G.A. Re, F. Sanna & G. Piluzza, 2023. Subterranean clover and sulla as valuable and complementary sources of bioactive compounds for rainfed mediterranean farming systems. Plants, 12: 417.
• Mustard, J.A., 2020. Neuroactive nectar: Compounds in nectar that interact with neurons. Arthropod Plant Interactions, 14: 151-159.
• Naika, M.B.N., N. Sathyanarayanan, R.S. Sajeevan, T. Bhattacharyya, P. Ghosh, M.S. Iyer, M. Jarjapu, A.G. Joshi, K. Harini, K.M. Shafi, N. Kalmankar, S.D. Karpe, B. Mam, S.N. Pasha & R. Sowdhamini, 2022. Exploring the medicinally important secondary metabolites landscape through the lens of transcriptome data in fenugreek (Trigonella foenum graecum L.). Scientific Reports, 12: 13534.
• Neugart, S., S. Rohn & M. Schreiner, 2015. Identification of complex, naturally occurring flavonoid glycosides in Vicia faba and Pisum sativum leaves by HPLC-DAD-ESI-MSn and the genotypic effect on their flavonoid profile. Food Research International, 76: 114-121.
• Nicolson, S.W., 2011. Bee food: The chemistry and nutritional value of nectar, pollen and mixtures of the two. Afr. Zool., 46: 197-204.
• Nicolson, S.W., 2022. Sweet solutions: nectar chemistry and quality. Philosophical Transactions of the Royal Society B, 377 (1853): 20210163.
• Nicolson, S.W., S. Lerch-Henning, M. Welsford & S.D. Johnson, 2015. Nectar palatability can selectively filter bird and insect visitors to coral tree flowers. Evolutionary Ecology, 29: 405-417.
• Ogbole, O.O., O.D. Akin-Ajani, T.O. Ajala, Q.A. Ogunniyi, J. Fettke & O.A. Odeku, 2023. Nutritional and pharmacological potentials of orphan legumes: Subfamily faboideae. Heliyon, 9: e15493.
• Özcan, M.M., F. Aljuhaimi, E.E. Babiker, N. Uslu, D.A. Ceylan, K. Ghafoor, M.M. Özcan, N. Dursun, I.M. Ahmed, F.G. Jamiu & O.N. Alsawmahi, 2019. Determination of antioxidant activity, phenolic compound, mineral contents and fatty acid compositions of bee pollen grains collected from different locations. Journal of Apicultural Science, 63: 69-79.
• Özyazıcı, G., 2020. Responses of sulfur and phosphorus doses on the yield and quality of fenugreek (Trigonella foenum-graecum L.). Applied Ecology and Environmental Research, 18 (5): 7041-7055.
• Özyazıcı, M.A., 2022. “Legume forage crops with medicinal value and their secondary metabolite contents: Medicago sp., Onobrychis sp., Melilotus sp., and Lupinus sp., 33-70”. In: New Development on Medicinal and Aromatic Plants-II. (Ed. G. Özyazıcı), Iksad Publishing House, Ankara, Türkiye.
• Palmer-Young, E.C., I.W. Farrell, L.S. Adler, N.J. Milano, P.A. Egan, R.R. Junker, R.E. Irwin & P.C. Stevenson, 2019. Chemistry of floral rewards: Intra- and interspecific variability of nectar and pollen secondary metabolites across taxa. Ecological Monographs, 89: 1-20.
• Pang, Z., J. Chen, T. Wang, C. Gao, Z. Li, L. Guo, J. Xu & Y. Cheng, 2021. Linking plant secondary metabolites and plant microbiomes: a review. Frontiers in Plant Science, 12: 621276.
• Petrović, M.P., M.S. Stanković, B.S. Anđelković, S.Z. Babić, V.G. Zornić, S.Lj. Vasiljević & Z.P. Dajić-Stevanović, 2016. Quality parameters and antioxidant activity of three clover species in relation to the livestock diet. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 44 (1): 201-208.
• Piasecka, A., N. Jedrzejczak-Rey & P. Bednarek, 2015. Secondary metabolites in plant innate immunity: conserved function of divergent chemicals. New Phytologist, 206: 948-964.
• Platikanov, S., S. Nikolov, D. Pavlova, L. Evstatieva & S. Popov, 2005. Volatiles from four Astragalus species: phenological changes and their chemotaxonomical application. Zeitschrift für Naturforsch C, 60 (7-8): 591-599.
• Quijada, J., C. Fryganas, H.M. Ropiak, A. Ramsay, I. Mueller-Harvey & H. Hoste, 2015. Anthelmintic activities against Haemonchus contortus or Trichostrongylus colubriformis from small ruminants are influenced by structural features of condensed tannins. Journal of Agricultural and Food Chemistry, 63 (28): 6346-6354.
• Quiroz, A., L. Mendez, A. Mutis, E. Hormazabal & F. Ortega, 2017. Antifeedant activity of red clover root isoflavonoids on Hylastinus obscurus. Journal of Soil Science and Plant Nutrition, 17 (1): 231-239.
• Raeeszadeh, M., J. Beheshtipour, R. Jamali & A. Akbari, 2022. The antioxidant properties of alfalfa (Medicago sativa L.) and its biochemical, antioxidant, anti-inflammatory, and pathological effects on nicotine-induced oxidative stress in the Rat Liver. Oxidative Medicine and Cellular Longevity, 2691577.
• Rafińska, K., P. Pomastowski, O. Wrona, R. Górecki & B. Buszewski, 2017. Medicago sativa as a source of secondary metabolites for agriculture and pharmaceutical industry. Phytochemistry Letters, 20: 520-539.
• Richardson, L.L., L.S. Adler, A.S. Leonard, J. Andicoechea, K.H. Regan, W.E. Anthony, J.S. Manson & R.E. Irwin, 2015. Secondary metabolites in floral nectar reduce parasite infections in bumblebees. Proceedings Royal Society B, 282: 20142471.
• Riddick, E.W., 2021. Potential of quercetin to reduce herbivory without disrupting natural enemies and pollinators. Agriculture, 11: 476.
• Robbins, R.J., 2003. Phenolic acids in foods: An overview of analytical methodology. Journal of Agricultural and Food Chemistry, 51: 2866-2887.
• Ruiz-López, M.A., L. Barrientos-Ramírez, P.M. García-López, E.H. Valdés-Miramontes, J.F. Zamora-Natera, R. Rodríguez-Macias, E. Salcedo-Pérez, J. Bañuelos-Pineda & J.J. Vargas-Radillo, 2019. Nutritional and bioactive compounds in Mexican lupin beans species: a mini-review. Nutrients, 11: 1785.
• Saleem, M., M. Karim, M.I. Qadir, B. Ahmed, M. Rafiq & B. Ahmad, 2014. In vitro antibacterial activity and phytochemical analysis of hexane extract of Vicia sativa. Bangladesh Journal of Pharmacology, 9 (2): 189-193.
• Salehi, B., I.M. Abu-Reidah, F. Sharopov, N. Karazhan, J. Sharifi-Rad, M. Akram, M. Daniyal, F.S. Khan, W. Abbaass & R. Zainab, 2021. Vicia plants-a comprehensive review on chemical composition and phytopharmacology. Phytotherapy Research, 35 (2): 790-809.
• Schmitt, A., R. Roy & C.J. Carter, 2021. Nectar antimicrobial compounds and their potential effects on pollinators. Current Opinion in Insect Science, 44: 55-63.
• Seigler, D.S., 1998. Plant Secondary Metabolism. Springer New York, NY, 759pp.
• Singaravelan, N., M. Inbar, G. Ne'eman, M. Distl, M. Wink & I. Izhaki, 2006. The effects of nectar-nicotine on colony fitness of caged honeybees. Journal of Chemical Ecology, 32: 49-59.
• Singaravelan, N., G. Nee'man, M. Inbar & I. Izhaki, 2005. Feeding responses of free-flying honeybees to secondary compounds mimicking floral nectars. Journal of Chemical Ecology, 31 (12): 2791-2804.
• Slavković, F. & A. Bendahmane, 2023. Floral phytochemistry: impact of volatile organic compounds and nectar secondary metabolites on pollinator behavior and health. Chemistry & Biodiversity, 20: e202201139.
• Sowa, P., M. Tarapatskyy, C. Puchalski, W. Jarecki & M. Dżugan, 2019. A novel honey-based product enriched with coumarin from Melilotus flowers. Journal of Food Measurement and Characterization, 13: 1748-1754.
• Stambolov, I., A. Shkondrov & I. Krasteva, 2023. Astragalus glycyphyllos L.: phytochemical constituents, pharmacology, and biotechnology. Pharmacia, 70 (3): 635-641.
• Stevenson, P.C., S.W. Nicolson & G.A. Wright, 2017. Plant secondary metabolites in nectar: impacts on pollinators and ecological functions. Functional Ecology, 31 (1): 65-75.
• Tava, A., L. Pecio, A. Stochmal & L. Pecetti, 2015. Clovamide and flavonoids from leaves of Trifolium pratense and T. pratense subsp. nivale grown in Italy. Natural Product Communications, 10: 933-936.
• Tiring, G., S. Satar & O. Özkaya, 2021. Sekonder metabolitler. Bursa Uludağ Üniversitesi Ziraat Fakültesi Dergisi, 35 (1): 203-215.
• Tiwari, R. & C.S. Rana, 2015. Plant secondary metabolites: a review. International Journal of Engineering Research and General Science, 3 (5): 661-670.
• Trigo, J.R., 2011. Effects of pyrrolizidine alkaloids through different trophic levels. Phytochemistry Reviews, 10: 83-98.
• Tundis, R., M. Marrelli, F. Conforti, M.C. Tenuta, M. Bonesi, F. Menichini & M.R. Loizzo, 2015. Trifolium pratense and T. repens (Leguminosae): Edible Flower Extracts as Functional Ingredients. Foods, 4: 338-348.
• Tuominen, A., E. Toivonen, P. Mutikainen & J.P. Salminen, 2013. Defensive strategies in Geranium sylvaticum. Part 1: Organ-specific distribution of water-soluble tannins, flavonoids and phenolic acids. Phytochemistry, 95: 394-407.
• Ullrich, C.I., R. Aloni, M.E.M. Saeed, W. Ullrich & T. Efferth, 2019. Comparison between tumors in plants and human beings: mechanisms of tumor development and therapy with secondary plant metabolites. Phytomedicine, 64: 153081.
• Vannette, R.L. & T. Fukami, 2016. Nectar microbes can reduce secondary metabolites in nectar and alter effects on nectar consumption by pollinators. Ecology, 97 (6): 1410-1419.
• Verónica, C.S., F.M. de los Ángeles, R.G. Claudio & S.M. Fernanda, 2014. Analysis of phenolic compounds in onion nectar by miniaturized off-line solid phase extraction-capillary zone electrophoresis. Analytical Methods, 6: 4878-4884.
• Vioque, J., J. Giron-Calle, V. Torres-Salas, Y. Elamine & M. Alaiz, 2020. Characterization of Vicia ervilia (bitter vetch) seed proteins, free amino acids, and polyphenols. Journal of Food Biochemistry, 44 (7): e13271.
• Vlaisavljević, S., B. Kaurinović, M. Popović, M. Djurendić-Brenesel, B. Vasiljević, D. Cvetković & S. Vasiljević, 2014. Trifolium pratense L. as a potential natural antioxidant. Molecules, 19 (1): 713-725.
• Vlaisavljević, S., B. Kaurinović, M. Popović, & S. Vasiljević, 2017. Profile of phenolic compounds in Trifolium pratense L. extracts at different growth stages and their biological activities. International Journal of Food Properties, 20 (12): 3090-3101.
• Wallace, R.J., 2004. Antimicrobial properties of plant secondary metabolites. Proceedings of the Nutrition Society, 63: 621-629.
• Wink, M., 2013. Evolution of secondary metabolites in legumes (Fabaceae). South African Journal of Botany, 89: 164-175.
• Wink, M., 2018. Plant secondary metabolites modulate insect behavior-steps toward addiction?. Frontiers in Physiology, 9: 364.
• Wink, M., 2019. Quinolizidine and pyrrolizidine alkaloid chemical ecology – a mini-review on their similarities and differences. Journal of Chemical Ecology, 45: 109-115.
• Wink, M., 2020. “Evolution of the angiosperms and co-evolution of secondary metabolites, especially of alkaloids, 151-174”. In: Co-Evolution of Secondary Metabolites. (Eds. J.M. Mérillon & K.G. Ramawat), Reference Series in Phytochemistry, Springer, Cham.
• Wu, F., Z. Duan, P. Xu, Q. Yan, M. Meng, M. Cao, C.S. Jones, X. Zong, P. Zhou, Y. Wang, K. Luo, S. Wang, Z. Yan, P. Wang, H. Di, Z. Ouyang, Y. Wang & J. Zhang, 2021. Genome and systems biology of Melilotus albus provides insights into coumarins biosynthesis. Plant Biotechnology Journal, 20 (3): 592.
• Yang, L., K.S. Wen, X. Ruan, Y.X. Zhao, F. Wei & Q. Wang, 2018. Response of plant secondary metabolites to environmental factors. Molecules, 23: 762.
• Yang, Y., M. Liu, K. Wang, Y. Yang, N. Su, W. Huang & Y. Wu, 2020. Chemical and cytological evaluation of honeybee pollen antioxidant ability. Journal of Food Science, 85: 824-833.
• Yerlikaya, S., M.C. Baloglu, A. Diuzheva, J. Jekő, Z. Cziáky & G. Zengin, 2019. Investigation of chemical profile, biological properties of Lotus corniculatus L. extracts and their apoptotic-autophagic effects on breast cancer cells. Journal of Pharmaceutical and Biomedical Analysis, 174: 286-299.
• Zagrobelny, M. & B.L. Møller, 2011. Cyanogenic glucosides in the biological warfare between plants and insects: the burnet moth-birdsfoot trefoil model system. Phytochemistry, 72: 1585-1592.
• Zhang, J., Z. Wang, P. Wen, Y. Qu, K. Tan & J.C. Nieh, 2018. The reluctant visitor: A terpenoid in toxic nectar can reduce olfactory learning and memory in Asian honey bees. The Journal of Experimental Biology, 221: jeb.168344.