144
Views
0
CrossRef citations to date
0
Altmetric
Research Article

Divergent Aspergillus flavus corn population is composed of prolific conidium producers: Implications for saprophytic disease cycle

ORCID Icon, ORCID Icon, , , , , ORCID Icon, & ORCID Icon show all
Received 27 Sep 2023, Accepted 12 Apr 2024, Published online: 10 May 2024

LITERATURE CITED

  • Abbas HK, Weaver MA, Horn BW, Carbone I, Monacell JT, Shier WT. 2011. Selection of Aspergillus flavus isolates for biological control of aflatoxins in corn. Toxin Rev. 30:59–70. doi:10.3109/15569543.2011.591539.
  • Abbas HK, Weaver MA, Zablotowicz RM, Horn BW, Shier WT. 2005. Relationships between aflatoxin production and sclerotia formation among isolates of Aspergillus section Flavi from the Mississippi Delta. Eur J Plant Pathol. 112:283–287. doi:10.1007/s10658-004-4888-8.
  • Adhikari BN, Bandyopadhyay R, Cotty PJ. 2016. Degeneration of aflatoxin gene clusters in Aspergillus flavus from Africa and North America. AMB Express. 6:62. doi:10.1186/s13568-016-0228-6.
  • Agbetiameh D, Ortega-Beltran A, Awuah RT, Atehnkeng J, Elzein A, Cotty PJ, Bandyopadhyay R. 2020. Field efficacy of two atoxigenic biocontrol products for mitigation of aflatoxin contamination in maize and groundnut in Ghana. Biol Control. 150:104351. doi:10.1016/j.biocontrol.2020.104351.
  • Agbetiameh D, Ortega-Beltran A, Awuah RT, Atehnkeng J, Islam M-S, Callicott KA, Cotty PJ, Bandyopadhyay R. 2019. Potential of atoxigenic Aspergillus flavus vegetative compatibility groups associated with maize and groundnut in Ghana as biocontrol agents for aflatoxin management. Front Microbiol. 10:2069. doi:10.3389/fmicb.2019.02069.
  • Atehnkeng J, Ojiambo PS, Donner M, Ikotun T, Sikora RA, Cotty PJ, Bandyopadhyay R. 2008. Distribution and toxigenicity of Aspergillus species isolated from Maize kernels in three agro-ecological zones in Nigeria. Int J Food Microbiol. 122:74–84. doi:10.1016/j.ijfoodmicro.2007.11.062.
  • Bandyopadhyay R, Ortega-Beltran A, Akande A, Mutegi C, Atehnkeng J, Kaptoge L, Senghor AL, Adhikari BN, Cotty PJ. 2016. Biological control of aflatoxins in Africa: current status and potential challenges in the face of climate change. World Mycotoxin J. 9:771–789. doi:10.3920/WMJ2016.2130.
  • Bayman P, Cotty PJ. 1991. Vegetative compatibility and genetic diversity in the Aspergillus flavus population of a single field. Can J Bot. 69:1707–1711. doi:10.1139/b91-216.
  • Bushnell B. 2014. BBMap: A Fast, Accurate, Splice-Aware Aligner. Lawrence Berkeley National Laboratory. LBNL Report #: LBNL-7065E. https://escholarship.org/uc/item/1h3515gn.
  • Camiletti BX, Moral J, Asensio CM, Torrico AK, Lucini EI, Giménez-Pecci MP, Michailides TJ. 2018. Characterization of Argentinian endemic Aspergillus flavus isolates and their potential use as biocontrol agents for mycotoxins in maize. Phytopathology. 108:818–828. doi:10.1094/PHYTO-07-17-0255-R.
  • Chang P-K, Abbas HK, Weaver MA, Ehrlich KC, Scharfenstein LL, Cotty PJ. 2012. Identification of genetic defects in the atoxigenic biocontrol strain Aspergillus flavus K49 reveals the presence of a competitive recombinant group in field populations. Int J Food Microbiol. 154:192–196. doi:10.1016/j.ijfoodmicro.2012.01.005.
  • Chang P-K, Ehrlich KC, Hua -S-ST. 2006. Cladal relatedness among Aspergillus oryzae isolates and Aspergillus flavus S and L morphotype isolates. Int J Food Microbiol. 108:172–177. doi:10.1016/j.ijfoodmicro.2005.11.008.
  • Chang P-K, Scharfenstein LL, Mack B, Ehrlich KC. 2012. Deletion of Aspergillus flavus orthologue of A. nidulans fluG reduces conidiation and promotes production of sclerotia but does not abolish aflatoxins biosynthesis. Appl Environ Microbiol. 78:7557–7563. doi:10.1128/AEM.01241-12.
  • Coley-Smith JR, Cooke RC. 1971. Survival and germination of fungal sclerotia. Annu Rev Phytopathol. 9:65–92. doi:10.1146/annurev.py.09.090171.000433.
  • Cotty PJ. 1989. Virulence and cultural characteristics of two Aspergillus flavus strains pathogenic on cotton. Phytopathology. 79:808–814. doi:10.1094/Phyto-79-808.
  • Crow JF, Kimura M. 1970. An introduction to population genetics theory. New York (NY/USA): Harper & Row Publishers.
  • Damann KE Jr, DeRobertis C, Sweany R. 2010. Mating between Aspergillus flavus cryptic species I & II. Phytopathology. 100:S28.
  • Danecek P, Auton A, Abecasis G, Albers CA, Banks E, De Pristo MA, Handsaker RE, Lunter G, Marth GT, Sherry ST, et al.; 1000 Genomes Project Analysis Group. 2011. The variant call format and VCFtools. Bioinformatics. 15:2156–2158. doi:10.1093/bioinformatics/btr330.
  • Danecek P, Bonfield JK, Liddle J, Marshall J, Ohan V, Pollard MO, Whitwham A, Keane T, McCarthy SA, Davies RM, et al. 2021. Twelve years of SAMtools and BCFtools. Gigascience. 10:giab008. doi:10.1093/gigascience/giab008.
  • Debuchy R, Berteaux-Lecellier V, Silar P. 2010. Mating systems and sexual morphogenesis in Ascomycetes. In: Borkovich KA, Ebbole DJ, editors. Cellular and molecular biology of filamentous fungi. Washington DC: ASM Press; p. 501–535.
  • Diener UL, Cole RJ, Sanders TH, Payne GA, Lee LS, Klich MA. 1987. Epidemiology of aflatoxin formation by Aspergillus flavus. Annu Rev Phytopathol. 25:249–270. doi:10.1146/annurev.py.25.090187.001341.
  • Drott MT, Debenport T, Higgins SA, Buckley DH, Milgroom MG. 2019. Fitness cost of aflatoxin production in Aspergillus flavus when competing with soil microbes could maintain balancing selection. mBio. 10:e02782–18. doi:10.1128/mBio.02782-18.
  • Drott MT, Fessler LM, Milgroom MG. 2019. Population subdivision and the frequency of aflatoxigenic isolates in Aspergillus flavus in the United States. Phytopathology. 109:878–886. doi:10.1094/PHYTO-07-18-0263-R.
  • Drott MT, Satterlee TR, Skerker JM, Pfannenstiel BT, Glass NL, Keller NP, Milgroom MG. 2020. The frequency of sex: population genomics reveals differences in recombination and population structure of the aflatoxin-producing fungus Aspergillus flavus. mBio. 11:e00963–20. doi:10.1128/mBio.00963-20.
  • Ehrlich KC, Chang P-K, Yu J, Cotty PJ. 2004. Aflatoxin biosynthesis cluster gene cypA is required for G aflatoxin formation. Appl Environ Microbiol. 70:6518–6524. doi:10.1128/AEM.70.11.6518-6524.2004.
  • Ehrlich KC, Montalbano BG, Cotty PJ. 2007. Analysis of single nucleotide polymorphisms in three genes shows evidence for genetic isolation of certain Aspergillus flavus compatibility groups. FEMS Microbiol Lett. 286:231–236. doi:10.1111/j.1574-6968.2006.00588.x.
  • Fountain JC, Clevenger JP, Nadon B, Youngblood RC, Korani W, Chang P-K, Starr D, Wang H, Isett B, Johnston HR, et al. 2020. Two new Aspergillus flavus reference genomes reveal a large insertion potentially contributing to isolate stress tolerance and aflatoxin production. G3-Genes Genomes Genet. 10:3515–3531. doi:10.1534/g3.120.401405.
  • Frisvad JC, Hubka V, Ezekiel CN, Hong SB, Nováková A, Chen AJ, Arzanlou M, Larsen TO, Sklenář F, Mahakarnchanakul W, et al. 2019. Taxonomy of Aspergillus section Flavi and their production of aflatoxins, ochratoxins and other mycotoxins. Stud Mycol. 93:1–63. doi:10.1016/j.simyco.2018.06.001.
  • Garrison E, Marth G 2012. Haplotype-based variant detection from short-read sequencing. arXiv:1207.3907.
  • Gebru ST, Mammel MK, Gangiredla J, Tartera C, Cary JW, Moore GG, Sweany RR. 2020. Draft genome sequences of 20 Aspergillus flavus isolates from corn kernels and cornfield soils in Louisiana. Microbiol Resour Announc. 9:e00826–20. doi:10.1128/MRA.00826-20.
  • Geiser DM, Dorner JW, Horn BW, Taylor JW. 2000. The phylogenetics of mycotoxin and sclerotium production in Aspergillus flavus and Aspergillus oryzae. Fungal Genet Biol. 31:169–179. doi:10.1006/fgbi.2000.1215.
  • Geiser DM, Pitt JI, Taylor JW. 1998. Cryptic speciation and recombination in the aflatoxin-producing fungus Aspergillus flavus. Proc Natl Acad Sci. 95:388–393. doi:10.1073/pnas.95.1.388.
  • Giorni P, Magan N, Pietri A, Bertuzzi T, Battilani P. 2007. Studies on Aspergillus section Flavi isolated from maize in northern Italy. Int J Food Microbiol. 113:330–338. doi:10.1016/j.ijfoodmicro.2006.09.007.
  • Horn BW. 2003. Ecology and population biology of aflatoxigenic fungi in soil. J Toxicol. 22:351–379.
  • Horn BW, Gell RM, Singh R, Sorensen RB, Carbone I. 2016. Sexual reproduction in Aspergillus flavus sclerotia: acquisition of novel alleles from soil populations and uniparental mitochondrial inheritance. PLOS ONE. 11:e0146169.
  • Horn BW, Greene RL. 1995. Vegetative compatibility within populations of Aspergillus flavus, A. parasiticus, and A. tamarii from a peanut field. Mycologia. 87:324–332. doi:10.1080/00275514.1995.12026537.
  • Horn BW, Greene RL, Sobolev VS, Dorner JW, Powell JH, Layton RC. 1996. Association of morphology and mycotoxin production with vegetative compatibility groups in Aspergillus flavus, A. parasiticus, and A. tamarii. Mycologia. 88:574–587. doi:10.1080/00275514.1996.12026688.
  • Horn BW, Moore GG, Carbone I. 2009. Sexual reproduction in Aspergillus flavus. Mycologia. 101:423–429. doi:10.3852/09-011.
  • Horn BW, Sorensen RB, Lamb MC, Sobolev VS, Olarte RA, Worthington CJ, Carbone I. 2014. Sexual reproduction in Aspergillus flavus sclerotia naturally produced in corn. Phytopathology. 104:75–85. doi:10.1094/PHYTO-05-13-0129-R.
  • Horowitz Brown S, Scott JB, Bhaheetharan J, Sharpee WC, Milde L, Wilson RA, Keller NP. 2009. Oxygenase coordination is required for morphological transition and the host-fungus interaction of Aspergillus flavus. Mol Plant Microbe Interact. 22:882–894. doi:10.1094/MPMI-22-7-0882.
  • Leslie JF, Klein KK. 1996. Female fertility and mating type effects on effective population size and evolution in filamentous fungi. Genetics. 144:557–567. doi:10.1093/genetics/144.2.557.
  • Li H 2013. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv:1303.3997.
  • Lockwood JL. 1988. Evolution of concepts associated with soilborne plant pathogens. Annu Rev Phytopathol. 26:93–121. doi:10.1146/annurev.py.26.090188.000521.
  • Luis JM, Carbone I, Payne GA, Bhatnagar D, Cary JW, Moore GG, Lebar MD, Wei Q, Mack B, Ojiambo PS. 2020. Characterization of morphological changes within stromata during sexual reproduction in Aspergillus flavus. Mycologia. 112:908–920. doi:10.1080/00275514.2020.1800361.
  • Marsh SF, Payne GA. 1984. Preharvest infection of corn silks and kernels by Aspergillus flavus. Phytopathology. 74:1284–1289. doi:10.1094/Phyto-74-1284.
  • Mauro A, Battilani P, Callicott KA, Giorni P, Pietri A, Cotty PJ. 2013. Structure of an Aspergillus flavus population from maize kernels in northern Italy. Int J Food Microbiol. 162:1–7. doi:10.1016/j.ijfoodmicro.2012.12.021.
  • Mauro A, Garcia-Cela E, Pietri A, Cotty PJ, Battilani P. 2018. Biological control products for aflatoxin prevention in Italy: commercial field evaluation of atoxigenic Aspergillus flavus active ingredients. Toxins. 10:e30. doi:10.3390/toxins10010030.
  • Mehl HL, Cotty PJ. 2010. Variation in competitive ability among isolates of Aspergillus flavus from different vegetative compatibility groups during maize infection. Phytopathology. 100:150–159. doi:10.1094/PHYTO-100-2-0150.
  • Milgroom MG. 2015. Population biology of plant pathogens: genetics, ecology, and evolution. St Paul (MN): The American Phytopathological Society.
  • Mohamed Nor NMI, Salleh B, Leslie JF. 2019. Fusarium species from sorghum in Thailand. Plant Pathol J. 35:301–312. doi:10.5423/PPJ.OA.03.2019.0049.
  • Molo MS, White JB, Cornish V, Gell RM, Baars O, Singh R, Carbone MA, Isakeit T, Wise KA, Woloshuk CP, et al. 2022. Asymmetrical lineage introgression and recombination in populations of Aspergillus flavus: implications for biological control. PLOS ONE. 17(10):e0276556. doi:10.1371/journal.pone.0276556.
  • Moore GG, Elliot JL, Singh R, Horn BW, Dorner JW, Stone EA, Chulze SN, Barros GG, Naik MK, Wright GC, et al. 2013. Sexuality generates diversity in the aflatoxin gene cluster: evidence on a global scale. PLOS Pathogens. 9:e1003574. doi:10.1371/journal.ppat.1003574.
  • Moore GG, Lebar MD, Carter-Wientjes CH. 2019. The role of extrolites secreted by nonaflatoxigenic Aspergillus flavus in biocontrol efficacy. J Appl Microbiol. 126:1257–1264. doi:10.1111/jam.14175.
  • Moore GG, Olarte RA, Horn BW, Elliot JL, Singh R, O’Neal CJ, Carbone I. 2017. Global population structure and adaptive evolution of aflatoxin-producing fungi. Ecol Evol. 7:9179–9191. doi:10.1002/ece3.3464.
  • Moore GG, Singh R, Horn BW, Carbone I. 2009. Recombination and lineage‐specific gene loss in the aflatoxin gene cluster of Aspergillus flavus. Mol Ecol. 18:4870–4887. doi:10.1111/j.1365-294X.2009.04414.x.
  • Novas MV, Cabral D. 2002. Association of mycotoxin and sclerotia production with compatibility groups in Aspergillus flavus from peanut in Argentina. Plant Dis. 86:215–219. doi:10.1094/PDIS.2002.86.3.215.
  • Ohkura M, Cotty PJ, Orbach MJ. 2018. Comparative genomics of Aspergillus flavus S and L morphotypes yield insights into niche adaptation. G3-Genes Genomes Genet. 8:3915–3930. doi:10.1534/g3.118.200553.
  • Ortega-Beltran A, Callicott KA, Cotty PJ. 2020. Founder events influence structures of Aspergillus flavus populations. Environ Microbiol. 22:3522–3534. doi:10.1111/1462-2920.15122.
  • Ortega-Beltran A, Cotty PJ. 2018. Frequent shifts in Aspergillus flavus populations associated with maize production in Sonora, Mexico. Phytopathology. 108:412–420. doi:10.1094/PHYTO-08-17-0281-R.
  • Pildain MB, Frisvad JC, Vaamonde G, Cabral D, Varga J, Samson RA. 2008. Two novel aflatoxin-producing Aspergillus species from Argentinean peanuts. Int J Syst Evol Microbiol. 58:725–735. doi:10.1099/ijs.0.65123-0.
  • Pildain MB, Vaamonde G, Cabral D. 2004. Analysis of population structure of Aspergillus flavus from peanut based on vegetative compatibility, geographic origin, mycotoxin and sclerotia production. Int J Food Microbiol. 93:31–40. doi:10.1016/j.ijfoodmicro.2003.10.007.
  • Probst C, Cotty PJ. 2012. Relationships between in vivo and in vitro aflatoxin production: reliable prediction of fungal ability to contaminate maize with aflatoxins. Fungal Biol. 116:503–510. doi:10.1016/j.funbio.2012.02.001.
  • Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, Maller J, Sklar P, de Bakker PI, Daly MJ. 2007. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet. 81:559–575. doi:10.1086/519795.
  • Ramirez-Prado JH, Moore GG, Horn BW, Carbone I. 2008. Characterization and population analysis of the mating-type genes in Aspergillus flavus and Aspergillus parasiticus. Fungal Genet Biol. 45:1292–1299. doi:10.1016/j.fgb.2008.06.007.
  • Raper KB, Thom CA. 1968. A manual of the Penicilla. Baltimore (MD): Williams & Wilkins Company.
  • Reyes Pineda JA 2017. Characterization of Aspergillus flavus soil and corn kernel populations from eight Mississippi River States [ Master’s thesis]. Baton Rouge: Louisiana State University.
  • Richard JL. 2008. Discovery of aflatoxins and significant historical features. Toxin Rev. 27:171–201. doi:10.1080/15569540802462040.
  • Seemann T 2015. Snippy: fast bacterial variant calling from NGS reads. https://github.com/tseemann/snippy.
  • Smouse PE, Long JC, Sokal RR. 1986. Multiple regression and correlation extensions of the Mantel test of matrix correspondence. Syst Zool. 35:627–632. doi:10.2307/2413122.
  • St Leger RJ, Screen SE, Shums-Pirzadeh B. 2000. Lack of host specialization in Aspergillus flavus. Appl Environ Microbiol. 66:320–324. doi:10.1128/AEM.66.1.320-324.2000.
  • Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 30:1312–1313. doi:10.1093/bioinformatics/btu033.
  • Sweany RR, Damann KE Jr. 2020. Influence of neighboring clonal-colonies on aflatoxin production by Aspergillus flavus. Front Microbiol. 10:3038. doi:10.3389/fmicb.2019.03038.
  • Sweany RR, Damann KE Jr, Kaller MD. 2011. Comparison of soil and corn kernel Aspergillus flavus populations: evidence for niche specialization. Phytopathology. 101:952–959. doi:10.1094/PHYTO-09-10-0243.
  • Sweany RR, DeRobertis CD, Kaller MD, Damann KE Jr. 2022. Intraspecific growth and aflatoxin inhibition responses to atoxigenic Aspergillus flavus: evidence of secreted, inhibitory substances in biocontrol. Phytopathology. 112:2084–2098. doi:10.1094/PHYTO-01-21-0022-R.
  • Sweany RR, Mack BM, Moore GG, Gilbert MK, Cary JW, Lebar MD, Rajasekaran K, Damann KE Jr. 2021. Genetic responses and aflatoxin inhibition during co-culture of aflatoxigenic and non-aflatoxigenic Aspergillus flavus. Toxins (Basel). 13:e794. doi:10.3390/toxins13110794.
  • Thom C, Raper KB. 1945. A manual of the Aspergilli. Baltimore (MD): The Williams & Wilkins Company.
  • Uchida M, Konishi T, Fujigasaki A, Kita K, Arie T, Teraoka T, Kanda Y, Mori M, Arazoe T, Kamakura T. 2023. Dysfunctional Pro1 leads to female sterility in rice blast fungi. iScience. 26:107020. doi:10.1016/j.isci.2023.107020.
  • Vaamonde G, Patriarca A, Fernández Pinto V, Comerio R, Degrossi C. 2003. Variability of aflatoxin and cyclopiazonic acid production by Aspergillus section Flavi from different substrates in Argentina. Int J Food Microbiol. 88:79–84. doi:10.1016/S0168-1605(03)00101-6.
  • Weaver MA, Callicott KA, Mehl HL, Opoku J, Park LC, Fields KS, Mandel JR. 2022. Characterization of the Aspergillus flavus population from highly aflatoxin-contaminated corn in the United States. Toxins. 14:e755. doi:10.3390/toxins14110755.
  • Weaver MA, Mack BM, Gilbert MK. 2019. Genome sequences of 20 georeferenced Aspergillus flavus isolates. Microbiol Resour Announc. 8:e01718. doi:10.1128/MRA.01718-18.
  • Weir BS, Cockerham CC. 1984. Estimating F-statistics for the analysis of population structure. Evolution. 38:1358–1370. doi:10.1111/j.1558-5646.1984.tb05657.x.
  • Wickham H. 2016. ggplot2: elegant graphics for data analysis. New York (NY): Springer-Verlag.
  • Wicklow DT. 1983. Taxonomic features and ecological significances of sclerotia. In: Diener UL, Asquith RL, Dickens JW, editors. Aflatoxin and Aspergillus flavus in corn. Southern cooperative service bulletin 279. Auburn (AL): Auburn University; p. 6–12.
  • Wicklow DT. 1991. Epidemiology of Aspergillus flavus in corn. In: Shotwell OL, Hurburgh CR Jr, editors. Aflatoxin in corn: new perspectives. Iowa agriculture and home economics experiment station research bulletin 599. Ames: Iowa State University; p. 315–328.
  • Wright S. 1931. Evolution in mendelian populations. Genetics. 16:97–159. doi:10.1093/genetics/16.2.97.
  • Yu J, Cleveland TE, Nierman WC, Bennett JW. 2005. Aspergillus flavus genomics: gateway to human and animal health, food safety, and crop resistance to diseases. Rev Iberoam Micol. 22:194–202. doi:10.1016/S1130-1406(05)70043-7.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.