Mycotoxin Research

, Volume 30, Issue 2, pp 61–70 | Cite as

Diplodiatoxin, chaetoglobosins, and diplonine associated with a field outbreak of Stenocarpella ear rot in Illinois

  • Kristina D. Rogers
  • Joseph C. Cannistra
  • James B. Gloer
  • Donald T. Wicklow
Original Paper

Abstract

Stenocarpella maydis causes a fungal dry-rot of maize ears and is associated with diplodiosis, a neuromycotoxicosis in cattle grazing harvested maize fields in southern Africa and Argentina. There have been no reports of Stenocarpella metabolites in maize crop residues. Chemical investigations of S. maydis-infected grain from ears exhibiting different levels of ear rot severity following a 2010 field outbreak of Stenocarpella ear rot in Illinois led to the detection of diplodiatoxin and chaetoglobosins M and O as major components in the ethyl acetate extracts by LC-MS. Following post-harvest moist incubation of the S. maydis-infected grain, the amounts of each compound increased (approx. tenfold) and chaetoglobosin K was detected as a dominant toxin. In separate 1H NMR-based analyses, the neurotoxin diplonine was detected as a minor component in methanol extracts of S. maydis-infected grain as well as cultures of S. maydis isolates from Midwest corn. Proline betaine (=stachydrine) and glycine betaine were also detected in these extracts as major components. This constitutes the first report of chaetoglobosin M, chaetoglobosin O, proline betaine, or glycine betaine from S. maydis, and the first record of diplodiatoxin, diplonine, proline betaine, glycine betaine, or chaetoglobosins M, O, or K being associated with a natural field outreak of S. maydis ear rot.

Keywords

Chaetoglobosins Diplodiosis Diplodiatoxin Diplonine Neuromycotoxicosis Proline betaine (Stachydrine) Stenocarpella maydis Zea mays 

Notes

Acknowledgments

Support for this work from the National Science Foundation (CHE1011847) is gratefully acknowledged. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the United States Department of Agriculture or the National Science Foundation. USDA is an equal opportunity provider and employer.

Conflict of interest

None.

References

  1. Alloing G, Travers I, Sagot B, Le Rudulier D, Dupont L (2006) Proline betaine uptake in Sinorhizobiuim meliloti: Characterization of Prb, an opp-like ABC transporter regulated by both proline betaine and salinity stress. J Bacteriol 188:6308–6317PubMedCentralPubMedCrossRefGoogle Scholar
  2. Bradley CA, Pedersen DK, Zhang GR, Pataky NR (2010) Occurrences of Diplodia leaf streak caused by Stenocarpella macrospora on corn (Zea mays) in Illinois. Plant Dis 94:1262CrossRefGoogle Scholar
  3. Bremer E, Kramer R (2000) Coping with osmotic challenges. Osmoregulation through accumulation and release of compatible solutes in bacteria. In: Storz G, Hennge-Aronis R (eds) Bacterial Stress Response. American Society For Microbiology, Washington, D.C., pp 79–97Google Scholar
  4. Brunk DG, Rich PJ, Rhodes D (1989) Genotypic variation for glycine betaine among public inbreds of maize. Plant Physiol 91:1122–1125PubMedCentralPubMedCrossRefGoogle Scholar
  5. Burlot L, Cherton J-C, Convert O, Correia L, Dennetiere B (2003) New chaetoglobosins from maize infested by Phomopsis leptostromiformis fungi. Production, identification, and semi-synthesis. Spectroscopy 17:725–734CrossRefGoogle Scholar
  6. Cutler HG, Crumley FG, Cox RH, Cole RJ, Dorner JW, Springer JP, Laterell FM, Thean JE, Rossi AE (1980) Chaetoglobosin K: a new plant growth inhibitor and toxin from Diplodia macrospora. J Agric Food Chem 28:139–142PubMedCrossRefGoogle Scholar
  7. Dien BS, Wicklow DT, Singh V, Moreau RA, Winkler-Moser JK, Cotta MA (2012) Influence of Stenocarpella maydis infected corn on the composition of corn kernel and its conversion into ethanol. Cereal Chem 89:15–23CrossRefGoogle Scholar
  8. Fincham JE, Hewlett R, DeGraaf AS, Taljaard JJF, Steytler JG, Rabie CJ, Seier JV, Venter FS, Woodruff CW, Wynchank S (1991) Mycotoxic peripheral myelinopathy, myopathy and hepatitis caused by Diplodia maydis on vervet monkeys. J Med Primatol 20:240–250PubMedGoogle Scholar
  9. Jakobsen AN, Aasen IM, Strøm AR (2007) Endogenously synthesized (−) -proto-quercitol and glycine betaine are principal compatible solutes of Schizochytrium sp. strain S8 (ATCC 20889) and three new isolates of phylogenetically related thraustochytrids. Appl Environ Microbiol 73:5848–5856PubMedCentralPubMedCrossRefGoogle Scholar
  10. Kellerman TS, Coetzer JAW, Naude TW, Botha CJ (2005) Plant Poisonings and Mycotoxicoses of Livestock in Southern Africa, 2nd edn. Oxford University Press, Cape TownGoogle Scholar
  11. LeRudulier D, Bernard T, Goas G, Hamelin J (1984) Osmoregulation in Klebsiella pneumoniae: enhancement of anaerobic growth and nitrogen fixation under stress by proline betaine, gamma-butyrobetaine, and other related compounds. Can J Microbiol 30:299–305CrossRefGoogle Scholar
  12. Marasas WFO (1977) Diplodiosis in cattle. In: Wyllie D, Morehouse GL (eds) Mycotoxic fungi, Mycotoxins and mycotoxicoses: an encyclopedic handbook, vol 2. Marcel Dekker, New York, pp 163–165Google Scholar
  13. McCormick SP (2013) Microbial detoxification of mycotoxins. J Chem Ecol 39:907–918PubMedCrossRefGoogle Scholar
  14. Naumann TA, Wicklow DT (2010) Allozyme-specific modification of a maize seed chitinase by a protein secreted by the fungal pathogen Stenocarpella maydis. Phytopathology 100:645–654PubMedCrossRefGoogle Scholar
  15. Odriozola E, Odeon A, Canton G, Clemente G, Escande A (2005) Diplodia maydis: a cause of death in cattle in Argentina. NZ Vet J 53:160–161CrossRefGoogle Scholar
  16. Petatan-Sagahon I, Anducho-Reyes MA, Silva-Rojas HV, Arana-Cuenca A, Tellez-Jurado A, Cardenez-Alvarez IO, Mercado-Flores Y (1995) Isolation of bacteria with antifungal activity against the phytopathogenic Stenocarpella maydis and Stenocarpella macrospora. Int J Mol Sci 12:5522–5537CrossRefGoogle Scholar
  17. Probst A, Tamm C (1982) Chaetoglobosin L, a new metabolite of Diplodia macrospora. Helv Chim Acta 65:1543–1546CrossRefGoogle Scholar
  18. Prozesky L, Kellerman TS, Swart PD, Maartens BP, Schultz RA (1994) Perinatal mortality in lambs exposed to cultures of Diplodia maydis during gestation. A pathological study of the central nervous system lesion. Onderstepoort J Vet 61:247–253Google Scholar
  19. Rhodes D, Hanson AD (1993) Quaternary ammonium and tertiary sulfonium compounds in higher plants. Annu Rev Plant Physiol Plant Mol Biol 44:357–384CrossRefGoogle Scholar
  20. Rogers KD (2011) Chemical investigations of fungicolous and endophytic fungi. Graduate College, The University of Iowa, Iowa City, Iowa, 201 ppGoogle Scholar
  21. Rossouw JD, Pretorius ZA, Silva HD, Lamkey KR (2009) Breeding for resistance to Stenocarpella ear rot in maize. In: Plant Breeding Review, vol. 31. WileyHoboken, pp 223–246Google Scholar
  22. Spoendlin C, Tamm C (1988) Chaetoglobosin M, a new metabolite of a mutant of Diplodia macrospora, belonging to the family of (1H-indol-3-yl)-substituted 10,11-diethyl-10,11-dinorcytochalasans. Helv Chim Acta 71:1881–1884CrossRefGoogle Scholar
  23. Snyman LD, Kellerman TS, Vleggaar R, Flett BC, Basson KM, Schultz RA (2011) Diplonine, a neurotoxin isolated from cultures of the fungus Stenocarpella maydis (Berk.) Sacc. that induces diplodiosis. J Agric Food Chem 59:9039–9044PubMedCrossRefGoogle Scholar
  24. Steyn PS, Wessels PL, Holzapfel CW, Potgieter DJJ, Louw WKA (1972) The isolation and structure of a toxic metabolite from Diplodia maydis (Berk.) Sacc. Tetrahedron 28:4775–4785CrossRefGoogle Scholar
  25. Upadhyay RK, Rohatgi L, Chaubey MK, Jain SC (2006) Ovipositional responses of the Pulse Beetle Bruchus chinensis (Coleoptera: Bruchidae) to extracts and compounds of Capparis decidua. J. Agric Food Chem 54:9747–9751CrossRefGoogle Scholar
  26. Wicklow DT, Rogers KD, Dowd PF, Gloer JB (2011) Bioactive metabolites from Stenocarpella maydis, a stalk and ear rot pathogen of maize. Fungal Biol 115:133–142PubMedCrossRefGoogle Scholar
  27. Wu S, Chen Y, Li Z, Yang L, Li S, Huang R (2008) Studies on the metabolites of endophytic fungus Phomopsis sp. from Azadirachta indica A. Juss. Nat Prod Res Develop 20:1014–1015Google Scholar

Copyright information

© Society for Mycotoxin Research and Springer-Verlag Berlin Heidelberg (outside the USA) 2014

Authors and Affiliations

  • Kristina D. Rogers
    • 1
  • Joseph C. Cannistra
    • 1
  • James B. Gloer
    • 1
  • Donald T. Wicklow
    • 2
  1. 1.Department of ChemistryUniversity of IowaIowa CityUSA
  2. 2.Bacterial Foodborne Pathogens and Mycology Research Unit, National Center for Agricultural Utilization Research, Agricultural Research ServiceU.S. Department of AgriculturePeoriaUSA

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