Characterization of morphological changes within stromata during sexual reproduction in Aspergillus flavus

LITERATURE CITED

• Bayman P, Cotty PJ. 1991. Vegetative compatibility and genetic diversity in the Aspergillus flavus population of a single field. Canadian Journal of Botany 69:1707–1711.
   Google Scholar
• Benjamin CR. 1955. Ascocarps of Aspergillus and Penicillium. Mycologia 47:669–687.
   Web of Science ®Google Scholar
• Bennett JW. 2010. An overview of the genus Aspergillus. In: Machida M, Gomi K, eds. Aspergillus: molecular biology and genomics. Portland, Oregon: Caiser Academic Press. p. 1–17.
   Google Scholar
• Bistis GN. 1981. Chemotropic interactions between trichogynes and conidia of opposite mating‐type in Neurospora crassa. Mycologia 73:959–975.
   Web of Science ®Google Scholar
• Bojović-Cvetić D, Vujičić R. 1988. Polysaccharide cytochemistry in maturing Aspergillus flavus sclerotia. Transaction of the British Mycological Society 91:619–624.
   Web of Science ®Google Scholar
• Cary JW, Han Z, Yin Y, Lohmar JM, Shantappa S, Harris-Coward PY, Mack BM, Ehrlich KC, Wei Q, Arroyo-Manzanares N, Uka V, Vanhaecke L, Bhatnagar D, Yu J, Nierman WC, Johns M, Sorensen D, Shen H, De Saeger S, Diana Di Mavungu J, Calvo AM. 2015. Transcriptome analysis of Aspergillus flavus reveals veA-dependent regulation of secondary metabolite gene clusters, including the novel aflavarin cluster. Eukaryotic Cell 14:983–997.
   PubMedGoogle Scholar
• Chang PK. 2008. A highly efficient gene-targeting system for Aspergillus parasiticus. Letters in Applied Microbiology 46:587–592.
   PubMed Web of Science ®Google Scholar
• Chang PK, Horn BW, Abe K, Gomi K. 2014. Aspergillus. In: Batt CA, Tortorello ML, eds. Encyclopedia of food microbiology. Vol. 1. London, UK: Elsevier, Academic Press. p. 77–82.
   Google Scholar
• Colotelo N. 1974. A scanning electron microscope study of developing sclerotia of Sclerotinia sclerotiorum. Canadian Journal of Botany 52:1127–1130.
   Google Scholar
• Cotty PJ, Bayman P. 1993. Competitive exclusion of a toxigenic strain of Aspergillus flavus by an atoxigenic strain. Phytopathology 83:1283–1287.
   Web of Science ®Google Scholar
• [CAST] Council for Agricultural Science and Technology. 2003. Mycotoxins: risks in plant, animal, and human systems. Task Force Report. Ames, Iowa: Council for Agricultural Science and Technology. p. 1–199.
   Google Scholar
• Damann KJ. 2015. Atoxigenic Aspergillus flavus biological control of aflatoxin contamination: what is the mechanism? World Mycotoxin Journal 8:235–244.
   Google Scholar
• Dijksterhuis J. 2007. Heat-resistant ascospores. In: Dijksterhuis J, Samson RA, eds. Food mycology: a multifaceted approach to fungi and food. Boca Raton, Florida: CRC Press. p. 101–117.
   Google Scholar
• Dorner JW. 2004. Biological control of aflatoxin contamination in crops. Journal of Toxicology Toxin Reviews 23:425–450.
   Web of Science ®Google Scholar
• Dyer PS, O’Gorman CM. 2012. Sexual development and cryptic sexuality in fungi: insights from Aspergillus species. FEMS Microbiology Reviews 36:165–192.
   PubMed Web of Science ®Google Scholar
• Ehrlich KC. 2014. Non-aflatoxigenic Aspergillus flavus to prevent aflatoxin contamination in crops: advantages and limitations. Frontiers in Microbiology 5:50.
   PubMed Web of Science ®Google Scholar
• Fennell DI, Warcup JH. 1959. The ascocarps of Aspergillus alliaceus. Mycologia 51:409–415.
   Web of Science ®Google Scholar
• Glass NL, Kaneko I. 2003. Fatal attraction: nonself recognition and heterokaryon incompatibility in filamentous fungi. Eukaryotic Cell 2:1–8.
   PubMed Web of Science ®Google Scholar
• Hedayati MT, Pasqualotto AC, Warn PA, Bowyer P, Denning DW. 2007. Aspergillus flavus: human pathogen, allergen and mycotoxin producer. Microbiology 153:1677–1692.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   Web of Science ®Google Scholar
• Horn BW, Moore GG, Carbone I. 2009a. Sexual reproduction in Aspergillus flavus. Mycologia 101:423–429.
   PubMed Web of Science ®Google Scholar
• Horn BW, Moore GG, Carbone I. 2011. Sexual reproduction in aflatoxin-producing Aspergillus nomius. Mycologia 103:174–183.
   PubMed Web of Science ®Google Scholar
• Horn BW, Olarte RA, Peterson SW, Carbone I. 2013. Sexual reproduction in Aspergillus tubingensis from section Nigri. Mycologia 105:1153–1163.
   PubMed Web of Science ®Google Scholar
• Horn BW, Ramirez-Prado JH, Carbone I. 2009b. Sexual reproduction and recombination in the aflatoxin-producing fungus Aspergillus parasiticus. Fungal Genetics and Biology 46:169–175.
   PubMed Web of Science ®Google Scholar
• Horn BW, Ramirez-Prado JH, Carbone I. 2009c. The sexual state of Aspergillus parasiticus. Mycologia 101:275–280.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Houbraken J, Dyer PS. 2015. Induction of the sexual cycle in filamentous ascomycetes. In: Van den Berg M, Maruthachalam K, eds. Genetic transformation systems in fungi. Vol. 2. Cham, Switzerland: Springer International Publishing. p. 23–46.
   Google Scholar
• Huang C, Jha A, Sweany R, De Robertis C, Damann KEJ. 2011. Intraspecific aflatoxin inhibition in Aspergillus flavus is thigmoregulated, independent of vegetative compatibility group and is strain dependent. PLoS ONE 6:e23470.
   PubMed Web of Science ®Google Scholar
• Khlangwiset P, Shephard GS, Wu F. 2011. Aflatoxins and growth impairment: a review. Critical Reviews in Toxicology 41:740–755.
   PubMed Web of Science ®Google Scholar
• Kim H, Borkovich KA. 2004. A pheromone receptor gene, pre‐1, is essential for mating type‐specific directional growth and fusion of trichogynes and female fertility in Neurospora crassa. Molecular Microbiology 52:1781–1798.
   PubMed Web of Science ®Google Scholar
• Kwon-Chung KJ, Sugui JA. 2009. Sexual reproduction in Aspergillus species of medical or economical importance: why so fastidious? Trends in Microbiology 17:481–487.
   Google Scholar
• Leslie JF, Klein KK. 1996. Female fertility and mating type effects on effective population size and evolution in filamentous fungi. Genetics 144:557–567.
   PubMed Web of Science ®Google Scholar
• Leslie JF, Yamashiro CT. 1997. Effects of the tol mutation on allelic interactions at het loci in Neurospora crassa. Genome 40:834–840.
   PubMed Web of Science ®Google Scholar
• McAlpin CE, Wicklow DT. 2005. Culture media and sources of nitrogen promoting the formation of stromata and ascocarps in Petromyces alliaceus (Aspergillus section Flavi). Canadian Journal of Microbiology 51:765–771.
   PubMed Web of Science ®Google Scholar
• Mitchell NJ, Bowers E, Hurburgh C, Wu F. 2016. Potential economic losses to the US corn industry from aflatoxin contamination. Food Additives and Contaminants: Part A 33:540–550.
   PubMed Web of Science ®Google Scholar
• Molo M, Heiniger R, Boerema L, Carbone I. 2019. Trial summary on the comparison of various non-toxigenic strains of Aspergillus flavus on mycotoxin levels and yield in maize. Agronomy Journal 111:942–946.
   Web of Science ®Google Scholar
• Moore GG, Elliott JL, Singh R, Horn BW, Dorner JW, Stone EA, Chulze SN, Barros GG, Naik MK, Wright GC, Hell K, Carbone I. 2013. Sexuality generates diversity in the aflatoxin gene cluster: evidence on a global scale. PLoS Pathogens 9:e1003574, doi:10.1371/journal.ppat.1003574
   PubMed Web of Science ®Google Scholar
• Moore GG, Olarte RA, Horn BW, Elliott JL, Singh R, O’Neal CJ, Carbone I. 2017. Global population structure and adaptive evolution of aflatoxin producing fungi. Ecology and Evolution 7:9179–9191.
   PubMed Web of Science ®Google Scholar
• Moore GG, Singh R, Horn BW, Carbone I. 2009. Recombination and lineage-specific gene loss in the aflatoxin gene cluster of Aspergillus flavus. Molecular Ecology 18:4870–4887.
   PubMed Web of Science ®Google Scholar
• Ohkura M, Cotty PJ, Orbach MJ. 2018. Comparative genomics of Aspergillus flavus S and L morphotypes yield insights into niche adaptation. G3: Genes|Genomes|Genetics 8:3915–3930.
   Web of Science ®Google Scholar
• Ojiambo PS, Battilani P, Cary JW, Blum BH, Carbone I. 2018. Cultural and genetic approaches to manage aflatoxin contamination: recent insights provide opportunities for improved control. Phytopathology 108:1024–1037.
   PubMed Web of Science ®Google Scholar
• Olarte RA, Horn BW, Dorner JW, Monacell JT, Singh R, Stone EA, Carbone I. 2012. Effect of sexual recombination on population diversity in aflatoxin production by Aspergillus flavus and evidence for cryptic heterokaryosis. Molecular Ecology 21:1453–1476.
   PubMed Web of Science ®Google Scholar
• Olarte RA, Worthington CJ, Horn BW, Moore GG, Singh R, Monacell JW, Dorner JT, Stone EA, Xie D-Y, Carbone I. 2015. Enhanced diversity and aflatoxigenicity in interspecific hybrids of Aspergillus flavus and Aspergillus parasiticus. Molecular Ecology 24:1889–1909.
   PubMed Web of Science ®Google Scholar
• Paulussen C, Hallsworth JE, Álvarez-Pérez S, Nierman WC, Hamill PG, Blain D, Rediers H, Lievens B. 2016. Ecology of aspergillosis: insights into the pathogenic potency of Aspergillus fumigatus and some other Aspergillus species. Microbial Biotechnology 10:296–322.
   PubMed Web of Science ®Google Scholar
• Rajasekaran K, Cary JW, Cotty PJ, Cleveland TE. 2008. Development of a GFP-expressing Aspergillus flavus strain to study fungal invasion, colonization, and resistance in cottonseed. Mycopathologia 165:89–97.
   PubMed Web of Science ®Google Scholar
• 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 Genetics and Biology 45:1292–1299.
   PubMed Web of Science ®Google Scholar
• Raper KB, Fennell DI. 1965. The genus Aspergillus. Baltimore, Maryland: Williams & Wilkins. 686 p.
   Google Scholar
• Read N, Beckett A. 1996. Ascus and ascospore morphogenesis. Mycological Research 100:1281–1314.
   Web of Science ®Google Scholar
• Saleh D, Milazzo J, Adreit H, Tharreau D, Fournier E. 2012. Asexual reproduction induces a rapid and permanent loss of sexual reproduction capacity in the rice fungal pathogen Magnaporthe oryzae: results of in vitro experimental evolution assays. BMC Evolutionary Biology 12:42.
   PubMed Web of Science ®Google Scholar
• Saupe SJ. 2000. Molecular genetics of heterokaryon incompatibility in filamentous ascomycetes. Microbiology and Molecular Biology Reviews 64:489–502.
   PubMed Web of Science ®Google Scholar
• Szewczyk E, Chiang YM, Oakley CE, Davidson AD, Wang CC, Oakley BR. 2008. Identification and characterization of the asperthecin gene cluster of Aspergillus nidulans. Applied and Environmental Microbiology 74:7607–7612.
   PubMed Web of Science ®Google Scholar
• Wild CP. 2007. Aflatoxin exposure in developing countries: the critical interface of agriculture and health. Food and Nutrition Bulletin 28:S380.
   Web of Science ®Google Scholar
• Wild CP, Miller JD, Groopman JD, editors. 2015. Mycotoxin control in low- and middle-income countries. IARC Working Group Reports, No. 9. Lyon, France: International Agency for Research on Cancer.
   Google Scholar
• Willetts HJ. 1997. Morphology, development and evolution of stromata/sclerotia and macroconidia of the Sclerotiniaceae. Mycological Research 101:939–952.
   Web of Science ®Google Scholar
• Wu C, Kimbrough JW. 1990. Ultrastructural studies on the cleistothecial development of Emericellopsis microspora (Eurotiales, Ascomycetes). Canadian Journal of Botany 68:1877–1888.
   Google Scholar