Influence of arbuscular mycorrhizal fungi on the nematicidal properties of leaf extracts of Thymus vulgaris L.

Open access

Abstract

The effect of arbuscolar mycorrhizal fungi (AMF) on the nematicidal activity of Thymus vulgaris against the rootknot nematodes Meloidogyne incognita and M. javanica was investigated in two in vitro experiments. In the first experiment egg masses of M. incognita and M. javanica were immersed for 3 weeks in aqueous leaf extracts of thyme plants non-inoculated or previously inoculated with Glomus mosseae or mixed AMF strains (Sclerocystis sinuosa, Glomus claroideum-1, G. claroideum-2 and G. claroideum-3). Thereafter the hatching test continued in distilled water for five more weeks. In the second experiment egg masses of both Meloidogyne species were exposed to the different thyme extracts for 4, 8 and 16 hours and then incubated in distilled water for 8 weeks. Distilled water and 5 mg/ml aqueous solution of fenamiphos nematicide were used as controls. Numbers of second stage juveniles emerging weekly were expressed as cumulative percentages of the total egg content of the egg masses. In the first experiment juvenile emergence from eggs of both Meloidogyne species immersed in thyme extracts for three weeks was completely suppressed since the first week. Hatching of eggs of M. incognita in all the extracts was significantly lower than that in water control, although emergence in the extract from uninoculated thyme plants was significantly higher than the others and no statistical different from that of aqueous fenamiphos solution. Emergence of M. javanica juveniles was significantly lower after immersion in all the extracts than in distilled water control and aqueous fenamiphos solution. In the second experiment a 4-hour exposure to the extract from thyme inoculated with G. mosseae and mixed AMF population significantly reduced the final hatch of M. incognita in comparison to distilled water. A 16-hour exposure to the extract from mixed AMF inoculated plants resulted in a significantly lower egg hatch than the shorter exposure times, whereas no statistical difference was found between 4 and 8 hour exposure to both extracts. Emergence of M. javanica juveniles was statistically lower than in water only after 16 hours exposure to the extracts from mixed AMF strains inoculated plants, but no difference was found among the different exposure times. Growth of T. vulgaris was significantly increased only by the infections of mixed AMF strains.

If the inline PDF is not rendering correctly, you can download the PDF file here.

  • [1] Aballay E. Insunza V. (2002): Evaluation of plants with nematicidal properties in the control Xiphinema index on table grapes cv. Thompson seedless in the central zone of Chile. Agric. Tec. 62: 357–365

  • [2] Aballay E. Flores P. Insunza V. (2001): Nematicidal effect of eight plant species on Xiphinema americanum sensu lato in Vitis vinifera var. Cabernat Sauvignon in Chile. Nematropica 31: 95–102

  • [3] Aballay E. Sepulveda R. Insunza V. (2004): Evaluation of five nematode antagonistic plants used as green manure to control Xiphinema index Thorne et Allen on Vitis vinifera L. Nematropica 34: 45–51

  • [4] Akiyama K. Hayashi H. (2002): Arbuscular mycorrhizal fungus promoted accumulation of two new triterpenoids in cucumber roots. Biosci. Biotechnol. Biochem. 66:762–769. DOI: 10.1271/bbb.66.762 http://dx.doi.org/10.1271/bbb.66.762

  • [5] Angelini L. G. Carpanese G. Cioni P. L. Morelli I. Macchia M. Flamini G. (2003): Essential Oils from Mediterranean Lamiaceae as Weed Germination Inhibitors. J. Agric. Food Chem. 51(21): 6158–6164. DOI: 10.1021/jf0210728 http://dx.doi.org/10.1021/jf0210728

  • [6] Calvet C. Pinochet J. Camprubi A. Estaún V. Rodríguez-Kabana R. (2001): Evaluation of natural chemical compounds against root-lesion and root-knot nematodes and side-effects on the infectivity of arbuscular mycorrhizal fungi. Eur. J. Plant Pathol. 107: 601–605. DOI: 10.1023/A:1017954315942 http://dx.doi.org/10.1023/A:1017954315942

  • [7] Chatterjee A. Sukul. N. C. Laskar S. Ghoshmajumdar S. (1982): Nematicidal principles from two species of Lamiaceae. J. Nematol. 14: 118–120

  • [8] Chitwood D. J. (2002): Phytochemical based strategies for nematode control. Annu. Rev. Phytopathol. 40: 221–249. DOI: 10.1146/annutev.phyto.40.032602.130045 http://dx.doi.org/10.1146/annurev.phyto.40.032602.130045

  • [9] Copetta A. Lingua G. Berta G. (2006): Effects of three AM fungi on growth distribution of glandular hairs and essential oil production in Ocimum basilicum L. Var. Genovese. Mycorrhiza 16: 485–494. DOI: 10.1007/S00 572-006-0065-6 http://dx.doi.org/10.1007/s00572-006-0065-6

  • [10] Daferera D. J. Ziogas B. N. Polissiou M. G. (2000): GC-MS analysis of essential oils from some Greek aromatic plants and their fungitoxicity on Penicillium digitatum. J. Agric. Food Chem. 48(6): 2576–2581. DOI: 10.1021/jf990835x http://dx.doi.org/10.1021/jf990835x

  • [11] Daferera D. J. Ziogas B. N. Polissiou M. G. (2003): The effectiveness of plant essential oils on the growth of Botrytis cinerea Fusarium sp. and Clavibacter michiganensis subsp. michiganensis. Crop Prot. 22: 39–44. DOI: 10.1016/S0261-2194(02)00095-9 http://dx.doi.org/10.1016/S0261-2194(02)00095-9

  • [12] Duke J. A. James L. F. Keeler R. F. Bailey E. M. Cheeke P. R. Hegarty M. P. (1992): Biting the biocide bullet. In: Duke J. A. Keeler R. F. Bailey E. M. Cheeke P. R. Hegarty M. P. (Eds.) Proceedings of the Third International Symposium “Poisonous Plants”. Iowa State University Press Ames USA 474–478

  • [13] Freitas M. S. M. Martins M. A. Curcino Vieira I. J. (2004): Yield and quality of essential oils of Mentha arvensis in response to inoculation with arbuscular mycorrhizal fungi. Pesqui. Agropecu. Bras. 39: 887–894

  • [14] Gerdemann J. W. Nicolson T. H. (1963): Spores of mycorrhizal Endogone species extracted from soil by wet sieving and decanting. Trans. Br. Mycol. Soc. 46: 235–244 http://dx.doi.org/10.1016/S0007-1536(63)80079-0

  • [15] Greco N. Thomason I. J. (1980): Effect of phenamiphos on Heterodera schachtii and Meloidogyne javanica. J. Nematol. 12: 91–96

  • [16] Guerrieri E. Lingua G. Digilio M. C. Massa N. Berta G. (2004): Do interactions between plant roots and the rhizosphere affect parasitoid behaviour? Ecol. Entomol. 29: 753–756 http://dx.doi.org/10.1111/j.0307-6946.2004.00644.x

  • [17] Gupta M. L. Prasad A. Ram M. Kumar S. (2002): Effect of the vesicular-arbuscular mycorrhizal (VAM) fungus Glomus fasciculatum on the essential oil yield related characters and nutrient acquisition in the crops of different cultivars of menthol mint (Mentha arvensis) under field conditions. Bioresour. Technol. 81: 77–79. DOI: 10.1016/S0960-8524(01)00109-2 http://dx.doi.org/10.1016/S0960-8524(01)00109-2

  • [18] Hussey R. S. Barker K. R. (1973): A comparison of methods of collecting inocula of Meloidogyne spp. including a new technique. Plant Dis. Rep. 57 1025–1028

  • [19] Insunza V. Aballay E. Macaya J. (2001a): Nematicidal activity of aqueous plant extracts on Xiphinema index. Nematol. Mediterr. 29: 35–40

  • [20] Insunza V. Aballay E. Macaya J. (2001b): In vitro nematicidal activity of aqueous plant extracts on clilean populations of Xiphinema americanum sensu lato. Nematropica 31: 47–54

  • [21] Isman M. B. (2000): Plant essential oils for pest and disease management. Crop Protection 19: 603–608. DOI: 10.1016/S0261-2194(00)00079-x http://dx.doi.org/10.1016/S0261-2194(00)00079-X

  • [22] Janssen A. M. Sheffer J. J. C. Baerheim Svendsen A. (1987): Antimicrobial activity of essential oils: A 1976- 1986 literature review: aspects of the test methods. Planta Med. 53: 395–398 http://dx.doi.org/10.1055/s-2006-962755

  • [23] Khaliq A. Janardhanan K. K. (1997): Influence of vesicular arbuscular mycorrhizal fungi on the productivity of cultivated mints. J. Med. Arom. Plant Sci. 19: 7–10

  • [24] Khaosaad T. Vierheilig H. Nell M. Zitterleglseer K. Novak J. (2006): Arbuscular mycorrhiza alters the concentration of essential oils in oregano (Origanum sp. Lamiaceae). Mycorrhiza 16(6) 443–446. DOI: 10.1007/S00572-006-0062-9 http://dx.doi.org/10.1007/s00572-006-0062-9

  • [25] Korayem A. M. Hasabo S. A Ameen H. H. (1993): Effects and mode of action of some plant extracts on certain plant parasitic nematodes. Anz. Schaedl.-Kde. Pfl.-Schutz Umweltschutz 66(2): 32–36

  • [26] Kurita N. Miyaji M. Kurane R. Takahara Y. (1981): Antifungal activity of components of essential oils. Agric. Biol. Chem. 45: 945–952

  • [27] Mago P. Mukerji K. G. (1994): Vesicular arbuscular mycorrhizae in Lamiaceae: I. Seasonal variation in some members. Phytomorphology 44(1–2): 83–88

  • [28] Marschner H. (1997): The Soil-Root Interface (Rhizosphere) in Relation to Mineral Nutrition. In: Marschner H. (Ed.) Mineral nutrition of higher plants. Academic Press London pp. 537–594

  • [29] Müller-Riebau F. Berger B. Yegen O. (1995): Chemical composition and fungitoxic properties to phytopathogenic fungi of essential oils of selected aromatic plants growing wild in Turkey. J. Agric. Food Chem. 43: 2262–2266 http://dx.doi.org/10.1021/jf00056a055

  • [30] Noling J. W. Becker J. O. (1994): The challenge of research and extension to define and implement alternatives to methyl bromide. 1994. J. Nematol. 26: 573–586

  • [31] Oka Y. Nacar S. Putievsky E. Ravid U. Yaniv Z. Spiegel Y. (2000): Nematicidal activity of essential oils and their components against the root-knot nematode. Phytopathology 90: 710–715. DOI: 10.1094/PHYTO.20 00.90.7.710 http://dx.doi.org/10.1094/PHYTO.2000.90.7.710

  • [32] Pandey R. Kalra A. Tandon S. Mehrotra N. Singh H. N. Kumar S. (2000): Essential oils as potent sources of nematicidal compounds. J. Phytopathology 148: 501–502. DOI: 10.1046/j.1439-0434.2000.00493.x http://dx.doi.org/10.1046/j.1439-0434.2000.00493.x

  • [33] Panizzi L. Flamini G. Cioni P. L. Morelli I. (1993): Composition and antimicrobial properties of essential oils of four Mediterranean Lamiaceae. J. Ethnopharmacol. 39(3): 167–170 http://dx.doi.org/10.1016/0378-8741(93)90032-Z

  • [34] Paster N. Juven B. J. Shaaya E. Menasherov M. Nitzan R. Weisslowicz H. Ravid U. (1990): Inhibitory effect of oregano and thyme essential oils on moulds and foodborne bacteria. Lett. Appl. Microbiol. 11: 33–37 http://dx.doi.org/10.1111/j.1472-765X.1990.tb00130.x

  • [35] Phillips J. M. Hayman D. S. (1970): Improved procedures for clearing roots and staining parasitic and VAM fungi for rapid assessment of infection. Trans. Brit. Mycol. Soc. 55 158–161 http://dx.doi.org/10.1016/S0007-1536(70)80110-3

  • [36] Plenchette C. Fortin J. A. Furlan V. (1983): Growth responses of several plant species to mycorrhizae in a soil of moderate P-fertility. I. Mycorrhizal dependency under field conditions. Plant Soil 70 199–209 http://dx.doi.org/10.1007/BF02374780

  • [37] Reddy M. V. B. Angers P. Gosselin A. Arul J. (1998): Characterization and use of essential oil from Thymus vulgaris against Botrytis cinerea and Rhizopus stolonifer in strawberry fruits. Phytochemistry 47: 1515–1520. DOI: 10.1016/S0031-9422(97)00795-4 http://dx.doi.org/10.1016/S0031-9422(97)00795-4

  • [38] Regnault-Roger C. Hamraoul A. Holeman M. Theron E. Pinel R. (1993): Insecticidal effect of essential oils from Mediterranean plants upon Acanthoscelides obtectus Say (Coleoptera Bruchidae) a pest of kidney bean (Phaseolus vulgaris L.). J. Chem. Ecol. (USA) 19(6): 1233–1244 http://dx.doi.org/10.1007/BF00987383

  • [39] Rustaiyan A. Masoudi S. Moufared A. Kamalinejad M Lajevardi T. Sedaghat S. Yari M. (2000): Volatile constituents of three Thymus species grown wild in Iran. Planta Med. 66: 197–198

  • [40] Ryan M.F. Byrne O. (1988): Plant-insect coevolution and inhibition of aceylcholinesterase. J. Chem. Ecol. 14: 1965–1975 http://dx.doi.org/10.1007/BF01013489

  • [41] Sasanelli N. di Vito M. (1991): The effect of Tagetes spp. on the hatching of an Italian population of Globodera rostochiensis. Nematol. mediterr. 19: 135–137

  • [42] Sieverding E. (1991): Vesicular-Arbuscular Mycorrhiza Management in Tropical Agrosystems. Eschborn pp. 52–54

  • [43] Smith S.E. Read D.J. (1997): Mycorrhizal symbiosis 2nd edn. Academic Press London

  • [44] Soler-Serratosa N. Kokalis-Burelle N. Rodriguez-Kabana R. Weaver C.F. King P.S. (1996): Allelochemicals for control of plant-parasitic nematodes. 1. In vivo nematicidal efficacy of thymol and thymol/benzaldeyde combinations. Nematropica 26: 57–71

  • [45] Takács T. Vörös I. (2003): Role of the arbuscular mycorrhizal fungi in the water and nutrient supply of their host plant. (In Hungarian) Növénytermelés. 52 583–593

  • [46] Trouvelot A. Kough J. L. Gianinazzi-Pearson V. (1986): Mesure du Taux de mycorrhization VA d’un systeme radiculaire. In 1er Symposium Europeen sur les Mycorrhizes. INRA Paris pp. 217–221

  • [47] Tsao R. Yu O. (2000): Nematicidal activity of monoterpenoid compounds against economically important nematodes in agriculture. J. Essential Oil Res. 12: 350–354

  • [48] Tworkoski T. (2002): Herbicide effects of essential oils. Weed Sci. 50: 425–431 http://dx.doi.org/10.1614/0043-1745(2002)050[0425:HEOEO]2.0.CO;2

  • [49] Zambonelli A. D’aulerio A. Z. Severi A. Benvenuti S. Maggi L. Bianchi A. (2004): Chemical composition and fungicidal activity of commercial essential oils of Thymus vulgaris L. J. Essential Oil Res. 16: 69–74

  • [50] Zhu H. H. Yao Q. (2004): Localized and systematic increase of phenols in tomato roots induced by Glomus versiforme inhibits Ralstonia solanacearum. J. Phytopathol. 152: 537–542. DOI: 10.1111/j.1439-0434.2004. 00892.x http://dx.doi.org/10.1111/j.1439-0434.2004.00892.x

Search
Journal information
Impact Factor

IMPACT FACTOR 2018: 0.731
5-year IMPACT FACTOR: 0.634

CiteScore 2018: 0.8

SCImago Journal Rank (SJR) 2018: 0.398
Source Normalized Impact per Paper (SNIP) 2018: 0.554

Target audience: researchers in the field of human, veterinary medicine and natural science
Cited By
Metrics
All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 259 117 7
PDF Downloads 105 67 0