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Food Microbiology and Biotechnology (FMB) | Bioactive compounds and Physiological properties
Nematicidal Activity of Kojic Acid Produced by Aspergillus oryzae against Meloidogyne incognita
1Department of Agricultural Chemistry, Institute of Environmentally Friendly Agriculture, College of Agriculture and Life Sciences, Chonnam National University, Gwangju 61186, Republic of Korea, 2Biological and Genetic Resources Assessment Division, National Institute of Biological Resources, Incheon 22689, Republic of Korea, 3World Institute of Kimchi, an Annex of Korea Food Research Institute, Gwangju 61755, Republic of Korea
Received: March 18, 2016; Accepted: May 11, 2016
J. Microbiol. Biotechnol. 2016; 26(8): 1383-1391
Published August 28, 2016 https://doi.org/10.4014/jmb.1603.03040
Copyright © The Korean Society for Microbiology and Biotechnology.
Abstract
The fungal strain EML-DML3PNa1 isolated from leaf of white dogwood (Cornus alba L.)
showed strong nematicidal activity with juvenile mortality of 87.6% at a concentration of 20%
fermentation broth filtrate at 3 days after treatment. The active fungal strain was identified as
Aspergillus oryzae, which belongs to section Flavi, based on the morphological characteristics
and sequence analysis of the ITS rDNA, calmodulin (CaM), and β-tubulin (BenA) genes. The
strain reduced the pH value to 5.62 after 7 days of incubation. Organic acid analysis revealed
the presence of citric acid (515.0 mg/kg), malic acid (506.6 mg/kg), and fumaric acid
(21.7 mg/kg). The three organic acids showed moderate nematicidal activities, but the mixture
of citric acid, malic acid, and fumaric acid did not exhibit the full nematicidal activity of
the culture filtrate of EML- DML3PNa1. Bioassay-guided fractionation coupled with 1H- and
13C-NMR and EI-MS analyses led to identification of kojic acid as the major nematicidal
metabolite. Kojic acid exhibited dose-dependent mortality and inhibited the hatchability of
M. incognita, showing EC50 values of 195.2 μg/ml and 238.3 μg/ml, respectively, at 72 h postexposure.
These results suggest that A. oryzae EML-DML3PNa1 and kojic acid have potential
as a biological control agent against M. incognita.
Keywords
Meloidogyne incognita, nematicidal activity, kojic acid, Aspergillus oryzae
References
- Abbott W. 1987. A method of computing the effectiveness of an insecticide. J. Am. Mosq. Control Assoc. 3: 302-303.
- Abdel-Rahman FH, Clark S, Saleh MA. 2008. Natural organic compounds as alternative to methyl bromide for nematodes control. J. Environ. Sci. Health B 43: 680-685.
- Aissani N. 2014. Nematicidal, antimicrobial and acaricidal activity of plant secondary metabolites. Degree of European Doctor of Philosophy, University of Cagliari, Cagliari, Italy.
- Aytemir MD, Ozcelik B. 2010. A study of cytotoxicity of novel chlorokojic acid derivatives with their antimicrobial and antiviral activities. Eur. J. Med. Chem. 45: 4089-4095.
- Bansal R, Bajaj A. 2003. Effect of volatile fatty acids on embryogenesis and hatching of Meloidogyne incognita eggs. Nematol. Mediterr. 33: 101-105.
- Blumenthal CZ. 2004. Production of toxic metabolites in Aspergillus niger, Aspergillus oryzae, and Trichoderma reesei:justification of mycotoxin testing in food grade enzyme preparations derived from the three fungi. Regul. Toxicol. Pharmacol. 39: 214-228.
- Browning M, Wallace DB, Dawson C, Alm SR, Amador JA. 2006. Potential of butyric acid for control of soil-borne fungal pathogens and nematodes affecting strawberries. Soil Biol. Biochem. 38: 401-404.
- Burdock GA, Soni MG, Carabin IG. 2001. Evaluation of health aspects of kojic acid in food. Regul. Toxicol. Pharmacol. 33: 80-101.
- Cayrol JC, Djian C, Pijarowski L. 1989. Study of the nematicidal properties of the culture filtrate of the nematophagous fungus Paecilomyces lilacinus. Rev. Nematol. 12: 331-336.
- Djian C, Pijarowski L, Ponchet M, Arpin N, Favre-Bonvin J. 1991. Acetic acid: a selective nematicidal metabolite from culture filtrates of Paecilomyces lilacinus (Thom) Samson and Trichoderma longibrachiatum Rifai. Nematologica 37: 101-112.
- Dong LQ, Zhang KQ. 2006. Microbial control of plant-parasitic nematodes: a five-party interaction. Plant Soil 288: 31-45.
- Glass NL, Donaldson GC. 1995. Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl. Environ. Microbiol. 61:1323-1330.
- Huter OF. 2011. Use of natural products in the crop protection industry. Phytochem. Rev. 10: 185-194.
- Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41: 95-98.
- Hallmann J, Sikora R. 1996. Toxicity of fungal endophyte secondary metabolites to plant parasitic nematodes and soilborne plant pathogenic fungi. Eur. J. Plant Pathol. 102: 155-162.
- Higa Y, Kawabe M, Nabae K, Toda Y, Kitamoto S, Hara T, et al. 2007. Kojic acid-absence of tumor-initiating activity in rat liver, and of carcinogenic and photo-genotoxic potential in mouse skin. J. Toxicol. Sci 32: 143-159.
- Hong SB, Go SJ, Shin HD, Frisvad JC, Samson RA. 2005. Polyphasic taxonomy of Aspergillus fumigatus and related species. Mycologia 97: 1316-1329.
- Hu Y, Zhang W, Zhang P, Ruan W, Zhu X. 2012. Nematicidal activity of chaetoglobosin A produced by Chaetomium globosum NK102 against Meloidogyne incognita. J. Agric. Food Chem. 61: 41-46.
- Hwang SM, Park MS, Kim JC, Jang KS, Choi YH, Choi GJ. 2014. Occurrence of Meloidogyne incognita infecting resistant cultivars and development of an efficient screening method for resistant tomato to the Mi-virulent nematode. Kor. J. Hortic. Sci. Technol. 32: 217-226.
- Kerry BR. 2000. Rhizosphere interactions and the exploitation of microbial agents for the biological control of plant-parasitic nematodes. Annu. Rev. Phytopathol. 38: 423-441.
- Kwok OCH, Plattner R, Weisleder D, Wicklow DT. 1992. A nematicidal toxin from Pleurotus ostreatus NRRL 3526. J. Chem. Ecol. 18: 127-136.
- Lee YS, Naning KW, Nguyen XH, Kim SB, Moon JH, Kim KY. 2014. Ovicidal activity of lactic acid produced by Lysobacter capsici YS1215 on eggs of root-knot nematodes, Meloidogyne incognita. J. Microbiol. Biotechnol. 24: 1510-1515.
- Li GH, Yu ZF, Li X, Wang XB, Zheng LJ, Zhang KQ. 2007. Nematicidal metabolites produced by the endophytic fungus Geotrichum sp. AL4. Chem. Biodivers. 4: 1520-1524.
- Lopez-Llorca LV, Jansson HB. 2006. Fungal parasites of invertebrates: multimodal biocontrol agents, pp. 310-335. In Robson GD, van West P, Gadd GM (eds.). Exploitation of Fungi. Cambridge University Press, Cambridge, UK.
- Manzanilla-Lopez RH, Esteves I, Finetti-Sialer MM, Hirsch PR, Ward E, Devonshire J, Hidalgo-Diaz L. 2013. Pochonia chlamydosporia: advances and challenges to improve its performance as a biological control agent of sedentary endoparasitic nematodes. J. Nematol. 45: 1-7.
- Mayer A, Anke H, Sterner O. 1997. Omphalotin, a new cyclic peptide with potent nematicidal activity from Omphalotus olearius I. Fermentation and biological activity. Nat. Prod. Lett. 10: 25-32.
- Mitkowski NA, Abawi GS. 2003. Root-knot nematodes. The Plant Health Instructor. DOI: 10.1094. PHI-I-2003-0917-01. Revised 2011.
- Nguyen BC, Chompoo J, Tawata S. 2015. Insecticidal and nematicidal activities of novel mimosine derivatives. Molecules 20: 16741-16756
- 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.
- Onkendi EM, Kariuki GM, Marais M, Moleleki LN. 2014. The threat of root-knot nematodes (Meloidogyne spp.) in Africa: a review. Plant Pathol. 63: 727-737.
- Owen NL, Hundley N. 2004. Endophytes - the chemical synthesizers inside plants. Sci. Prog. 87: 79-99.
- Rho HS, Baek HS, Ahn SM, Kim DH, Chang IS. 2008. Synthesis of new anti-melanogenic compounds containing two molecules of kojic acid. Bull. Kor. Chem. Soc. 29: 1569-1571.
- Saruno R, Kato F, Ikeno T. 1979. Kojic acid, a tyrosinase inhibitor from Aspergillus albus. Agric. Biol. Chem. 43: 1337-1338.
- Schulz B, Boyle C, Draeger S, Rommert AK, Krohn K. 2002. Endophytic fungi: a source of novel biologically active secondary metabolites. Mycol. Res. 106: 996-1004.
- Schwarz M, Kopcke B, Weber RWS, Sterner O, Anke H. 2004. 3-Hydroxypropionic acid as a nematicidal principle in endophytic fungi. Phytochemistry 65: 2239-2245.
- Seiber JN, Coats J, Duke SO, Gross AD. 2014. Biopesticides:state of the art and future opportunities. J. Agric. Food Chem. 62: 11613-11619.
- Sharone E, Chet I, Viterbo A, Bar-Eyal M, Nagan H, Samuels GJ, Spiegel Y. 2007. Parasitism of Trichoderma on Meloidogyne javanica and role of the gelatinous matrix. Eur. J. Plant Pathol. 118: 247-258.
- Stadler M, Anke H, Sterner O. 1993. Linoleic acid - the nematicidal principle of several nematophagous fungi and its production in trap-forming submerged cultures. Arch. Microbiol. 160: 401-405.
- Sun J, Wang H, Lu F, Du L, Wang G. 2008. The efficacy of nematicidal strain Syncephalastrum racemosum. Ann. Microbiol. 58: 369-373.
- Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30: 2725-2729.
- Tian B, Yang J, Zhang KQ. 2007. Bacteria used in the biological control of plant-parasitic nematodes: populations, mechanisms of action, and future prospects. FEMS Microbiol. Ecol. 61: 197-213.
- Tian X, Yao Y, Chen G, Mao Z, Wang X, Xie B. 2014. Suppression of Meloidogyne incognita by the endophytic fungus Acremonium implicatum from tomato root galls. Int. J. Pest Manag. 60: 239-245.
- Thompson JD, Gibson TJ, Plewniak F, Jenmougin F, Higgins DG. 1997. The CLUSTAL_X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25: 4876-4882.
- Varga J, Frisvad JC, Samson RA. 2011. Two new aflatoxin producing species, an overview of Aspergillus section Flavi. Stud. Mycol. 69: 57-80.
- Viglierchio DR, Schmitt RV. 1983. On the methodology of nematode extraction from field samples: Baermann funnel modifications. J. Nematol. 15: 438-444.
- Warrior P, Rehberger LA, Beach M, Grau PA, Kirfman GW, Conley JM. 1999. Commercial development and introduction of DiTera, a new nematicide. Pest Manag. Sci. 55: 376-379.
- White TJ, Bruns T, Lee S, Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA gene for phylogenetics, pp. 315-322. In Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds.). PCR Protocols: A Guide to Methods and Applications. Academic Press, San Diego, CA.
- Xiong X, Pirrung MC. 2008. Modular synthesis of candidate indole-based insulin mimics by claisen rearrangement. Org. Lett. 10: 1151-1154.
- Zuckerman BM, Matheny M, Acosta N. 1994. Control of plant-parasitic nematodes by a nematicidal strain of Aspergillus niger. J. Chem. Ecol. 20: 33-43.
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Research article
J. Microbiol. Biotechnol. 2016; 26(8): 1383-1391
Published online August 28, 2016 https://doi.org/10.4014/jmb.1603.03040
Copyright © The Korean Society for Microbiology and Biotechnology.
Nematicidal Activity of Kojic Acid Produced by Aspergillus oryzae against Meloidogyne incognita
Tae Yoon Kim 1, Ja Yeong Jang 1, Sun Jeong Jeon 1, Hye Won Lee 1, Chang-Hwan Bae 2, Joo Hong Yeo 2, Hyang Burm Lee 1, In Seon Kim 1, Hae Woong Park 3 and Jin-Cheol Kim 1*
1Department of Agricultural Chemistry, Institute of Environmentally Friendly Agriculture, College of Agriculture and Life Sciences, Chonnam National University, Gwangju 61186, Republic of Korea, 2Biological and Genetic Resources Assessment Division, National Institute of Biological Resources, Incheon 22689, Republic of Korea, 3World Institute of Kimchi, an Annex of Korea Food Research Institute, Gwangju 61755, Republic of Korea
Received: March 18, 2016; Accepted: May 11, 2016
Abstract
The fungal strain EML-DML3PNa1 isolated from leaf of white dogwood (Cornus alba L.)
showed strong nematicidal activity with juvenile mortality of 87.6% at a concentration of 20%
fermentation broth filtrate at 3 days after treatment. The active fungal strain was identified as
Aspergillus oryzae, which belongs to section Flavi, based on the morphological characteristics
and sequence analysis of the ITS rDNA, calmodulin (CaM), and β-tubulin (BenA) genes. The
strain reduced the pH value to 5.62 after 7 days of incubation. Organic acid analysis revealed
the presence of citric acid (515.0 mg/kg), malic acid (506.6 mg/kg), and fumaric acid
(21.7 mg/kg). The three organic acids showed moderate nematicidal activities, but the mixture
of citric acid, malic acid, and fumaric acid did not exhibit the full nematicidal activity of
the culture filtrate of EML- DML3PNa1. Bioassay-guided fractionation coupled with 1H- and
13C-NMR and EI-MS analyses led to identification of kojic acid as the major nematicidal
metabolite. Kojic acid exhibited dose-dependent mortality and inhibited the hatchability of
M. incognita, showing EC50 values of 195.2 μg/ml and 238.3 μg/ml, respectively, at 72 h postexposure.
These results suggest that A. oryzae EML-DML3PNa1 and kojic acid have potential
as a biological control agent against M. incognita.
Keywords: Meloidogyne incognita, nematicidal activity, kojic acid, Aspergillus oryzae
References
- Abbott W. 1987. A method of computing the effectiveness of an insecticide. J. Am. Mosq. Control Assoc. 3: 302-303.
- Abdel-Rahman FH, Clark S, Saleh MA. 2008. Natural organic compounds as alternative to methyl bromide for nematodes control. J. Environ. Sci. Health B 43: 680-685.
- Aissani N. 2014. Nematicidal, antimicrobial and acaricidal activity of plant secondary metabolites. Degree of European Doctor of Philosophy, University of Cagliari, Cagliari, Italy.
- Aytemir MD, Ozcelik B. 2010. A study of cytotoxicity of novel chlorokojic acid derivatives with their antimicrobial and antiviral activities. Eur. J. Med. Chem. 45: 4089-4095.
- Bansal R, Bajaj A. 2003. Effect of volatile fatty acids on embryogenesis and hatching of Meloidogyne incognita eggs. Nematol. Mediterr. 33: 101-105.
- Blumenthal CZ. 2004. Production of toxic metabolites in Aspergillus niger, Aspergillus oryzae, and Trichoderma reesei:justification of mycotoxin testing in food grade enzyme preparations derived from the three fungi. Regul. Toxicol. Pharmacol. 39: 214-228.
- Browning M, Wallace DB, Dawson C, Alm SR, Amador JA. 2006. Potential of butyric acid for control of soil-borne fungal pathogens and nematodes affecting strawberries. Soil Biol. Biochem. 38: 401-404.
- Burdock GA, Soni MG, Carabin IG. 2001. Evaluation of health aspects of kojic acid in food. Regul. Toxicol. Pharmacol. 33: 80-101.
- Cayrol JC, Djian C, Pijarowski L. 1989. Study of the nematicidal properties of the culture filtrate of the nematophagous fungus Paecilomyces lilacinus. Rev. Nematol. 12: 331-336.
- Djian C, Pijarowski L, Ponchet M, Arpin N, Favre-Bonvin J. 1991. Acetic acid: a selective nematicidal metabolite from culture filtrates of Paecilomyces lilacinus (Thom) Samson and Trichoderma longibrachiatum Rifai. Nematologica 37: 101-112.
- Dong LQ, Zhang KQ. 2006. Microbial control of plant-parasitic nematodes: a five-party interaction. Plant Soil 288: 31-45.
- Glass NL, Donaldson GC. 1995. Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl. Environ. Microbiol. 61:1323-1330.
- Huter OF. 2011. Use of natural products in the crop protection industry. Phytochem. Rev. 10: 185-194.
- Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41: 95-98.
- Hallmann J, Sikora R. 1996. Toxicity of fungal endophyte secondary metabolites to plant parasitic nematodes and soilborne plant pathogenic fungi. Eur. J. Plant Pathol. 102: 155-162.
- Higa Y, Kawabe M, Nabae K, Toda Y, Kitamoto S, Hara T, et al. 2007. Kojic acid-absence of tumor-initiating activity in rat liver, and of carcinogenic and photo-genotoxic potential in mouse skin. J. Toxicol. Sci 32: 143-159.
- Hong SB, Go SJ, Shin HD, Frisvad JC, Samson RA. 2005. Polyphasic taxonomy of Aspergillus fumigatus and related species. Mycologia 97: 1316-1329.
- Hu Y, Zhang W, Zhang P, Ruan W, Zhu X. 2012. Nematicidal activity of chaetoglobosin A produced by Chaetomium globosum NK102 against Meloidogyne incognita. J. Agric. Food Chem. 61: 41-46.
- Hwang SM, Park MS, Kim JC, Jang KS, Choi YH, Choi GJ. 2014. Occurrence of Meloidogyne incognita infecting resistant cultivars and development of an efficient screening method for resistant tomato to the Mi-virulent nematode. Kor. J. Hortic. Sci. Technol. 32: 217-226.
- Kerry BR. 2000. Rhizosphere interactions and the exploitation of microbial agents for the biological control of plant-parasitic nematodes. Annu. Rev. Phytopathol. 38: 423-441.
- Kwok OCH, Plattner R, Weisleder D, Wicklow DT. 1992. A nematicidal toxin from Pleurotus ostreatus NRRL 3526. J. Chem. Ecol. 18: 127-136.
- Lee YS, Naning KW, Nguyen XH, Kim SB, Moon JH, Kim KY. 2014. Ovicidal activity of lactic acid produced by Lysobacter capsici YS1215 on eggs of root-knot nematodes, Meloidogyne incognita. J. Microbiol. Biotechnol. 24: 1510-1515.
- Li GH, Yu ZF, Li X, Wang XB, Zheng LJ, Zhang KQ. 2007. Nematicidal metabolites produced by the endophytic fungus Geotrichum sp. AL4. Chem. Biodivers. 4: 1520-1524.
- Lopez-Llorca LV, Jansson HB. 2006. Fungal parasites of invertebrates: multimodal biocontrol agents, pp. 310-335. In Robson GD, van West P, Gadd GM (eds.). Exploitation of Fungi. Cambridge University Press, Cambridge, UK.
- Manzanilla-Lopez RH, Esteves I, Finetti-Sialer MM, Hirsch PR, Ward E, Devonshire J, Hidalgo-Diaz L. 2013. Pochonia chlamydosporia: advances and challenges to improve its performance as a biological control agent of sedentary endoparasitic nematodes. J. Nematol. 45: 1-7.
- Mayer A, Anke H, Sterner O. 1997. Omphalotin, a new cyclic peptide with potent nematicidal activity from Omphalotus olearius I. Fermentation and biological activity. Nat. Prod. Lett. 10: 25-32.
- Mitkowski NA, Abawi GS. 2003. Root-knot nematodes. The Plant Health Instructor. DOI: 10.1094. PHI-I-2003-0917-01. Revised 2011.
- Nguyen BC, Chompoo J, Tawata S. 2015. Insecticidal and nematicidal activities of novel mimosine derivatives. Molecules 20: 16741-16756
- 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.
- Onkendi EM, Kariuki GM, Marais M, Moleleki LN. 2014. The threat of root-knot nematodes (Meloidogyne spp.) in Africa: a review. Plant Pathol. 63: 727-737.
- Owen NL, Hundley N. 2004. Endophytes - the chemical synthesizers inside plants. Sci. Prog. 87: 79-99.
- Rho HS, Baek HS, Ahn SM, Kim DH, Chang IS. 2008. Synthesis of new anti-melanogenic compounds containing two molecules of kojic acid. Bull. Kor. Chem. Soc. 29: 1569-1571.
- Saruno R, Kato F, Ikeno T. 1979. Kojic acid, a tyrosinase inhibitor from Aspergillus albus. Agric. Biol. Chem. 43: 1337-1338.
- Schulz B, Boyle C, Draeger S, Rommert AK, Krohn K. 2002. Endophytic fungi: a source of novel biologically active secondary metabolites. Mycol. Res. 106: 996-1004.
- Schwarz M, Kopcke B, Weber RWS, Sterner O, Anke H. 2004. 3-Hydroxypropionic acid as a nematicidal principle in endophytic fungi. Phytochemistry 65: 2239-2245.
- Seiber JN, Coats J, Duke SO, Gross AD. 2014. Biopesticides:state of the art and future opportunities. J. Agric. Food Chem. 62: 11613-11619.
- Sharone E, Chet I, Viterbo A, Bar-Eyal M, Nagan H, Samuels GJ, Spiegel Y. 2007. Parasitism of Trichoderma on Meloidogyne javanica and role of the gelatinous matrix. Eur. J. Plant Pathol. 118: 247-258.
- Stadler M, Anke H, Sterner O. 1993. Linoleic acid - the nematicidal principle of several nematophagous fungi and its production in trap-forming submerged cultures. Arch. Microbiol. 160: 401-405.
- Sun J, Wang H, Lu F, Du L, Wang G. 2008. The efficacy of nematicidal strain Syncephalastrum racemosum. Ann. Microbiol. 58: 369-373.
- Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30: 2725-2729.
- Tian B, Yang J, Zhang KQ. 2007. Bacteria used in the biological control of plant-parasitic nematodes: populations, mechanisms of action, and future prospects. FEMS Microbiol. Ecol. 61: 197-213.
- Tian X, Yao Y, Chen G, Mao Z, Wang X, Xie B. 2014. Suppression of Meloidogyne incognita by the endophytic fungus Acremonium implicatum from tomato root galls. Int. J. Pest Manag. 60: 239-245.
- Thompson JD, Gibson TJ, Plewniak F, Jenmougin F, Higgins DG. 1997. The CLUSTAL_X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25: 4876-4882.
- Varga J, Frisvad JC, Samson RA. 2011. Two new aflatoxin producing species, an overview of Aspergillus section Flavi. Stud. Mycol. 69: 57-80.
- Viglierchio DR, Schmitt RV. 1983. On the methodology of nematode extraction from field samples: Baermann funnel modifications. J. Nematol. 15: 438-444.
- Warrior P, Rehberger LA, Beach M, Grau PA, Kirfman GW, Conley JM. 1999. Commercial development and introduction of DiTera, a new nematicide. Pest Manag. Sci. 55: 376-379.
- White TJ, Bruns T, Lee S, Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA gene for phylogenetics, pp. 315-322. In Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds.). PCR Protocols: A Guide to Methods and Applications. Academic Press, San Diego, CA.
- Xiong X, Pirrung MC. 2008. Modular synthesis of candidate indole-based insulin mimics by claisen rearrangement. Org. Lett. 10: 1151-1154.
- Zuckerman BM, Matheny M, Acosta N. 1994. Control of plant-parasitic nematodes by a nematicidal strain of Aspergillus niger. J. Chem. Ecol. 20: 33-43.
