Fumonisin B1, a toxin produced by Fusarium verticillioides, modulates maize β-1,3-glucanase activities involved in defense response

Planta

Volumn 235, Issue 5, 2012, Pages 965-978

  Sánchez Rangel, Diana ^a   Sánchez Nieto, Sobeida ^a   Plasencia, Javier ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

1,3 Glucanase; Chitinase; Fumonisin B1; Fusarium verticillioides; Maize; Sphinganine analog mycotoxin

Indexed keywords

CHITINASE; FUMONISIN; FUMONISIN B1; GLUCAN 1,3 BETA GLUCOSIDASE; IMMUNOLOGICAL ADJUVANT; MYCOTOXIN; PATHOGENESIS RELATED PROTEINS, PLANT; PATHOGENESIS-RELATED PROTEINS, PLANT; VEGETABLE PROTEIN;

ARTICLE; DISEASE RESISTANCE; ENZYMOLOGY; FUSARIUM; IMMUNOLOGY; MAIZE; METABOLISM; MICROBIOLOGY; PLANT SEED;

ADJUVANTS, IMMUNOLOGIC; CHITINASE; DISEASE RESISTANCE; FUMONISINS; FUSARIUM; GLUCAN 1,3-BETA-GLUCOSIDASE; MYCOTOXINS; PLANT PROTEINS; SEEDS; ZEA MAYS;

ANIMALIA; GIBBERELLA FUJIKUROI; GIBBERELLA MONILIFORMIS; ZEA MAYS;

EID: 84860216054     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-011-1555-0     Document Type: Article

References (75)

1. Abbas HK, Tanaka T, Duke SO, Porter JK, Wray EM, Hodges L, Sessions AE, Wang E, Merrill AH, Riley RT (1994) Fumonisin- and AAL-toxin-induced disruption of sphingolipid metabolism with accumulation of free sphingoid bases. Plant Physiol 106: 1085-1093.
2. Abramovitch RB, Martin GB (2004) Strategies used by bacterial pathogens to suppress plant defenses. Curr Plant Biol 7: 356-364.
3. Asai T, Stone JM, Heard JE, Kovtun Y, Yorgey P, Sheen J, Ausubel FM (2000) Fumonisin B1-induced cell death in Arabidopsis protoplasts requires jasmonate, ethylene, and salicylate-dependent signaling pathways. Plant Cell 12: 1823-1835.
4. Bradford M (1976) A rapid and sensitive method for quantification of microgram quantities of protein utilizing the principle of protein-dye-binding. Anal Biochem 72: 248-254.
5. Brodersen P, Petersen M, Pike HM, Olszak B, Skov S, Odum N, Jørgensen LB, Brown RE, Mundy J (2002) Knockout of Arabidopsis accelerated-cell-death11 encoding a sphingosine transfer protein causes activation of programmed cell death and defense. Genes Dev 16: 490-502.
6. Campo S, Carrascal M, Coca M, Abian J, San Segundo B (2004) The defense response in germinating maize embryos against fungal infection: a proteomics approach. Proteomics 4: 383-396.
7. Caruso C, Chilosi G, Caporale C, Leonardo L, Bertini L, Magro P, Buonocore V (1999) Induction of pathogenesis-related proteins in germinating wheat seeds infected with Fusarium culmorum. Plant Sci 140: 87-97.
8. Casacuberta JM, Raventós D, Puigdoménech P, San Segundo B (1992) Expression of the gene encoding the PR-like protein PRms in germinating maize embryos. Mol Gen Genet 234: 97-104.
9. Collingel DB, Kragh KM, Mikkelsen JD, Nielsenl KK, Rasmussen U, Vad K (1993) Plant chitinases. Plant J 3: 31-40.
10. Cordero MJ, Raventós D, San Segundo B (1994) Differential expression and induction of chitinases and β-1, 3-glucanases in response to fungal infection during germination of maize seeds. Mol Plant Microbe Interact 7: 23-31.
11. Damasceno C, Bishop JG, Ripoll DR, Win J, Kamoun S, Rose JKC (2008) Structure of the glucanase inhibitor protein (GIP) family from Phytophthora species suggests coevolution with endo-beta-1, 3-glucanases. Mol Plant Microbe Interact 21: 820-830.
12. de la Torre-Hernandez ME, Rivas-San Vicente M, Greaves-Fernandez N, Cruz-Ortega R, Plasencia J (2010) Fumonisin B1 induces nuclease activation and SA accumulation through long-chain sphingoid base build-up in germinating maize. Physiol Mol Plant Pathol 74: 334-337.
13. Desjardins AE, Plattner RD (2000) Fumonisin B1-nonproducing strains of Fusarium verticillioides cause maize (Zea mays) ear infection and ear rot. J Agric Food Chem 48: 5773-5780.
14. Desjardins AE, Plattner RD, Nelson PE (1994) Fumonisin production and other traits of Fusarium moniliforme strains from maize in northeast Mexico. Appl Environ Microbiol 60: 1695-1697.
15. Desjardins AE, Plattner RD, Nelsen TC, Leslie JF (1995) Genetic analysis of fumonisin production and virulence of Gibberella fujikuroi mating population A (Fusarium moniliforme) on maize (Zea mays) seedlings. Appl Environ Microbiol 61: 79-86.
16. Desjardins AE, Busman M, Muhitch M, Proctor RH (2007) Complementary host-pathogen genetic analyses of the role of fumonisins in the Zea mays-Gibberella moniliformis interaction. Physiol Mol Plant Pathol 70: 149-160.
17. Doehlert DC, Knutson CA, Vesonder RF (1994) Phytotoxic effects of fumonisin B1 on maize seedling growth. Mycopathologia 127: 117-121.
18. Doko MB, Rapior S, Visconti AN, Schojoth JE (1995) Incidence and levels of fumonisin contamination in maize genotypes grown in Europe and Africa. J Agric Food Chem 43: 429-434.
19. Duncan KE, Howard RJ (2010) Biology of maize kernel infection by Fusarium verticillioides. Mol Plant Microbe Interact 23: 6-16.
20. Fadl AEM (1998) Occurence and toxigenicity of Fusarium moniliforme from freshly harvested maize ears with special references to fumonisin production in Egypt. Mycopathologia 140: 99-103.
21. Ferreira R, Monteiro S, Freitas R, Santos C, Chen Z, Batista L, Duarte J, Borges A, Teixeira A (2007) The role of plant defence proteins in fungal pathogenesis. Mol Plant Pathol 8: 677-700.
22. Glenn AE, Zitomer NC, Zimeri AM, Williams LD, Riley RT, Proctor RH (2008) Transformation-mediated complementation of a FUM gene cluster deletion in Fusarium verticillioides restores both fumonisin production and pathogenicity on maize seedlings. Mol Plant Microbe Interact 21: 87-97.
23. +-ATPase. Planta 221: 589-596.
24. Haïssam J, Lepoivre P (1998) Characterization of an Exo-β-1, 3-glucanase produced by Pichia animala Strain K, antagonist of Botrytis cinerea on apples. Phytopathology 88: 335-343.
25. Ham K, Wu S, Darvill A, Albersheim P (1997) Fungal pathogens secrete and inhibitor protein that distinguishes isoforms of plant pathogenesis-related endo-β-1, 3-glucanases. Plant J 11: 169-179.
26. Hoj PB, Fincher GB (1995) Molecular evolution of plant β-glucan endohydrolases. Plant J 7: 367-379.
27. Hu LB, Zhang T, Yang ZM, Zhou W, Shi ZQ (2009) Inhibition of fengycins on the production of fumonisin B1 from Fusarium verticillioides. Lett Appl Microbiol 48: 84-89.
28. Ito S, Ohnishi M, Fujino Y (1985) Investigation of sphingolipids in pea seeds. Agric Biol Chem 49: 539-540.
29. Ji C, Norton RA, Wicklow DT, Dowd P (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.
30. Kasprzewska A (2003) Plant Chitinases: regulation and function. Cell Mol Biol Lett 8: 809-824.
31. Kedera CJ, Leslie JF, Claflin LE (1994) Genetic diversity of Fusarium Section Liseola (Gibberella fujikuroi) in individual maize stalks. Phytopathology 84: 603-607.
32. Kedera CJ, Plattner RD, Desjardins AE (1999) Incidence of Fusrium spp. and levels of fumonisin B1 in maize western Kenya. Appl Environ Microbiol 65: 41-44.
33. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
34. Lam E, Kato N, Lawton M (2001) Programmed cell death, mitochondria and the plant hypersensitive response. Nature 411: 848-853.
35. Lawrence CB, Joosten MH, Tuzun S (1996) Differential induction of pathogenesis-related proteins in tomato by Alternaria solani and the association of a basic chitinase isozyme with resistance. Physiol Mol Plant Pathol 48: 361-377.
36. Leah R, Tommerup H, Svendsen I, Mundy J (1991) Biochemical and molecular characterization of three barley seed proteins with antifungal properties. J Biol Chem 266: 1564-1573.
37. Leubner-Metzger G (2003) Functions and regulation of β-1, 3-glucanases during seed germination, dormancy release and after-ripening. Seed Sci Res 13: 17-34.
38. Liang H, Yao N, Song JT, Luo S, Lu H, Greenberg JT (2003) Ceramides modulate programmed cell death in plants. Genes Dev 17: 2636-2641.
39. Loake G, Grant M (2007) Salicylic acid in plant defence the players and protagonists. Curr Plant Biol 10: 466-472.
40. Marín SV, Sanchis Vinas I, Canela R, Magan N (1995) Effect on water activity and temperature on growth and fumonisin B1 and B2 production by Fusarium proliferatum and F. moniliforme in grain. Lett Appl Microbiol 21: 298-301.
41. Markham JE, Li J, Cahoon E, Jaworski JG (2006) Separation and identification of major plant sphingolipid classes from leaves. J Biol Chem 281: 22684-22694.
42. Misas-Villamil J, van der Hoorn R (2008) Enzyme-inhibitor interactions at the plant-pathogen interface. Curr Plant Biol 11: 380-388.
43. Munkvold GP, McGee DC, Cariton WM (1997) Importance of different pathways for maize kernel infection by Fusarium moniliforme. Phytopathology 87: 209-217.
44. Murata T, Amarume S, Hattori T, Tokuyama S, Tokuyasu K, Kawagishi H, Usui T (2005) Purification and characterization of a chitinase from Amycolatopsis orientalies with N-acetyllactosamine-repeating unit releasing activity. Biochem Biophys Res Commun 336: 514-520.
45. Murillo I, Cavallarin L, San Segundo B (1997) The maize pathogenesis-related PRms protein localizes to plasmodesmata in maize radicles. Plant Cell 9: 145-156.
46. Naumann TA, Wicklow DT, Kendra DF (2010) Maize seed chitinase is modified by a protein secreted by Bipolaris zeicola. Physiol Mol Plant Pathol 74: 134-141.
47. O'Connell E, Piggott C, Tuohy M (2011) Purification of exo-1, 3-beta-glucanase, a new extracellular glucanolytic enzyme from Talaromyces emersonii. Appl Microbiol Biotechnol 89: 685-696.
48. Peer M, Stegmann M, Mueller MJ, Waller F (2010) Pseudomonas syringae infection triggers de novo synthesis of phytosphingosine from sphinganine in Arabidopsis thaliana. FEBS Lett 584: 4053-4056.
49. Proctor RH, Plattner RD, Desjardins AE, Busaman M, Butchko R (2006) Fumonisin production in the maize pathogen Fusarium verticillioides: genetic basis of naturally occurring chemical variation. J Agric Food Chem 54: 2424-2430.
50. Reese ET, Parrish FW (1971) Nojirimycin and d-glucono-1, 5-lactone as inhibitors of carbohydrases. Carbohyd Res 18: 381-388.
51. Rose JKC, Ham KS, Darvill AG, Albersheim P (2002) Molecular cloning and characterization of glucanase inhibitor proteins: coevolution of a counter defense mechanism by plant pathogens. Plant Cell 14: 1329-1345.
52. Sánchez-Rangel D, Plasencia J (2010) The role of sphinganine analog mycotoxins on the virulence of plant pathogenic fungi. Toxin Rev 29: 73-86.
53. Sánchez-Rangel D, SanJuan-Badillo A, Plasencia J (2005) Fumonisin production by Fusarium verticillioides strains isolated from maize in México and development of a polymerase chain reaction to detect potential toxigenic strains in grains. J Agric Food Chem 53: 8565-8571.
54. Saucedo-García M, Guevara-García A, González-Solís A, Cruz-García F, Vázquez-Santana S, Markham JE, Lozano-Rosas MG, Dietrich CR, Ramos-Vega M, Cahoon EB, Gavilanes-Ruíz M (2011) MPK6, sphinganine and the LCB2a gene from serine palmitoyltransferase are required in the signaling pathway that mediates cell death induced by long chain bases in Arabidopsis. New Phytol 191: 943-957.
55. Seetharaman K, Whitehead E, Keller N, Waniska R, Rooney L (1997) In vitro activity of sorghum seed antifungal proteins against grain mold pathogens. J Agric Food Chem 45: 3666-36671.
56. Sela-Buurlage M, Ponstein A, Bres-Vloemans S, Melchers L, van den Elzen P, Cornelissen B (1993) Only specific tobacco (Nicotiana tabacum) chitinases and β-1, 3-glucanases exhibit antifungal activity. Plant Physiol 101: 857-863.
57. Shi L, Bielawski J, Mu J, Dong H, Teng C, Zhang J, Yang X, Tomishige N, Hanada K, Hannun YA, Zuo J (2007) Involvement of sphingoid bases in mediating reactive oxygen intermediate production and programmed cell death in Arabidopsis. Cell Res 17: 1030-1040.
58. Stahl EA, Bishop JG (2000) Plant-pathogen arms race at the molecular level. Curr Opin Plant Biol 3: 299-304.
59. Stone JM, Heard JE, Asai T, Ausubel FM (2000) Simulation of fungal-mediated cell death by fumonisin B1 and selection of fumonisin B1-resistant (fbr) Arabidopsis mutants. Plant Cell 12: 1811-1822.
60. Sydenham EW, Shepard GS, Thiel PG (1992) Liquid chromatographic determination of fumonisin B1, B2 and B3 in foods and feeds. JAOAC Int 75: 313-316.
61. Takahashi Y, Berberich T, Kanzaki H, Matsumura H, Saitoh H, Kusano T, Terauchi R (2009) Serine palmitoyltransferase, the first step enzyme on sphingolipid biosynthesis, is involved in non-host resistance. Mol Plant Microbe Int 22: 31-38.
62. Takakuwa N, Saito K, Ohnishi M, Oda Y (2005) Determination of glucosylceramide contents in crop tissues and by-products from their processing. Bioresour Tech 96: 1089-1092.
63. Tian M, Huitema E, da Cunha L, Torto-Alalibo T, Kamoun S (2004) A Kazal-like extracellular serine protease inhibitor from Phytophthora infestans targets the tomato pathogenesis related protease P69B. J Biol Chem 279: 26370-26377.
64. Tian M, Benedetti B, Kamoun S (2005) A second Kazal-like protease inhibitor from Phytophthora infestans inhibits and interacts with the apoplastic pathogenesis-related protease P69B of tomato. Plant Physiol 138: 1785-1793.
65. Tian M, Win J, Song J, van der Hoorn R, van der Knaap E, Kamoun S (2007) A Phytophthora infestans cystatin-like protein targets a novel tomato papain-like apoplastic protease. Plant Physiol 143: 364-377.
66. van Asch MAJ, Rijkenberg FHJ, Coutinho TA (1992) Phytotoxicity of fumonisin B1, moniliformin and T-2 toxin to corn cultures. Phytopathology 82: 1330-1332.
67. van Hove F, Waalwijk C, Logrieco A, Munaut F, Moretti A (2011) Gibberella musae (Fusarium musae) sp. nov; a recently discovered species from banana is sister to F. verticillioides. Mycologia 103: 570-585.
68. Wang E, Norred WP, Bacon CW, Riley RT, Merril AH (1991) Inhibition of sphingolipid biosynthesis by fumonisins. J Biol Chem 266: 14486-14490.
69. Wang W, Yang X, Tangchaiburana S, Ndeh R, Markham JE, Tsegaye Y, Dunn TM, Wang GL, Bellizzi M, Parsons JF, Morrissey D, Bravo JE, Lynch DV, Xiao S (2008) An inositolphosphorylceramide synthase is involved in regulation of plant programmed cell death associated with defense in Arabidopsis. Plant Cell 20: 3163-3179.
70. Williams LD, Glenn AE, Bacon CW, Smith MA, Riley RT (2006) Fumonisin production and bioavailability to maize seedlings grown from seeds inoculated with Fusarium verticillioides and grown in natural soils. J Agric Food Chem 54: 5694-5700.
71. Williams LD, Glenn AE, Zimeri AM, Bacon CW, Smith MA, Riley RT (2007) Fumonisin disruption of ceramide biosynthesis in maize roots and the effects on plant development and Fusarium verticillioides-induced seedling disease. J Agric Food Chem 55: 2937-2946.
72. Windels CE, Burnes PM, Kommedahl T (1988) Five-years preservation of Fusarium species on silica gel and soil. Phytopathology 78: 107-109.
73. Wolpert TJ, Dunkle LD, Ciuffetti LM (2002) Host-selective toxins and avirulence determinants: what's in a name? Annu Rev Phytopathol 40: 251-285.
74. York WS, Qin Q, Rose J (2004) Proteinaceous inhibitors of endo-β-glucanases. Biochim Biophys Acta 1696: 223-233.
75. Zitomer NC, Jones S, Bacon C, Glenn AE, Baldwin T, Riley RT (2010) Translocation of sphingoid bases and their 1-phosphates, but not fumonisins, from roots to aerial tissues of maize seedlings watered with fumonisins. J Agric Food Chem 58: 7476-7481.