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Environmental effects on resistance gene expression in milk stage popcorn kernels and associations with mycotoxin production

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Abstract

Like other forms of maize, popcorn is subject to increased levels of contamination by a variety of different mycotoxins under stress conditions, although levels generally are less than dent maize under comparable stress. Gene array analysis was used to determine expression differences of disease resistance-associated genes in milk stage kernels from commercial popcorn fields over 3 years. Relatively lower expression of resistance gene types was noted in years with higher temperatures and lower rainfall, which was consistent with prior results for many previously identified resistance response-associated genes. The lower rates of expression occurred for genes such as chitinases, protease inhibitors, and peroxidases; enzymes involved in the synthesis of cell wall barriers and secondary metabolites; and regulatory proteins. However, expression of several specific resistance genes previously associated with mycotoxins, such as aflatoxin in dent maize, was not affected. Insect damage altered the spectrum of resistance gene expression differences compared to undamaged ears. Correlation analyses showed expression differences of some previously reported resistance genes that were highly associated with mycotoxin levels and included glucanases, protease inhibitors, peroxidases, and thionins.

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References

  • Atkinson NJ, Urwin PE (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot. doi:10.1093/jxb/ers100. 21 pp

    PubMed Central  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B 57:289–300

    Google Scholar 

  • Campos-Bermudez VA, Fauguel CM, Tronconi MA, Casati P, Presello DA, Andreo CS (2013) Transcriptional and metabolic changes associated to the infection by Fusarium verticillioides in maize inbreds with contrasting ear rot resistance. PLoS One 8:e61580

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chen ZY, Brown RL, Russin JS, Lax AR, Cleveland TE (1999) A corn trypsin inhibitor with antifungal activity inhibits Aspergillus flavus α-amylase. Phytopathology 89:902–907

    Article  CAS  PubMed  Google Scholar 

  • Christensen SA, Nemchenko A, Borrego E, Murray I, Sobhy IS, Bosak L, Deplasion S, Erb M, Robert CAM, Vaughn KA, Herrfurth C, Tumlinson J, Feussner I, Jackson D, Turlings TCJ, Engelberth J, Nansen C, Meeley R, Kolomiets MV (2013) The maize lipoxygenase ZMLOX10, mediates green leaf volatile, jasmonate and herbivore-induced plant volatile production for defense against insect attack. Plant J 74:59–73

    Article  CAS  PubMed  Google Scholar 

  • Dowd PF (1990) Responses of Carpophilus hemipterus larvae and adults to selected secondary metabolites of maize. Entomol Exp Appl 54:29–36

    Article  CAS  Google Scholar 

  • Dowd PF (1994) Enhanced maize (Zea mays L.) pericarp browning: associations with insect resistance and involvement of oxidizing enzymes. J Chem Ecol 20:2777–2803

    Article  CAS  PubMed  Google Scholar 

  • Dowd PF (2000) Indirect reduction of ear molds and associated mycotoxins in Bacillus thuringiensis corn under controlled and open field conditions: utility and limitations. J Econ Entomol 93:1669–1679

    Article  CAS  PubMed  Google Scholar 

  • Dowd PF (2001) Biotic and abiotic factors limiting efficacy of Bt corn in indirectly reducing mycotoxin levels in commercial fields. J Econ Entomol 94:1067–1074

    Article  CAS  PubMed  Google Scholar 

  • Dowd PF, Bennett GA, McGuire MR, Nelsen TC, Shasha BS, Simmons FW (1999) Adherent malathion flour granules as an environmentally selective control for chewing insect pests of dent corn ears: II. Indirect reduction of mycotoxigenic ear molds. J Econ Entomol 92:68–75

    Article  CAS  Google Scholar 

  • Dowd PF, Johnson ET (2005) Association of a specific cationic peroxidase isozyme with maize stress and disease resistance responses, genetic identification, and identification of a cDNA coding for the isozyme. J Agric Food Chem 53:4464–4470

    Article  CAS  PubMed  Google Scholar 

  • Dowd PF, Johnson ET (2010) Field incidence of mycotoxins in commercial popcorn and potential environmental influences. Mycotox Res 26:15–22

    Article  CAS  Google Scholar 

  • Dowd PF, Johnson ET, Pinkerton TS (2010) Identification and properties of insect resistance-associated maize anionic peroxidases. Phytochem 71:1289–1297

  • Dowd PF, Johnson ET, Pinnkerton TS, Hughes SR (2008) Genetically modified plants containing plant-derived genes for broad spectrum insect control to reduce mycotoxins: bioactive proteins. In: Wolf TW, Koch JP (eds) Genetically modified plants. Nova Science Publishers, New York, pp 127–150

  • Englishloeb GM (1990) Plant drought stress and outbreaks of spider mites—a field test. Ecology 71:1401–1411

    Article  Google Scholar 

  • Englishloeb G, Stout MJ, Duffey SS (1997) Drought stress in tomatoes: changes in plant chemistry and potential nonlinear consequences to insect herbivores. Oikos 79:456–468

    Article  Google Scholar 

  • Fritsche-Neto R, Borem A (2012) Plant breeding for biotic stress resistance. Springer, New York

    Book  Google Scholar 

  • Fürstenberg-Hägg J, Zagrobelny M, Bak S (2013) Plant defense against insect herbivores. Int J Mol Sci 14:10242–10297

    Article  PubMed Central  PubMed  Google Scholar 

  • Garcia-Lara S, Bergvinson DJ, Burt AJ, Ramputh AJ, Diaz-Pontones DM, Arnason JT (2004) The role of pericarp cell wall components in maize weevil resistance. Crop Sci 44:1546–1552

    Article  Google Scholar 

  • Garcia-Lara S, Arnason JT, Diaz-Pontones D, Gonzalez E, Bergvinson DJ (2007) Soluble peroxidase activity in maize endosperm associated with maize weevil resistance. Crop Sci 47:1125–1130

    Article  Google Scholar 

  • Gembeh SV, Brown RL, Grimm C, Cleveland TE (2001) Identification of chemical components of corn kernel pericarp wax associated with resistance to Aspergillus flavus infection and aflatoxin production. J Agric Food Chem 49:4635–4641

    Article  CAS  PubMed  Google Scholar 

  • Glauser G, Marti G, Villard N, Doyen GA, Wolfender J, Turlings TC, Erb M (2011) Induction and detoxification of maize 1,4-benzoxazin-3-ones by insect herbivores. Plant J 68:901–911

    Article  CAS  PubMed  Google Scholar 

  • Guangsheng Y, Zhiming Z, Kai X, Maojun Z, Yaou S, Guangtang P (2012) Large-scale identification of differentially expressed genes in maize inbreds susceptible and resistant to Fusarium ear rot. Plant Omics J 5:471–475

    Google Scholar 

  • Hedge P, Abernathy K, Gay C, Dharap S, Gaspard R, Hughes JE, Snesrud E, Lee N, Quackenbush J (2000) A concise guide to cDNA microarray analysis. Biotech 29:548–556

  • Hedin PA, Davis FM, Williams WP, Salin ML (1984) Possible factors of leaf-feeding resistance in corn to the southwestern corn borer. J Agric Food Chem 32:262–267

    Article  CAS  Google Scholar 

  • Ji C, Norton RA, Wicklow DT, Dowd PF (2000) Isoform patterns of chitinase and β-1,3-glucanase in maturing corn kernels (Zea mays L.) associated with Aspergillus flavus milk stage infection. J Agric Food Chem 48:507–511

    Article  CAS  PubMed  Google Scholar 

  • Johnson ET, Dowd PF (2004) Differentially enhanced insect resistance, at a cost, in Arabidopsis thaliana constitutively expressing a transcription factor of defensive metabolites. J Agric Food Chem 52:5135–5138

    Article  CAS  PubMed  Google Scholar 

  • Johnson EJ, Skory CD, Dowd PF (2014) Identification of a bioactive Bowman-Birk inhibitor from an insect resistant early maize inbred. J Agric Food Chem 62:5458–5465

    Article  CAS  PubMed  Google Scholar 

  • Joshi M, Rong X, Moll S, Kers J, Franco C, Loria A (2007) Streptomyces turgidiscabies secretes a novel virulence protein, Nec1, which facilitates infection. Mol Plant Microbe Interact 20:599–608

    Article  CAS  PubMed  Google Scholar 

  • Kelley RY, Williams WP, Mylroie JE, Boykin DL, Hawkins LK, Windham GL, Brooks TD, Bridges SM, Scheffler BE, Wilkinson JR (2009) Genomic profile of maize response to Aspergillus flavus infection. Toxin Rev 28:129–141

    Article  CAS  Google Scholar 

  • Kelley RY, Williams WP, Mylroie JE, Boykin DL, Harper JW, Windham GL, Ankala A, Shan X (2012) Identification of maize gene associated with host plant resistance or susceptibility to Aspergillus flavus infection and aflatoxin accumulation. PLoS One 7:e36892

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Koornneef A, Pieterse CMJ (2008) Cross-talk in defense signaling. Plant Physiol 146:839–844

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lawrence SD, Novak NG (2006) Expression of poplar chitinase in tomato leads to inhibition of development in Colorado potato beetle. Biotechnol Lett 28:593–599

    Article  CAS  PubMed  Google Scholar 

  • Liu W, Saint DA (2002) A new quantitative method of real time reverse transcription polymerase chain reaction assay based on simulation of polymerase chain reaction kinetics. Anal Biochem 302:52–59

    Article  CAS  PubMed  Google Scholar 

  • Luo M, Liu J, Lee RD, Scully BT, Guo B (2010) Monitoring the expression of maize genes in developing kernels under drought stress using oligo-microarray. J Integr Plant Biol 52:1059–1074

    Article  CAS  PubMed  Google Scholar 

  • Metcalf RL, Metcalf RA (1993) Destructive and useful insects: their habits and control, 5th edn. McGraw Hill, New York

    Google Scholar 

  • Miller JD, Fielder DA, Dowd PF, Norton RA, Collins FW (1996) Isolation of 4-acetyl-benzoxazolin-2-one (4-ABOA) and diferuloyl putricine from an extract of Gibberella ear rot resistant corn that blocks mycotoxin biosynthesis, and the insect toxicity of 4-ABOA and related compounds. Biochem Syst Ecol 24:647–658

    Article  CAS  Google Scholar 

  • Oerke EC (2005) Crop losses to pests. J Agric Sci 144:31–43

    Article  Google Scholar 

  • Payne GM (1999) Mycotoxins and mycotoxicoses. In: White DG (ed) Compendium of corn diseases, 3rd edn. APS Press, St. Paul, pp 47–49

    Google Scholar 

  • Pechan T, Cohen A, Williams WP, Luthe DS (2002) Insect feeding mobilizes a unique plant defense protease that disrupts the peritrophic matrix of caterpillars. Proc Natl Acad Sci U S A 99:13319–13323

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pflieger S, Vefebvre V, Causse M (2001) The candidate gene approach in plant genetics: a review. Mol Breeding 7:275–291

    Article  CAS  Google Scholar 

  • Rehrig EM, Appel HW, Schultz JC (2011) Measuring ‘normalcy’ in plant gene expression after herbivore attack. Mol Ecol Resour 11:294–304

    Article  CAS  PubMed  Google Scholar 

  • Saleemullah AL, Khalil IA, Shah H (2006) Aflatoxin content of stored and artificially inoculated cereals and nuts. Food Chem 98:699–703

    Article  CAS  Google Scholar 

  • Sales MP, Pimenta PP, Paes NS, Grossi-de-Sa MF, Xavier-FIlho JX (2001) Vicillins (7S storage globulins) of cowpea (Vigna unguiculata) seeds bind to the chitinous structures of the midgut of Callosobruchus maculatus (Coleoptera: Bruchidae) larvae. Braz J Med Biol Res 34:27–34

  • Sema-Saldivar SO (2012) Cereal grains: laboratory reference and procedures manual. CRC Press, Boca Raton, 394 pp

    Google Scholar 

  • Sturaro M, Hartings H, Schmelzer E, Velasco R, Salamini F, Motto M (2005) Cloning and characterization of GLOSSY1 a maize gene involved in cuticle membrane and wax production. Plant Physiol 136:478–489

    Article  Google Scholar 

  • Wang G, Wang G, Zhang X, Wang F, Song R (2012) Isolation of high quality RNA from cereal seeds containing high levels of starch. Phytochem Anal 23:159–163

    Article  PubMed  Google Scholar 

  • Warburton ML, Williams WP (2014) Aflatoxin resistance in maize: what have we learned lately? Adv Botany. doi:10.1155/2014/352831

  • Widstrom NW, Wilson DM, McMillian WW (1981) Aflatoxin contamination of preharvest corn as influenced by timing and method of inoculation. Appl Environ Microbiol 42:249–251

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wong HL, Sakamoto T, Kawasaki T, Umemura K, Shimamoto K (2004) Down-regulation of metallothionein, a reactive oxygen scavenger, by the small GTPase OsRac1 in rice. Plant Physiol 135:1447–1456

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhu Y, Qian W, Hua J (2010) Temperature modulates plant defense responses through NB-LRR proteins. PLoS Pathog 6:e1000844

    Article  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

We thank D. Clark and D. Duval for allowing us to sample fields, the Central Illinois Irrigated Growers Association for facilitating the collaboration, D. Lee and M. Doehring for technical assistance, and A. P. Rooney and F.E. Vega for comments on prior versions of this manuscript.

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Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture. USDA is an equal opportunity provider and employer.

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  1. Crop BioProtection Research Unit, USDA, Agricultural Research Service, Peoria, IL, USA

    Patrick F. Dowd & Eric T. Johnson

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  1. Patrick F. Dowd
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Correspondence to Patrick F. Dowd.

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Dowd, P.F., Johnson, E.T. Environmental effects on resistance gene expression in milk stage popcorn kernels and associations with mycotoxin production. Mycotoxin Res 31, 63–82 (2015). https://doi.org/10.1007/s12550-014-0215-1

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  • DOI: https://doi.org/10.1007/s12550-014-0215-1

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