Down-regulation of aflatoxin biosynthetic genes in Aspergillus parasiticus by Heliopsis longipes roots and affinin for reduction of aflatoxin production

References

• Yu, J.; Bhatnagar, D.; Ehrlich, K. C. Aflatoxin Biosynthesis. Rev. Iberoam. Micol. 2002, 19, 191–200.
   PubMedGoogle Scholar
• Yu, J.; Chang, P. K.; Ehrlich, K. C.; Cary, J. W.; Bhatnagar, D.; Cleveland, T. E.; Payne, G. A.; Linz, J. E.; Woloshuk, C. P.; Bennett, J. W. Clustered Pathway Genes in Aflatoxin Biosynthesis. Appl. Environ. Microbiol. 2004, 70, 1253–1262.
   PubMed Web of Science ®Google Scholar
• Caceres, I.; Khoury, A. A.; Khoury, R. E.; Lorber, S.; Oswald, I. P.; Khoury, A. E.; Atoui, A.; Puel, O.; Bailly, J. D. Aflatoxin Biosynthesis and Genetic Regulation: A Review. Toxins (Basel) 2020, 12, 150.
   Web of Science ®Google Scholar
• Yu, J.; Woloshuk, C. P.; Bhatnagar, D.; Cleveland, T. E. Cloning and Characterization of avfA and omtB Genes Involved in Aflatoxin Biosynthesis in Three Aspergillus Species. Gene 2000, 248, 157–167. DOI: https://doi.org/10.1016/S0378-1119(00)00126-8.
   PubMed Web of Science ®Google Scholar
• Chang, P. K. The Aspergillus parasiticus Protein AFLJ Interacts with the Aflatoxin Pathway-Specific Regulator AFLR. Mol. Genet. Genomics 2003, 268, 711–719.
   PubMed Web of Science ®Google Scholar
• Price, M. S.; Yu, J.; Nierman, W. C.; Kim, H. S.; Pritchard, B.; Jacobus, C. A.; Bhatnagar, D.; Cleveland, T. E.; Payne, G. A. The Aflatoxin Pathway Regulator AflR Induces Gene Transcription inside and outside of the Aflatoxin Biosynthetic Cluster. FEMS Microbiol Lett 2006, 255, 275–279. DOI: https://doi.org/10.1111/j.1574-6968.2005.00084.x.
   PubMed Web of Science ®Google Scholar
• Yabe, K.; Nakajima, H. Enzyme Reactions and Genes in Aflatoxin Biosynthesis. Appl. Microbiol. Biotechnol. 2004, 64, 745–755.
   PubMed Web of Science ®Google Scholar
• Roze, L. V.; Hong, S. Y.; Linz, J. E. Aflatoxin Biosynthesis: Current Frontiers. Annu. Rev. Food Sci. Technol. 2013, 4, 293–311.
   PubMed Web of Science ®Google Scholar
• Yu, J. Current Understanding on Aflatoxin Biosynthesis and Future Perspective in Reducing Aflatoxin Contamination. Toxins. (Basel) 2012, 4, 1024–1057.
   PubMed Web of Science ®Google Scholar
• Jahanshiri, Z.; Shams-Ghahfarokhi, M.; Allameh, A.; Razzaghi-Abyaneh, M. Inhibitory Effect of Eugenol on Aflatoxin B 1 Production in Aspergillus parasiticus by Downregulating the Expression of Major Genes in the Toxin Biosynthetic Pathway. World J. Microbiol. Biotechnol. 2015, 31, 1071–1078. DOI: https://doi.org/10.1007/s11274-015-1857-7.
   PubMed Web of Science ®Google Scholar
• Moon, Y. S.; Kim, H. M.; Chun, H. S.; Lee, S. E. Organic Acids Suppress Aflatoxin Production via Lowering Expression of Aflatoxin Biosynthesis-Related Genes in Aspergillus flavus. Food Control 2018, 88, 207–216. DOI: https://doi.org/10.1016/j.foodcont.2018.01.017.
   Web of Science ®Google Scholar
• Buitimea-Cantúa, G. V.; Buitimea-Cantúa, N. E.; del Refugio Rocha-Pizaña, M.; Rosas-Burgos, E. C.; Hernández-Morales, A.; Molina-Torres, J. Antifungal and anti-Aflatoxigenic Activity of Heliopsis longipes Roots and Affinin/Spilanthol against Aspergillus parasiticus by Downregulating the Expression of alfD and aflR Genes of the Aflatoxins Biosynthetic Pathway. J. Environ. Sci. Heal. B 2020a, 55, 210–219. DOI: https://doi.org/10.1080/03601234.2019.1681818.
   PubMed Web of Science ®Google Scholar
• Buitimea-Cantúa, G. V.; Buitimea-Cantúa, N. E.; Rocha-Pizaña, M. D. R.; Hernández-Morales, A.; Magaña-Barajas, E.; Molina-Torres, J. Inhibitory Effect of Capsicum Chinense and Piper nigrum Fruits, Capsaicin and Piperine on Aflatoxins Production in Aspergillus parasiticus by Downregulating the Expression of Afl D, Afl M, Afl R, and Afl S Genes of Aflatoxins Biosynthetic Pathway. J. Environ. Sci. Heal. B 2020b, 55, 835–843. DOI: https://doi.org/10.1080/03601234.2020.1787758.
   PubMed Web of Science ®Google Scholar
• Kim, G.; Lee, S. E. Antifungal and Antiaflatoxigenic Properties of Naphthoquinones toward Aspergillus flavus and Their Mode of Inhibitory Action on Aflatoxin Biosynthesis. Food Control 2021, 119, 107506. DOI: https://doi.org/10.1016/j.foodcont.2020.107506.
   Web of Science ®Google Scholar
• Buitimea-Cantúa, G. V.; Marsch-Martinez, N.; Ríos-Chavez, P.; Méndez-Bravo, A.; Molina-Torres, J. Global Gene Expression Analyses of the Alkamide-Producing Plant Heliopsis longipes Supports a Polyketide Synthase-Mediated Biosynthesis Pathway. PeerJ 2020, 8, e10074. DOI: https://doi.org/10.7717/peerj.10074.
   PubMed Web of Science ®Google Scholar
• Molina-Torres, J.; Salazar-Cabrera, C. J.; Armenta-Salinas, C.; Ramírez-Chávez, E. Fungistatic and Bacteriostatic Activities of Alkamides from Heliopsis longipes Roots: Affinin and Reduced Amides. J. Agric. Food Chem. 2004, 52, 4700–4704.
   PubMed Web of Science ®Google Scholar
• Mell, P.; Grance, T. The NIST Definition of Cloud Computing. Computer Security Division, Information Technology Laboratory, National Institute of Standards and Technology, United States Department of Commerce. National Institute of Standards and Technology, Gaithersburg, 2011; pp. 20899–28930.
   Google Scholar
• Patel, T. K.; Anand, R.; Singh, A. P.; Shankar, J.; Tiwary, B. N. Evaluation of Aflatoxin B1 Biosynthesis in A. flavus Isolates from Central India and Identification of Atoxigenic Isolates. Biotechnol. Bioproc. E. 2014, 19, 1105–1113. DOI: https://doi.org/10.1007/s12257-014-0464-z.
   Web of Science ®Google Scholar
• Cota‐Arriola, O.; Cortez‐Rocha, M. O.; Rosas‐Burgos, E. C.; Burgos‐Hernández, A.; López‐Franco, Y. L.; Plascencia‐Jatomea, M. Antifungal Effect of Chitosan on the Growth of Aspergillus parasiticus and Production of Aflatoxin B1. Polym. Int. 2011, 60, 937–944.
   Web of Science ®Google Scholar
• Ma, J.; Mo, H.; Chen, Y.; Ding, D.; Hu, L. Inhibition of Aflatoxin Synthesis in Aspergillus flavus by Three Structurally Modified Lentinans. Int. J. Mol. Sci. 2014, 15, 3860–3870.
   PubMed Web of Science ®Google Scholar
• Caceres, I.; El Khoury, R.; Medina, Á.; Lippi, Y.; Naylies, C.; Atoui, A.; El Khoury, A.; Oswald, I. P.; Bailly, J.-D.; Puel, O. Deciphering the anti-Aflatoxinogenic Properties of Eugenol Using a Large-Scale q-PCR Approach. Toxins (Basel) 2016, 8, 123.
   Web of Science ®Google Scholar
• Guan, X.; Zhao, Y.; Liu, X.; Shang, B.; Xing, F.; Zhou, L.; Wang, Y.; Zhang, C.; Bhatnagar, D.; Liu, Y. The bZIP Transcription Factor Afap1 Mediates the Oxidative Stress Response and Aflatoxin Biosynthesis in Aspergillus flavus. Rev. Argent. Microbiol. 2019, 51, 292–301.
   PubMed Web of Science ®Google Scholar
• Mayer, Z.; Bagnara, A.; Färber, P.; Geisen, R. Quantification of the Copy Number of nor-1, a Gene of the Aflatoxin Biosynthetic Pathway by Real-Time PCR, and Its Correlation to the Cfu of Aspergillus flavus in Foods. Int. J. Food Microbiol. 2003, 82, 143–151.
   PubMed Web of Science ®Google Scholar
• Yoshinari, T.; Akiyama, T.; Nakamura, K.; Kondo, T.; Takahashi, Y.; Muraoka, Y.; Nonomura, Y.; Nagasawa, H.; Sakuda, S. Dioctatin a is a Strong Inhibitor of Aflatoxin Production by Aspergillus parasiticus. Microbiology (Reading) 2007, 153, 2774–2780.
   PubMed Web of Science ®Google Scholar
• Jones, D. T.; Taylor, W. R.; Thornton, J. M. The Rapid Generation of Mutation Data Matrices from Protein Sequences. Bioinformatics 1992, 8, 275–282. DOI: https://doi.org/10.1093/bioinformatics/8.3.275.
   Web of Science ®Google Scholar
• Velez-Haro, J. M.; Buitimea-Cantúa, N. E.; Rosas-Burgos, E. C.; Molina-Torres, J.; Buitimea-Cantúa, G. V. Effect of the Roots Extract from Heliopsis longipes on Aspergillus parasiticus Growth. Biotecnia. 2018, 20, 127–134. DOI: https://doi.org/10.18633/biotecnia.v20i3.720.
   Web of Science ®Google Scholar
• García-Chávez, A.; Chávez, E. R.; Molina-Torres, J. El género Heliopsis (Heliantheae; Asteraceae) en México y las alcamidas presentes en sus raíces. Acta Bot. Mex 2004, 69, 115–131.
   Google Scholar
• Molina-Torres, J.; Salgado-Garciglia, R.; Ramirez-Chavez, E.; Del Rio, R. E. Purely Olefinic Alkamnides in Heliopsis longipes and Acmella (Spilanthes) Oppositifolia. Biochem. Syst. Ecol. 1996, 24, 43–47. DOI: https://doi.org/10.1016/0305-1978(95)00099-2.
   Web of Science ®Google Scholar
• Ren, Y.; Jin, J.; Zheng, M.; Yang, Q.; Xing, F. Ethanol Inhibits Aflatoxin B1 Biosynthesi in Aspergillus flavus by up-Regulating Oxidative Stress-Related Genes. Front. Microbiol. 2020, 10, 2946–2958. DOI: https://doi.org/10.3389/fmicb.2019.02946.
   PubMed Web of Science ®Google Scholar
• Carrasco, H.; Raimondi, M.; Svetaz, L.; Liberto, M. D.; Rodriguez, M. V.; Espinoza, L.; Madrid, A.; Zacchino, S. Antifungal Activity of Eugenol Analogues. Influence of Different Substituents and Studies on Mechanism of Action. Molecules 2012, 17, 1002–1024. DOI: https://doi.org/10.3390/molecules17011002.
   PubMed Web of Science ®Google Scholar
• Darvishi, E.; Omidi, M.; Bushehri, A. A. S.; Golshani, A.; Smith, M. L. The Antifungal Eugenol Perturbs Dual Aromatic and Branched-Chain Amino Acid Permeases in the Cytoplasmic Membrane of Yeast. PloS One. 2013, 8, e76028.
   PubMed Web of Science ®Google Scholar
• Shishodia, S. K.; Tiwari, S.; Hoda, S.; Vijayaraghavan, P.; Shankar, J. SEM and qRT-PCR Revealed Quercetin Inhibits Morphogenesis of Aspergillus flavus Conidia via Modulating calcineurin-Crz1 Signalling Pathway. Mycology 2020, 11, 118–125.
   PubMedGoogle Scholar
• Uka, V.; Cary, J. W.; Lebar, M. D.; Puel, O.; De Saeger, S.; Diana Di Mavungu, J. Chemical Repertoire and Biosynthetic Machinery of the Aspergillus flavus Secondary Metabolome: A Review. Compr. Rev. Food Sci. F 2020, 19, 2797–2842. DOI: https://doi.org/10.1111/1541-4337.12638.
   Web of Science ®Google Scholar
• Chang, P. K.; Yu, J.; Ehrlich, K. C.; Boue, S. M.; Montalbano, B. G.; Bhatnagar, D.; Cleveland, T. E. adhA in Aspergillus parasiticus is Involved in Conversion of 5′-Hydroxyaverantin to Averufin. Appl. Environ. Microbiol. 2000, 66, 4715–4719.
   PubMed Web of Science ®Google Scholar
• Cleveland, T. E.; Yu, J.; Fedorova, N.; Bhatnagar, D.; Payne, G. A.; Nierman, W. C.; Bennett, J. W. Potential of Aspergillus flavus Genomics for Applications in Biotechnology. Trends Biotech 2009, 27, 151–157. DOI: https://doi.org/10.1016/j.tibtech.2008.11.008.
   PubMed Web of Science ®Google Scholar
• Liang, D.; Xing, F.; Selvaraj, J. N.; Liu, X.; Wang, L.; Hua, H.; Zhou, L.; Zhao, Y.; Wang, Y.; Liu, Y. Inhibitory Effect of Cinnamaldehyde, Citral, and Eugenol on Aflatoxin Biosynthetic Gene Expression and Aflatoxin B1 Biosynthesis in Aspergillus flavus. J. Food Sci. 2015, 80, M2917–M2924.
   PubMed Web of Science ®Google Scholar
• Zhao, X.; Zhi, Q. Q.; Li, J. Y.; Keller, N. P.; He, Z. M. The Antioxidant Gallic Acid Inhibits Aflatoxin Formation in Aspergillus flavus by Modulating Transcription Factors FarB and CreA. Toxins (Basel) 2018, 10, 270–287.
   Web of Science ®Google Scholar
• Wang, P.; Ma, L.; Jin, J.; Zheng, M.; Pan, L.; Zhao, Y.; Sun, X.; Liu, Y.; Xing, F. The anti-Aflatoxigenic Mechanism of Cinnamaldehyde in Aspergillus flavus. Sci. Rep. 2019, 9, 10411–10499.
   PubMed Web of Science ®Google Scholar
• Ehrlich, K. C.; Montalbano, B. G.; Cotty, P. J. Sequence Comparison of aflR from Different Aspergillus Species Provides Evidence for Variability in Regulation of Aflatoxin Production. Fungal Genet. Biol. 2003, 38, 63–74.
   PubMed Web of Science ®Google Scholar
• Kong, Q.; Chi, C.; Yu, J.; Shan, S.; Li, Q.; Li, Q.; Guan, B.; Nierman, W. C.; Bennett, J. W. The Inhibitory Effect of Bacillus megaterium on Aflatoxin and Cyclopiazonic Acid Biosynthetic Pathway Gene Expression in Aspergillus flavus. Appl. Microbiol. Biotechnol. 2014, 98, 5161–5172.
   PubMed Web of Science ®Google Scholar
• Moon, Y. S.; Choi, W. S.; Park, E. S.; Bae, I. K.; Choi, S. D.; Paek, O.; Kim, S. H.; Chun, H. S.; Lee, S. E. Antifungal and Antiaflatoxigenic Methylenedioxy-Containing Compounds and Piperine-like Synthetic Compounds. Toxins (Basel) 2016, 8, 240.
   Web of Science ®Google Scholar
• Caceres, I.; El Khoury, R.; Bailly, S.; Oswald, I. P.; Puel, O.; Bailly, J. D. Piperine Inhibits Aflatoxin B1 Production in Aspergillus flavus by Modulating Fungal Oxidative Stress Response. Fungal Genet. Biol. 2017, 107, 77–85.
   PubMed Web of Science ®Google Scholar
• Chang, P. K.; Ehrlich, K. C.; Yu, J.; Bhatnagar, D.; Cleveland, T. E. Increased Expression of Aspergillus parasiticus aflR, Encoding a Sequence-Specific DNA-Binding Protein, Relieves Nitrate Inhibition of Aflatoxin Biosynthesis. Appl. Environ. Microbiol. 1995, 61, 2372–2377.
   PubMed Web of Science ®Google Scholar