Bacterial endophytes from wild maize suppress fusarium graminearum in modern maize and inhibit mycotoxin accumulation

Frontiers in Plant Science

Volumn 6, Issue OCTOBER, 2015, Pages

  Mousa, Walaa K ^a,b   Shearer, Charles R ^a   Limay Rios, Victor ^a   Zhou, Ting ^c   Raizada, Manish N ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b Mansoura University 35516   (Egypt)

^c AGRICULTURE AND AGRI FOOD CANADA   (Canada)

Author keywords

Deoxynivalenol; Endophyte; Fusarium graminearum; Gibberella ear rot; Maize; Paenibacillus; Parviglumis; Zea diploperennis

Indexed keywords

EID: 84944318420     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00805     Document Type: Article

References (68)

1. Anthony, R. M., Brown, T. J., and French, G. L. (2000). Rapid diagnosis of bacteremia by universal amplification of 23S ribosomal DNA followed by hybridization to an oligonucleotide array. J. Clin. Microbiol. 38, 781-788.
2. Bacon, C. W., and Hinton, D. M. (2011). In planta reduction of maize seedling stalk lesions by the bacterial endophyte Bacillus mojavensis. Can. J. Microbiol. 57, 485-492. doi: 10.1139/w11-031
3. Beatty, P. H., and Jensen, S. E. (2002). Paenibacillus polymyxa produces fusaricidin-type antifungal antibiotics active against Leptosphaeria maculans, the causative agent of blackleg disease of canola. Can. J. Microbiol. 48, 159-169. doi: 10.1139/w02-002
4. Benrey, B., Callejas, A., Rios, L., Oyama, K., and Denno, R. F. (1998). The effects of domestication of Brassica and Phaseolus on the interaction between phytophagous insects and parasitoids. Biol. Control 11, 130-140. doi: 10.1006/bcon.1997.0590
5. Calvin, N., and Hanawalt, P. (1988). High-efficiency transformation of bacterial cells by electroporation. J. Bacteriol. 170, 2796-2801.
6. Chen, Y. H., Gols, R., and Benrey, B. (2015). Crop domestication and its impact on naturally selected trophic interactions. Annu. Rev. Entomol. 60, 35-58. doi: 10.1146/annurev-ento-010814-020601
7. Choi, S.-K., Park, S.-Y., Kim, R., Lee, C.-H., Kim, J. F., and Park, S.-H. (2008). Identification and functional analysis of the fusaricidin biosynthetic gene of Paenibacillus polymyxa E681. Biochem. Biophys. Res. Commun. 365, 89-95. doi: 10.1016/j.bbrc.2007.10.147
8. Chulze, S., Palazzini, J., Torres, A., Barros, G., Ponsone, M., Geisen, R., et al. (2014). Biological control as a strategy to reduce the impact of mycotoxins in peanuts, grapes and cereals in Argentina. Food Addit. Contam. 32, 471-479. doi: 10.1080/19440049.2014.984245
9. Cotta, S. R., Voll, R. E., de Jurelevicius, D. A., Marques, J. M., and Seldin, L. (2014). Endophytic microbial community in two transgenic maize genotypes and in their near-isogenic non-transgenic maize genotype. BMC Microbiol. 14:332. doi: 10.1186/s12866-014-0332-1
10. Dávila-Flores, A. M., DeWitt, T. J., and Bernal, J. S. (2013). Facilitated by nature and agriculture: performance of a specialist herbivore improves with host-plant life history evolution, domestication, and breeding. Oecologia 173, 1425-1437. doi: 10.1007/s00442-013-2728-2
11. Dereeper, A., Audic, S., Claverie, J.-M., and Blanc, G. (2010). BLAST-EXPLORER helps you building datasets for phylogenetic analysis. BMC Evol. Biol. 10:8. doi: 10.1186/1471-2148-10-8
12. Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., et al. (2008). Phylogeny. fr: robust phylogenetic analysis for the non-specialist. Nucl. Acids Res. 36, 465-469. doi: 10.1093/nar/gkn180
13. Desjardins, A. E., Plattner, R. D., and Gordon, T. R. (2000). Gibberella fujikuroimating population A and Fusarium subglutinans from teosinte species and maize from Mexico and Central America. Mycol. Res. 104, 865-872. doi: 10.1017/S0953756299002002
14. Edwards, S. G. (2004). Influence of agricultural practices on Fusarium infection of cereals and subsequent contamination of grain by trichothecene mycotoxins. Toxicol. Lett. 153, 29-35. doi: 10.1016/j.toxlet.2004.04.022
15. Eilenberg, J. (2006). “Concepts and visions of biological control,” in An Ecological and Societal Approach to Biological Control, eds J. Eilenberg and H. M. T. Hokkanen (Dordrecht: Springer), 1-11.
16. Gaudin, A. C. M., McClymont, S. A., Holmes, B. M., Lyons, E., and Raizada, M. N. (2011). Novel temporal, fine-scale and growth variation phenotypes in roots of adult-stage maize (Zea mays L.) in response to low nitrogen stress. Plant Cell Environ. 34, 2122-2137. doi: 10.1111/j.1365-3040.2011.02409.x
17. Gols, R., Wagenaar, R., Bukovinszky, T., Dam, N. M. V., Dicke, M., Bullock, J. M., et al. (2008). Genetic variation in defense chemistry in wild cabbages affects herbivores and their endoparasitoids. Ecology 89, 1616-1626. doi: 10.1890/07-0873.1
18. Haggag, W., and Timmusk, S. (2008). Colonization of peanut roots by biofilm-forming Paenibacillus polymyxa initiates biocontrol against crown rot disease. J. Appl. Microbiol. 104, 961-969. doi: 10.1111/j.1365-2672.2007.03611.x
19. Han, J. W., Kim, E. Y., Lee, J. M., Kim, Y. S., Bang, E., and Kim, B. S. (2012). Site-directed modification of the adenylation domain of the fusaricidin nonribosomal peptide synthetase for enhanced production of fusaricidin analogs. Biotechnol. Lett. 34, 1327-1334. doi: 10.1007/s10529-012-0913-8
20. Hassan, Y. I., Watts, C., Li, X.-Z., and Zhou, T. (2015). A novel peptide-binding motifs inference approach to understand deoxynivalenol molecular toxicity. Toxins 7, 1989-2005. doi: 10.3390/toxins7061989
21. Hayat, M. A. (1989). Principles and Techniques of Electron Microscopy: Biological Applications. New York, NY: CRC Press.
22. He, J., Boland, G., and Zhou, T. (2009). Concurrent selection for microbial suppression of Fusarium graminearum, Fusarium Head Blight and deoxynivalenol in wheat. J. Appl. Microbiol. 106, 1805-1817. doi: 10.1111/j.1365-2672.2009.04147.x
23. He, Z., Kisla, D., Zhang, L., Yuan, C., Green-Church, K. B., and Yousef, A. E. (2007). Isolation and identification of a Paenibacillus polymyxa strain that coproduces a novel lantibiotic and polymyxin. Appl. Environ. Microbiol. 73, 168-178. doi: 10.1128/AEM.02023-06
24. Iltis, H. H., and Doebley, J. F. (1980). Taxonomy of Zea (Gramineae). II. Subspecific categories in the Zea mays complex and a generic synopsis. Am. J. Bot. 67, 994-1004. doi: 10.2307/2442442
25. Janisiewicz, W. J., Jurick, W. M., Vico, I., Peter, K. A., and Buyer, J. S. (2013). Culturable bacteria from plum fruit surfaces and their potential for controlling brown rot after harvest. Postharvest Biol. Technol. 76, 145-151. doi: 10.1016/j.postharvbio.2012.10.004
26. Jelinek, C. F., Pohland, A., and Wood, G. (1988). Worldwide occurrence of mycotoxins in foods and feeds-an update. J. Assoc. Off. Anal. Chem. 72, 223-230.
27. Johnston-Monje, D., and Raizada, M. N. (2011). Conservation and diversity of seed associated endophytes in across boundaries of evolution, ethnography and ecology. PLoS ONE 6:e20396. doi: 10.1371/journal.pone.0020396
28. Johnston-Monje, D., Mousa, W. K., Lazarovits, G., and Raizada, M. N. (2014). Impact of swapping soils on the endophytic bacterial communities of pre-domesticated, ancient and modern maize. BMC Plant Biol. 14:233. doi: 10.1186/s12870-014-0233-3
29. Kajimura, Y., and Kaneda, M. (1996). Fusaricidin A, a new depsipeptide antibiotic produced by Bacillus polymyxa kt-8 taxonomy, fermentation, isolation, structure elucidation and biological activity. J. Antibiot. 49, 129-135. doi: 10.7164/antibiotics.49.129
30. Kajimura, Y., and Kaneda, M. (1997). Fusaricidins B, C and D, new depsipeptide antibiotics produced by Bacillus polymyxa kt-8: isolation, structure elucidation and biological activity. J. Antibiot. 50, 220-228. doi: 10.7164/antibiotics.50.220
31. Kebebe, A., Reid, L., Zhu, X., Wu, J., Woldemariam, T., Voloaca, C., et al. (2015). Relationship between kernel drydown rate and resistance to Gibberella Ear Rot in maize. Euphytica 201, 79-88. doi: 10.1007/s10681-014-1185-2
32. Lange, E. S., Balmer, D., Mauch−Mani, B., and Turlings, T. C. (2014). Insect and pathogen attack and resistance in maize and its wild ancestors, the teosintes. New Phytol. 204, 329-341. doi: 10.1111/nph.13005
33. Ling, N., Huang, Q., Guo, S., and Shen, Q. (2011). Paenibacillus polymyxa SQR-21 systemically affects root exudates of watermelon to decrease the conidial germination of Fusarium oxysporum f. sp. niveum. Plant soil 341, 485-493. doi: 10.1007/s11104-010-0660-3
34. MacDonald, M. V., and Chapman, R. (1997). The incidence of Fusarium moniliformeon maize from Central America, Africa and Asia during 1992-1995. Plant Pathol. 46, 112-125. doi: 10.1046/j.1365-3059.1997.d01-200.x
35. Magnani, G., Cruz, L., Weber, H., Bespalhok, J., Daros, E., Baura, V., et al. (2013). Culture-independent analysis of endophytic bacterial communities associated with Brazilian sugarcane. Genet. Mol. Res. 12, 4549-4558. doi: 10.4238/2013.October.15.3
36. Matsuoka, Y., Vigouroux, Y., Goodman, M. M., Sanchez, J., Buckler, E., and Doebley, J. (2002). A single domestication for maize shown by multilocus microsatellite genotyping. Proc. Natl. Acad. Sci. U.S.A. 99, 6080-6084. doi: 10.1073/pnas.052125199
37. Mei, L., Liang, Y., Zhang, L., Wang, Y., and Guo, Y. (2014). Induced systemic resistance and growth promotion in tomato by an indole-3-acetic acid-producing strain of Paenibacillus polymyxa. Ann. Appl. Biol. 165, 270-279. doi: 10.1111/aab.12135
38. Mousa, W. K., and Raizada, M. N. (2013). The diversity of anti-microbial secondary metabolites produced by fungal endophytes: an interdisciplinary perspective. Front. Microbiol. 4:65. doi: 10.3389/fmicb.2013.00065
39. Mousa, W. K., and Raizada, M. N. (2015). Biodiversity of genes encoding anti-microbial traits within plant associated microbes. Front. Plant Sci. 6:231. doi: 10.3389/fpls.2015.00231
40. Moussa, T. A. A., Almaghrabi, O. A., and Abdel-Moneim, T. S. (2013). Biological control of the wheat root rot caused by Fusarium graminearum using some PGPR strains in Saudi Arabia. Ann. Appl. Biol. 163, 72-81. doi: 10.1111/aab.12034
41. Munkvold, G. P. (2003a). Cultural and genetic approaches to managing mycotoxins in maize. Ann. Rev. Phytopathol. 41, 99-116. doi: 10.1146/annurev.phyto.41.052002.095510
42. Munkvold, G. P. (2003b). “Epidemiology of Fusarium diseases and their mycotoxins in maize ears,” in Epidemiology of Mycotoxin Producing Fungi, eds X. Xu, J. A. Bailey, and B. M. Cooke (Dordrecht: Springer), 705-713.
43. Naghmouchi, K., Hammami, R., Fliss, I., Teather, R., Baah, J., and Drider, D. (2012). Colistin A and colistin B among inhibitory substances of Paenibacillus polymyxaJB05-01-1. Arch. Microbiol. 194, 363-370. doi: 10.1007/s00203-011-0764-z
44. Paulus, H., and Gray, E. (1964). The biosynthesis of polymyxin B by growing cultures of Bacillus polymyxa. J. Biol. Chem. 239, 865-871.
45. Piperno, D. R., Ranere, A. J., Holst, I., Iriarte, J., and Dickau, R. (2009). Starch grain and phytolith evidence for early ninth millennium BP maize from the Central Balsas River Valley, Mexico. Proc. Natl. Acad. Sci. U.S.A. 106, 5019-5024. doi: 10.1073/pnas.0812525106
46. Raza, W., Yang, W., and Shen, Q. (2008). Paenibacillus polymyxa: antibiotics, hydrolytic enzymes and hazard assessment. J. Plant Pathol. 90, 419-430. doi: 10.4454/jpp.v90i3.683
47. Raza, W., Yang, X., Wu, H., Wang, Y., Xu, Y., and Shen, Q. (2009). Isolation and characterisation of fusaricidin-type compound-producing strain of Paenibacillus polymyxa SQR-21 active against Fusarium oxysporum f. sp. nevium. Eur. J. Plant Pathol. 125, 471-483. doi: 10.1007/s10658-009-9496-1
48. Raza, W., Yuan, J., Ling, N., Huang, Q., and Shen, Q. (2015). Production of volatile organic compounds by an antagonistic strain Paenibacillus polymyxa WR-2 in the presence of root exudates and organic fertilizer and their antifungal activity against Fusarium oxysporum f. sp. niveum. Biol. Control 80, 89-95. doi: 10.1016/j.biocontrol.2014.09.004
49. Reid, L., Zhu, X., Parker, A., and Yan, W. (2009). Increased resistance to Ustilago zeae and Fusarium verticilliodes in maize inbred lines bred for Fusarium graminearumresistance. Euphytica 165, 567-578. doi: 10.1007/s10681-008-9782-6
50. Rodrigues, I., and Naehrer, K. (2012). A three-year survey on the worldwide occurrence of mycotoxins in feedstuffs and feed. Toxins 4, 663-675. doi: 10.3390/toxins4090663
51. Rosenthal, J. P., and Dirzo, R. (1997). Effects of life history, domestication and agronomic selection on plant defence against insects: evidence from maizes and wild relatives. Evol. Ecol. 11, 337-355. doi: 10.1023/A:1018420504439
52. Sánchez−Velásquez, L. R., Ezcurra, E., Martínez−Ramos, M., Álvarez-Buylla, E., and Lorente, R. (2002). Population dynamics of Zea diploperennis, an endangered perennial herb: effect of slash and burn practice. J. Ecol. 90, 684-692. doi: 10.1046/j.1365-2745.2002.00702.x
53. Schaafsma, A. W., Limay-Rios, V., Paul, D. E., and Miller, J. D. (2009). Mycotoxins in fuel ethanol co-products derived from maize: a mass balance for deoxynivalenol. J. Sci. Food Agri. 89, 1574-1580. doi: 10.1002/jsfa.3626
54. Schmidt, R., Köberl, M., Mostafa, A., Ramadan, E. M., Monschein, M., Jensen, K. B., et al. (2014). Effects of bacterial inoculants on the indigenous microbiome and secondary metabolites of chamomile plants. Front. Microbiol. 5:64. doi: 10.3389/fmicb.2014.00064
55. Shi, C., Yan, P., Li, J., Wu, H., Li, Q., and Guan, S. (2014). Biocontrol of Fusarium graminearum growth and deoxynivalenol production in wheat kernels with bacterial antagonists. Int. J. Environ. Res. Public Health 11, 1094-1105. doi: 10.3390/ijerph110101094
56. Smith, J. S. C., Duvick, D. N., Smith, O. S., Cooper, M., and Feng, L. (2004). Changes in pedigree backgrounds of Pioneer brand maize hybrids widely grown from 1930 to 1999. Crop Sci. 44, 1935-1946. doi: 10.2135/cropsci2004.1935
57. Sutton, J. (1982). Epidemiology of wheat head blight and maize ear rot caused by Fusarium graminearum. Can. J. Plant Pathol. 4, 195-209. doi: 10.1080/07060668209501326
58. Timmusk, S., Grantcharova, N., and Wagner, E. G. H. (2005). Paenibacillus polymyxainvades plant roots and forms biofilms. Appl. Environ. Microbiol. 71, 7292-7300. doi: 10.1128/AEM.71.11.7292-7300.2005
59. Timmusk, S., Van West, P., Gow, N., and Paul Huffstutler, R. (2009). Paenibacillus polymyxa antagonizes oomycete plant pathogens Phytophthora palmivora and Pythium aphanidermatum. J. Appl. Microbiol. 106, 1473-1481. doi: 10.1111/j.1365-2672.2009.04123.x
60. van der Lee, T., Zhang, H., van Diepeningen, A., and Waalwijk, C. (2014). Biogeography of Fusarium graminearum species complex and chemotypes: a review. Food Add. Contam. 32, 53-460. doi: 10.1080/19440049.2014.984244
61. Voss, K. A. (2010). A new perspective on deoxynivalenol and growth suppression. Toxicol. Sci. 113, 281-283. doi: 10.1093/toxsci/kfp287
62. Wang, E. T., Tan, Z. Y., Guo, X. W., Rodríguez-Duran, R., Boll, G., and Martínez-Romero, E. (2006). Diverse endophytic bacteria isolated from a leguminous tree Conzattia multiflora grown in Mexico. Arch. Microbiol. 186, 251-259. doi: 10.1007/s00203-006-0141-5
63. Wang, H., Nussbaum-Wagler, T., Li, B., Zhao, Q., Vigouroux, Y., Faller, M., et al. (2005). The origin of the naked grains of maize. Nature 436, 714-719. doi: 10.1038/nature03863
64. Wang, K., Kang, L., Anand, A., Lazarovits, G., and Mysore, K. S. (2007). Monitoring in planta bacterial infection at both cellular and whole-plant levels using the green fluorescent protein variant GFPuv. New Phytol. 174, 212-223. doi: 10.1111/j.1469-8137.2007.01999.x
65. Wegulo, S. N., Bockus, W. W., Nopsa, J. H., De Wolf, E. D., Eskridge, K. M., Peiris, K. H., et al. (2011). Effects of integrating cultivar resistance and fungicide application on Fusarium Head Blight and deoxynivalenol in winter wheat. Plant Dis. 95, 554-560. doi: 10.1094/PDIS-07-10-0495
66. White, J. F., and Bacon, C. W. (2012). The secret world of endophytes in perspective. Fungal Ecol. 5, 287-288. doi: 10.1016/j.funeco.2012.03.003
67. Wilson, D. (1995). Endophyte: the evolution of a term, and clarification of its use and definition. Oikos 73, 274-276. doi: 10.2307/3545919
68. Xu, S. J., and Kim, B. S. (2014). Biocontrol of Fusarium crown and root rot and promotion of growth of tomato by Paenibacillus strains isolated from soil. Mycobiology 42, 158-166. doi: 10.5941/MYCO.2014.42.2.158