Alkaloids with allelopathic activity are not as well-known as other allelochemicals. Our study revealed that total alkaloids from seeds of the medicinal plant Peganum harmala L. possessed significant growth inhibitory effect on four treated plants, with dicot plants (lettuce and amaranth) being more sensitive than the tested monocot plants (wheat and ryegrass). Further investigation led to the isolation of harmaline and harmine as the main active ingredients in the total alkaloids of P. harmala seeds. Harmaline exerted potent inhibitory effects on seedling growth of treated plants, especially dicots, inhibiting root elongation of lettuce and amaranth by 31% and 47% at a very low concentration (5 μg/mL), whereas harmine exhibited much weaker non-selective inhibitory effect on the plants. Considering the high yield and poor utilization of P. harmala in China, we anticipate that this plant could be exploited as an alternative weed management tool in the future.
References
[1]
Kartal, M.; Altun, M.L.; Kurucu, S. HPLC method for the analysis of harmol, harmalol, harmin and harmaline in the seeds of Peganum harmala L. J. Pharm. Biomed. Anal. 2003, 31, 263–269, doi:10.1016/S0731-7085(02)00568-X.
[2]
Abbott, L.B.; Bettmann, G.T.; Sterling, T.M. Physiology and recovery of african rue (Peganum harmala) seedlings under water-deficit stress. Weed Sci. 2008, 56, 52–57, doi:10.1614/WS-07-094.1.
[3]
Zhao, T.; Wang, Z.T.; Branford-White, C.J.; Xu, H.; Wang, C.H. Classification and differentiation of the genus Peganum indigenous to China based on chloroplast trnL-F and psbA-trnH sequences and seed coat morphology. Plant Biol. (Stuttg). 2011, 13, 940–947, doi:10.1111/j.1438-8677.2011.00455.x.
[4]
Duan, J.A.; Zhou, R.H.; Zhao, S.X.; Wang, M.S.; Che, C.T. Studies on the chemical constituents of Peganum multisectum Maxim II. The alkaloids from seeds and antitumour activity. J. Chin. Pharma. Univ. 1998, 29, 21–23.
[5]
Chatterjee, A.; Ganguly, M. Alkaloidal constituents of Peganum harmala and synthesis of the minor alkaloid deoxyvascinone. Phytochemistry 1968, 7, 307–311, doi:10.1016/S0031-9422(00)86329-3.
[6]
Sharaf, M.; El-Ansari, M.A.; Matlin, S.A.; Saleh, N.A.M. Four flavonoid glycosides from Peganum harmala. Phytochemistry 1997, 44, 533–536.
[7]
Movafeghi, A.; Abedini, M.; Fathiazad, F.; Aliasgharpour, M.; Omidi, Y. Floral nectar composition of Peganum harmala L. Nat. Prod. Res. 2009, 23, 301–308, doi:10.1080/14786410802076291.
[8]
Xing, M.; Shen, F.; Liu, L.; Chen, Z.; Guo, N.; Wang, X.; Wang, W.; Zhang, K.; Wu, X.; Wang, X.; et al. Antimicrobial efficacy of the alkaloid harmaline alone and in combination with chlorhexidine digluconate against clinical isolates of Staphylococcus aureus grown in planktonic and biofilm cultures. Lett. Appl. Microbiol. 2012, 54, 475–482, doi:10.1111/j.1472-765X.2012.03233.x.
[9]
Herraiz, T.; Gonzaleza, D.; Ancin-Azpilicuetac, C.; Aranb, V.J.; Guillena, H. β-Carboline alkaloids in Peganum harmala and inhibition of human monoamine oxidase (MAO). Food Chem. Toxicol. 2010, 48, 839–845, doi:10.1016/j.fct.2009.12.019.
[10]
Farouk, L.; Laroubi, A.; Aboufatima, R.; Benharref, A.; Chait, A. Evaluation of the analgesic effect of alkaloid extract of Peganum harmala L.: Possible mechanisms involved. J. Ethnopharmacol. 2008, 115, 449–454, doi:10.1016/j.jep.2007.10.014.
[11]
Lamchouri, F.; Settaf, A.; Cherra, Y.; Hassar, M.; Zemzami, M.; Atif, N.; Nadori, E.B.; Zaid, A.; Lyoussi, B. In vitro cell-toxicity of Peganum harmala alkaloids on cancerous cell-lines. Fitoterapia 2000, 71, 50–54, doi:10.1016/S0367-326X(99)00117-3.
[12]
Berrougui, H.; Cordero, M.; Khalil, A.; Hamamouchia, M.; Ettiab, A.; Marhuenda, E.; Herrara, M. Vasorelaxant effects of harmine and harmaline extracted from Peganum harmala L. seeds in isolated rat aorta. Pharmacol. Res. 2006, 54, 150–157, doi:10.1016/j.phrs.2006.04.001.
[13]
Sodaeizadeh, H.; Rafieiolhossaini, M.; Havlik, J.; Damme, P.V. Allelopathic activity of different plant parts of Peganum harmala L. and identification of their growth inhibitors substances. Plant Growth Regul. 2009, 59, 227–236, doi:10.1007/s10725-009-9408-6.
[14]
Inderjit; Nilsen, E.T. Bioassays and field studies for allelopathy in terrestrial plants: Progress and problems. Crit. Rev. Plant Sci. 2003, 22, 221–238, doi:10.1080/713610857.
[15]
Callaway, R.M.; Aschehoug, E.T. Invasive plants versus their new and old neighbors: A mechanism for exotic invasion. Science 2000, 290, 521–523, doi:10.1126/science.290.5491.521.
[16]
Shao, H.; Huang, X.; Wei, X.; Zhang, C. Phytotoxic effects and a phytotoxin from the invasive plant Xanthium italicum Moretti. Molecules 2012, 17, 4037–4046, doi:10.3390/molecules17044037.
[17]
Shanab, S.M.M.; Shalaby, E.A.; Lightfoot, D.A.; El-Shemy, H.A. Allelopathic effects of water hyacinth (Eichhornia crassipes). 2010, 5, e13200, doi:10.1371/journal.pone.0013200.
[18]
Blair, A.C.; Nissen, S.J.; Brunk, G.R.; Hufbauer, R.A. A lack of evidence for an ecological role of the putative allelochemical (+/？)-catechin in spotted knapweed invasion success. J. Chem. Ecol. 2006, 32, 2327–2331, doi:10.1007/s10886-006-9168-y.
[19]
Gibson, D.M.; Krasnoff, S.B.; Biazzo, J.; Milbrath, L. Phytotoxicity of antofine from invasive swallow-worts. J. Chem. Ecol. 2011, 37, 871–879, doi:10.1007/s10886-011-9994-4.
[20]
Ens, E.J.; French, K.; Bremner, J.B. Evidence for allelopathy as a mechanism of community composition change by an invasive exotic shrub, Chrysanthemoides monilifera spp. rotundata. Plant Soil 2009, 316, 125–137, doi:10.1007/s11104-008-9765-3.
[21]
Bhowmik, P.C.; Inderjit. Challenges and opportunities in implementing allelopathy for natural weed management. Crop. Prot. 2003, 22, 661–671, doi:10.1016/S0261-2194(02)00242-9.
[22]
Liu, J.; Hu, H.; Zhao, G. Effects of alkaloid extract from Peganum multisectum on growth and some physiological characteristics of Zea mays seedlings [in Chinese]. Acta Prataculturae Sin. 2007, 1, 75–80.
[23]
Liu, J.; Hu, H.; Wang, X. Study on Allelopathy of aqueous extract from Peganum multisectum (Maxim.) Bobr. on perennial ryegrass (Lolium perenne L.) and its physiological biochemical manifestation[in Chinese]. Acta Agrestia Sin. 2008, 16, 374–379.
[24]
Khan, A.M.; Qureshi, R.A.; Ullah, F.; Gilani, S.A. Phytotoxic effects of selected medicinal plants collected from Margalla Hills, Islamabad Pakistan. J. Med. Plants Res. 2011, 5, 4671–4675.
[25]
Sodaeizadeh, H.; Rafieiolhossaini, M.; van Damme, P. Herbicidal activity of a medicinal plant, Peganum harmala L., and decomposition dynamics of its phytotoxins in the soil. Ind. Crops Prod. 2010, 31, 385–394, doi:10.1016/j.indcrop.2009.12.006.
[26]
Chon, S.U.; Jang, H.G.; Kim, D.K.; Kim, Y.M.; Boo, H.O.; Kim, Y.J. Allelopathic potential in lettuce (Lactuca sativa L.) plants. Sci. Hortic. 2005, 106, 309–317.
[27]
Wang, X.; Geng, Y.; Wang, D.J.; Shi, X.G.; Liu, J.H. Separation and purification of harmine and harmaline from Peganum harmala using pH-zone-refining counter-current chromatography. J. Sep. Sci. 2008, 31, 3543–3547, doi:10.1002/jssc.200800322.
[28]
Macías, F.A.; Lacret, R.; Varela, R.M.; Nogueiras, C.; Molinillo, J.M.G. Isolation and phytotoxicity of terpenes from Tectona grandis. J. Chem. Ecol. 2010, 36, 396–404, doi:10.1007/s10886-010-9769-3.
[29]
Shao, H.; Peng, S.; Wei, X.; Zhang, D.; Zhang, C. Potential allelochemicals from an invasive weed Mikania micrantha H.B.K. J. Chem. Ecol. 2005, 31, 1657–1668, doi:10.1007/s10886-005-5805-0.
[30]
Popovici, J.; Bertrand, C.; Jacquemoud, D.; Bellvert, F.; Fernandez, M.P.; Comte, G.; Piola, F. An allelochemical from myrica gale with strong phytotoxic activity against highly invasive fallopia x bohemica taxa. Molecules 2011, 16, 2323–2333, doi:10.3390/molecules16032323.
[31]
Inderjit; Dakshini, K.M.M. On laboratory bioassays in allelopathy. Bot. Rev. 1995, 61, 28–44, doi:10.1007/BF02897150.
[32]
Inderjit; Weston, L.A. Are laboratory bioassays for allelopathy suitable for prediction of field responses? J. Chem. Ecol. 2000, 26, 2111–2118, doi:10.1023/A:1005516431969.
[33]
Sosa, T.; Valares, C.; Alias, J.C.; Lobon, C. Persistence of flavonoids in Cistus ladanifer soils. Plant Soil 2010, 337, 51–63, doi:10.1007/s11104-010-0504-1.
[34]
Inderjit; Bhowmik, P.C. Sorption of benzoic acid onto soil colloids and its implications for allelopathy studies. Biol. Fert. Soils 2004, 40, 345–348, doi:10.1007/s00374-004-0785-8.
[35]
Jilani, G.; Mahmood, S.; Chaudhry, A.N.; Hassan, I.; Akram, M. Allelochemicals: Sources, toxicity and microbial transformation in soil—A review. Ann. Microbiol. 2008, 58, 351–357, doi:10.1007/BF03175528.
[36]
Zhang, H.; Chen, L.; Hu, Z. Xeromorphic characters in the vegetative organs of Peganum harmala. Acta Phytoeco. Geobot. Sin. 1992, 16, 243–248.
[37]
Asgarpanah, J.; Ramezanloo, F. Chemistry, pharmacology and medicinal properties of Peganum harmala L. Afr. J. Pharm. Pharmacol. 2012, 6, 1573–1580.
[38]
Heap, I.M. The occurrence of herbicide-resistant weeds worldwide. Pestic. Sci. 1997, 51, 235–243, doi:10.1002/(SICI)1096-9063(199711)51:3<235::AID-PS649>3.0.CO;2-N.
[39]
Vyvyan, J.R. Allelochemicals as leads for new herbicides and agrochemicals. Tetrahedron 2002, 58, 1631–1646, doi:10.1016/S0040-4020(02)00052-2.
[40]
Mitchell, G.; Bartlett, D.W.; Fraser, T.E.; Hawkes, T.R.; Holt, D.C.; Townson, J.K.; Wichert, R.A. Mesotrione: A new selective herbicide for use in maize. Pest Manag. Sci. 2001, 57, 120–128, doi:10.1002/1526-4998(200102)57:2<120::AID-PS254>3.0.CO;2-E.
[41]
Grayson, B.T.; Williams, K.S.; Freehauf, P.A.; Pease, R.R.; Ziesel, W.T.; Sereno, R.L.; Reinsfelder, R.E. The physical and chemical properties of the herbicide cinmethylin (SD 95481). Pestic. Sci. 1987, 21, 143–153, doi:10.1002/ps.2780210207.
[42]
Duke, S.O.; Dayan, F.E.; Romangni, J.G.; Rimando, A.M. Natural products as sources of herbicides: current status and future trends. Weed Res. 2000, 40, 99–111, doi:10.1046/j.1365-3180.2000.00161.x.
[43]
Weston, L.A. Utilization of allelopathy for weed management in agroecosystems. Agron. J. 1996, 88, 860–866, doi:10.2134/agronj1996.00021962003600060004x.
