Resistance to Aspergillus flavus in maize and peanut: Molecular biology, breeding, environmental stress, and future perspectives

Crop Journal

Volumn 3, Issue 3, 2015, Pages 229-237

  Fountain, Jake C ^a   Khera, Pawan ^a,b,c   Yang, Liming ^a,c,d   Nayak, Spurthi N ^b   Scully, Brian T ^c   Lee, Robert D ^e   Chen, Zhi Yuan ^f   Kemerait, Robert C ^a   Varshney, Rajeev K ^b   Guo, Baozhu ^c  

^a UNIVERSITY OF GEORGIA   (United States)

^b INTERNATIONAL CROPS RESEARCH INSTITUTE FOR THE SEMI ARID TROPICS ICRISAT   (India)

^c AGRICULTURAL RESEARCH SERVICE   (United States)

^d HUAIYIN NORMAL UNIVERSITY   (China)

^e UNIVERSITY OF GEORGIA   (United States)

^f LOUISIANA STATE UNIVERSITY   (United States)

Author keywords

Aflatoxin contamination; Host resistance; Molecular breeding; Reactive oxygen species; ROS

Indexed keywords

EID: 85009110433     PISSN: 20955421     EISSN: 22145141     Source Type: Journal    
DOI: 10.1016/j.cj.2015.02.003     Document Type: Article

References (89)

1. [1] Horn, B.W., Moore, G.G., Carbone, I., Sexual reproduction in Aspergillus flavus. Mycologia 101 (2009), 423–429.
2. [2] Horn, B.W., Ramirez-Prado, J.H., Carbone, I., The sexual state of Aspergillus parasiticus. Mycologia 101 (2009), 275–280.
3. [3] Diener, U.L., Cole, R.J., Sanders, T.H., Payne, G.A., Lee, S., Klich, M.A., Epidemiology of aflatoxin formation by Aspergillus flavus. Annu. Rev. Phytopathol. 25 (1987), 249–270.
4. [4] Wu, F., Khlangwiset, P., Health economic impacts and cost-effectiveness of aflatoxin reduction strategies in Africa: case studies in biocontrol and postharvest interventions. Food Addit. Contam. A 27 (2010), 496–509.
5. [5] Fountain, J.C., Scully, B.T., Ni, X., Kemerait, R.C., Lee, R.D., Chen, Z.Y., Guo, B.Z., Environmental influences on maize–Aspergillus flavus interactions and aflatoxin production. Front. Microbiol. 5 (2014), 1–7.
6. [6] Shephard, G.S., Impact of mycotoxins on human health in developing countries. Food Addit. Contam. A 25 (2008), 146–151.
7. [7] Wild, C.P., Gong, Y.Y., Mycotoxins and human disease: a largely ignored global health issue. Carcinogenesis 31 (2010), 71–82.
8. [8] Amaike, S., Keller, N.P., Aspergillus flavus. Annu. Rev. Phytopathol. 49 (2011), 107–133.
9. [9] Kelley, R.Y., Williams, W.P., Mylroie, J.E., Boykin, D.L., Harper, J.W., Windham, G.L., Ankala, A., Shan, X., Identification of maize genes associated with host plant resistance or susceptibility to Aspergillus flavus infection and aflatoxin accumulation. PLoS ONE, 7, 2012, 5.
10. [10] Liang, X., Luo, M., Guo, B.Z., Resistance mechanisms to Aspergillus flavus infection and aflatoxin contamination in peanut (Arachis hypogaea). Plant Pathol. J. 5 (2006), 115–124.
11. [11] Chadha, P., Das, R.H., A pathogenesis related protein, AhPR10 from peanut: an insight of its mode of antifungal activity. Planta 225 (2006), 213–222.
12. [12] Chen, Z.Y., Brown, R.L., Damann, K.E., Cleveland, T.E., Identification of a maize kernel stress-related protein and its effect on aflatoxin accumulation. Phytopathology 94 (2004), 938–945.
13. [13] Chen, Z.Y., Brown, R.L., Lax, A.R., Guo, B.Z., Cleveland, T.E., Russin, J.S., Resistance to Aspergillus flavus in corn kernels is associated with a 14-kDa protein. Phytopathology 88 (1998), 276–281.
14. [14] Chen, Z.Y., Brown, R.L., Menkir, A., Cleveland, T.E., Identification of resistance-associated proteins in closely-related maize lines varying in aflatoxin accumulation. Mol. Breed. 30 (2012), 53–68.
15. [15] Chen, Z.Y., Brown, R.L., Rajasekaran, K., Damann, K.E., Cleveland, T.E., Identification of a maize kernel pathogenesis-related protein and evidence for its involvement in resistance to Aspergillus flavus infection and aflatoxin production. Phytopathology 96 (2006), 87–95.
16. [16] Chen, Z.Y., Brown, R.L., Russin, J.S., Lax, A.R., Cleveland, T.E., A corn trypsin inhibitor with antifungal activity inhibits Aspergillus flavus α-amylase. Phytopathology 89 (1999), 902–907.
17. [17] Moore, K.G., Price, M.S., Boston, R.S., Weissinger, A.K., Payne, G.A., A chitinase from Tex6 maize kernels inhibits growth of Aspergillus flavus. Phytopathology 94 (2004), 82–87.
18. [18] Pechanova, O., Pechan, T., Williams, W.P., Luthe, D.S., Proteomic analysis of the maize rachis: potential roles of constitutive and induced proteins in resistance to Aspergillus flavus infection and aflatoxin accumulation. Proteomics 11 (2011), 114–127.
19. [19] Roze, L.V., Hong, S.Y., Linz, J.E., Aflatoxin biosynthesis: current frontiers. Annu. Rev. Food Sci. Tech. 4 (2013), 293–311.
20. [20] Wang, T., Chen, X.-P., Li, H.-F., Liu, H.-Y., Hong, Y.-B., Yang, Q.-L., Chi, X.-Y., Yang, Z., Yu, S.-L., Li, L., Liang, X.-Q., Transcriptome identification of the resistance-associated genes (RAGs) to Aspergillus flavus infection in pre-harvested peanut (Arachis hypogaea). Funct. Plant Biol. 40 (2013), 292–303.
21. [21] Guo, B.Z., Chen, Z.Y., Lee, R.D., Scully, B.T., Drought stress and preharvest aflatoxin contamination in agricultural commodities: genetics, genomics and proteomics. J. Int. Plant Biol. 50 (2008), 1281–1291.
22. [22] Jiang, T., Fountain, J., Davis, G., Kemerait, R., Scully, B., Lee, R.D., Guo, B., Root morphology and gene expression analysis in response to drought stress in maize (Zea mays). Plant Mol. Biol. Report. 30 (2012), 360–369.
23. [23] Scully, B.T., Krakowsky, M.D., Ni, X., Wilson, J.P., Lee, R.D., Guo, B.Z., Preharvest aflatoxin contamination of corn and other grain crops grown on the U.S. Southeastern Coastal Plain. Toxin Rev. 28 (2009), 169–179.
24. [24] Torres, A.M., Barros, G.G., Palacios, S.A., Chulze, S.N., Battilani, P., Review on pre- and post-harvest management of peanuts to minimize aflatoxin contamination. Food Res. Int. 62 (2014), 11–19.
25. [25] Yang, L., Fountain, J.C., Jiang, T., Scully, B.T., Lee, R.D., Kemerait, R.C., Chen, S., Guo, B., Protein profiles reveal diverse drought-responsive signaling pathways in maize kernels. Int. J. Mol. Sci. 15 (2014), 18892–18918.
26. [26] Guo, B.Z., Yu, J., Ni, X., Lee, R.D., Kemerait, R.C., Scully, B.T., Crop stress and aflatoxin contamination: perspectives and prevention strategies. Venkateswarlu, B., Shankerk, A.K., Shanker, C., Makeswari, M., (eds.) Crop Stress and Its Management: Perspectives and Strategies, 2012, Springer, New York, 399–427.
27. [27] Fountain, J.C., Raruang, Y., Luo, M., Brown, R.L., Guo, B.Z., Chen, Z.Y., Potential roles of WRKY transcription factors in regulating host defense responses during Aspergillus flavus infection of immature maize kernels. Physiol. Mol. Plant Pathol. 89 (2015), 31–40.
28. [28] Rushton, P.J., Somssich, I.E., Ringler, P., Shen, Q.J., WRKY transcription factors. Trends Plant Sci. 15 (2010), 247–258.
29. [29] Miao, Y., Laun, T., Zimmermann, P., Zentgraf, U., Targets of the WRKY53 transcription factor and its role during leaf senescence in Arabidopsis. Plant Mol. Biol. 55 (2004), 853–867.
30. [30] Popescu, S.C., Popescu, G.V., Bachan, S., Zhang, Z., Seay, M., Gerstein, M., Snyder, M., Dinesh-Kumar, S.P., Differential binding of calmodulin-related proteins to their targets revealed through high-density Arabidopsis protein microarrays. Proc. Natl. Acad. Sci. U. S. A. 104 (2007), 4730–4735.
31. [31] Li, H., Gao, Y., Xu, H., Dai, Y., Deng, D., Chen, J., ZmWRKY33, a WRKY maize transcription factor conferring enhanced salt stress tolerances in Arabidopsis. Plant Growth Regul. 70 (2013), 207–216.
32. + antiporter genes conferring tolerance to salinity in interspecific derivatives of peanut (Arachis hypogaea L.). Aust. J. Crop. Sci. 7 (2013), 1173–1180.
33. [33] Gill, S.S., Tuteja, N., Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48 (2010), 909–930.
34. [34] Eulgem, T., Somssich, I.E., Networks of WRKY transcription factors in defense signaling. Curr. Opin. Plant Biol. 10 (2007), 366–371.
35. [35] Miao, Y., Laun, T.M., Smykowski, A., Zentgraf, U., Arabidopsis MEKK1 can take a short cut: it can directly interact with senescence-related WRKY53 transcription factor on the protein level and can bind to its promoter. Plant Mol. Biol. 65 (2007), 63–76.
36. [36] Wan, J., Zhang, S., Stacey, G., Activation of a mitogen-activated protein kinase pathway in Arabidopsis by chitin. Mol. Plant Pathol. 5 (2004), 125–135.
37. [37] Zhang, B., Ramonell, K., Somerville, S., Stacey, G., Characterization of early, chitin-induced gene expression in Arabidopsis. Mol. Plant-Microbe Interact. 15 (2002), 963–970.
38. 2 + conduction by plant cyclic nucleotide gated channels and associated signaling components in pathogen defense signal transduction cascades. New Phytol. 190 (2011), 566–572.
39. [39] Jiang, M., Zhang, J., Cross-talk between calcium and reactive oxygen species originated from NADPH oxidase in abscisic acid-induced antioxidant defence in leaves of maize seedlings. Plant Cell Environ. 26 (2003), 929–939.
40. 2 production in leaves of maize (Zea mays) plants. New Phytol. 173 (2007), 27–38.
41. [41] Roze, L.V., Chanda, A., Wee, J., Awad, D., Linz, J.E., Stress-related transcription factor AtfB integrates secondary metabolism with oxidative stress response in aspergilla. J. Biol. Chem. 286 (2011), 35137–35148.
42. [42] Affeldt, K.J., Brodhagen, M., Keller, N.P., Aspergillus oxylipin signaling and quorum sensing pathways depend on G protein-coupled receptors. Toxins 4 (2012), 695–717.
43. [43] Gao, X., Kolomiets, M.V., Host-derived lipids and oxylipins are crucial signals in modulating mycotoxin production by fungi. Toxin Rev. 28 (2009), 79–88.
44. [44] Grice, C.M., Bertuzzi, M., Bignell, E.M., Receptor-mediated signaling in Aspergillus fumigatus. Front. Microbiol., 4, 2013, 26.
45. [45] Chanda, A., Roze, L.V., Kang, S., Artymovich, K.A., Hicks, G.R., Raikhel, N.V., Calvo, A.M., Linz, J.E., A key role for vesicles in fungal secondary metabolism. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 19533–19538.
46. [46] Chanda, A., Roze, L.V., Linz, J.E., Aflatoxin export in Aspergillus parasiticus: a possible role for exocytosis. Eukaryot. Cell 9 (2010), 1724–1727.
47. [47] Linz, J.E., Chanda, A., Hong, S.Y., Whitten, D.A., Wilkerson, C., Roze, L.V., Proteomic and biochemical evidence support a role for transport vesicles and endosomes in stress response and secondary metabolism in Aspergillus parasiticus. J. Proteome Res. 11 (2011), 767–775.
48. [48] Roze, L.V., Chanda, A., Linz, J.E., Compartmentalization and molecular traffic in secondary metabolism: a new understanding of established cellular processes. Fungal Genet. Biol. 48 (2011), 35–48.
49. 1-induced DNA damage and its repair. Cancer Lett. 241 (2006), 174–183.
50. [50] Guengerich, F.P., Johnson, W.W., Shimada, T., Ueng, Y.F., Yamazaki, H., Langouët, S., Activation and detoxication of aflatoxin B1. Mutat. Res. 402 (1998), 121–128.
51. [51] Jameson, N., Georgelis, N., Fouladbash, E., Martens, S., Hannah, L.C., Lal, S., Helitron mediated amplification of cytochrome P450 monooxygenase gene in maize. Plant Mol. Biol. 67 (2008), 295–304.
52. [52] Mideros, S.X., Windham, G.L., Williams, W.P., Nelson, R.J., Aspergillus flavus biomass in maize estimated by quantitative real-time polymerase chain reaction is strongly correlated with aflatoxin concentration. Plant Dis. 93 (2009), 1163–1170.
53. [53] Farooq, M., Wahid, A., Kobayashi, N., Fujita, D., Basra, S.M.A., Plant drought: effects, mechanisms, and management. Agron. Sustain. Dev. 29 (2009), 185–212.
54. [54] Fountain, J.C., Chen, Z.Y., Scully, B.T., Kemerait, R.C., Lee, R.D., Guo, B.Z., Pathogenesis-related gene expressions in different maize genotypes under drought stressed conditions. Afr. J. Plant Sci. 4 (2010), 433–440.
55. [55] Hajheidari, M., Eivazi, A., Buchanan, B.B., Wong, J.H., Majidi, I., Salekdeh, G.H., Proteomics uncovers a role for redox in drought tolerance in wheat. J. Proteome Res. 6 (2007), 1451–1460.
56. [56] Kakumanu, A., Ambavaram, M.M., Klumas, C., Krishnan, A., Batlang, U., Myers, E., Grene, R., Pereira, A., Effects of drought on gene expression in maize reproductive and leaf meristem tissue revealed by RNA-Seq. Plant Physiol. 160 (2012), 846–867.
57. [57] Reverberi, M., Punelli, M., Scala, V., Scarpari, M., Uva, P., Mentzen, W.I., Dolezal, A.L., Woloshuk, C., Pinzari, F., Fabbri, A.A., Fanelli, C., Payne, G.A., Genotypic and phenotypic versatility of Aspergillus flavus during maize exploitation. PLoS ONE, 8, 2013 (e68735).
58. [58] Guo, B.Z., Widstrom, N.W., Lee, R.D., Wilson, D.M., Coy, A.E., Prevention of preharvest aflatoxin contamination: integration of crop management and genetics in corn. Abbas, H., (eds.) Aflatoxin and Food Safety, 2005, CRC Press, Boca Raton, Florida, 437–457.
59. [59] Willcox, M.C., Davis, G.L., Warburton, M.L., Windham, G.L., Abbas, H.K., Betrán, J., Holland, J.B., Williams, W.P., Confirming quantitative trait loci for aflatoxin resistance from Mp313E in different genetic backgrounds. Mol. Breed. 32 (2013), 15–26.
60. [60] Brooks, T.D., Williams, W.P., Windham, G.L., Willcox, M.C., Abbas, H.K., Quantitative trait loci contributing resistance to aflatoxin accumulation in maize inbred Mp313E. Crop Sci. 45 (2005), 171–174.
61. [61] Yin, Z., Wang, Y., Wu, F., Gu, X., Bian, Y., Wang, Y., Deng, D., Quantitative trait locus mapping of resistance to Aspergillus flavus infection using a recombinant inbred line population in maize. Mol. Breed. 33 (2014), 39–49.
62. [62] Warburton, M.L., Williams, W.P., Aflatoxin resistance in maize: what have we learned lately?. Adv. Bot., 2014, 2014, 10.
63. [63] Almeida, G.D., Makumbi, D., Magorokosho, C., Nair, S., Borém, A., Ribaut, J.M., Bänziger, M., Prasanna, B.M., Crossa, J., Babu, R., QTL mapping in three tropical maize populations reveals a set of constitutive and adaptive genomic regions for drought tolerance. Theor. Appl. Genet. 126 (2013), 583–600.
64. [64] Visscher, P.M., Posthuma, D., Statistical power to detect genetic loci affecting environmental sensitivity. Behav. Genet. 40 (2010), 728–733.
65. [65] Guo, B.Z., Krakowsky, M.D., Ni, X., Scully, B.T., Lee, R.D., Coy, A.E., Widstrom, N.W., Registration of maize inbred line GT603. J. Plant Regist. 5 (2011), 211–214.
66. [66] Guo, B.Z., Widstrom, N.W., Lee, R.D., Coy, A.E., Lynch, R.E., Registration of maize germplasm GT601 (AM-1) and GT602 (AM-2). J. Plant Regist. 1 (2007), 153–154.
67. [67] Scully, B.T., Krakowsky, M.D., Ni, X., Tapp, P.J., Knoll, J.K., Lee, R.D., Guo, B.Z., Registration of maize inbred line ‘GT888’. J. Plant Regist., 9, 2015 (in press).
68. [68] Williams, W.P., Krakowsky, M.D., Scully, B.T., Brown, R.L., Menkir, A., Warburton, M.L., Windham, G.L., Identifying and developing maize germplasm with resistance to accumulation of aflatoxins. World Mycotoxin J. 8 (2014), 193–209.
69. [69] Williams, W.P., Windham, G.L., Buckley, P.M., Diallele analysis of aflatoxin accumulation in maize. Crop Sci. 48 (2008), 134–138.
70. [70] Brown, R.L., Menkir, A., Chen, Z.Y., Bhatnagar, D., Yu, J., Yao, H., Cleveland, T.E., Breeding aflatoxin-resistant maize lines using recent advances in technologies — a review. Food Addit. Contam. A 30 (2013), 1382–1391.
71. [71] Wagacha, J.M., Muthomi, J.W., Mycotoxin problems in Africa: current status, implications to food safety and health and possible management strategies. Int. J. Food Microbiol. 124 (2008), 1–12.
72. [72] Sanders, T.H., Blankenship, P.D., Cole, R.J., Hill, R.A., Effect of soil temperature and drought on peanut pod and stem temperatures relative to Aspergillus flavus invasion and aflatoxin contamination. Mycopathologia 86 (1984), 51–54.
73. [73] Girdthai, T., Jogloy, S., Vorasoot, N., Akkasaeng, C., Wongkaew, S., Holbrook, C.C., Patanothai, A., Associations between physiological traits for drought tolerance and aflatoxin contamination in peanut genotypes under terminal drought. Plant Breed. 129 (2010), 693–699.
74. [74] Sudhakar, P., Lathat, P., Babitha, M., Reddy, P.V., Naidu, P.H., Relationship of drought tolerance traits with aflatoxin contamination in groundnut. Indian J. Plant Physiol. 12 (2007), 261–265.
75. [75] Dorner, J., Cole, R., Sanders, T., Blankenship, P., Interrelationship of kernel water activity, soil temperature, maturity, and phytoalexin production in pre-harvest aflatoxin contamination of drought-stressed peanuts. Mycopathologia 105 (1989), 117–128.
76. [76] Pitt, J.I., Taniwaki, M.H., Cole, M.B., Mycotoxin production in major crops as influenced by growing, harvesting, storage and processing, with emphasis on the achievement of Food Safety Objectives. Food Control 32 (2013), 205–215.
77. [77] Golombek, S.D., Johasen, C., Effect of soil temperature on vegetative and reproductive growth and development in three Spanish genotypes of groundnut (Arachis hypogaea L.). Peanut Sci. 24 (1997), 67–72.
78. [78] Arunyanark, A., Jogloy, S., Wongkaew, S., Akkasaeng, C., Vorasoot, N., Wright, G.C., Rachaputi, R.C.N., Patanothai, A., Association between aflatoxin contamination and drought tolerance traits in peanut. Field Crop Res. 114 (2009), 14–22.
79. [79] Girdthai, T., Jogloy, S., Vorasoot, N., Akkasaeng, C., Wongkaew, S., Holbrook, C.C., Patanothai, A., Heritability of, and genotypic correlations between, aflatoxin traits and physiological traits for drought tolerance under end of season drought in peanut (Arachis hypogaea L.). Field Crops Res. 118 (2010), 169–176.
80. [80] Guo, B.Z., Yu, J., Holbrook, C.C., Cleveland, T.E., Nierman, W.C., Scully, B.T., Strategies in prevention of preharvest aflatoxin contamination in peanuts: aflatoxin biosynthesis, genetics and genomics. Peanut Sci. 36 (2009), 11–20.
81. [81] Guo, B.Z., Chen, C.Y., Chu, Y., Holbrook, C.C., Ozias-Akins, P., Stalker, H.T., Advances in genetics and genomics for sustainable peanut production. Benkeblia, N., (eds.) Sustainable Agriculture and New Biotechnologies, 2012, CRC Press, Boca Raton, Florida, 341–367.
82. [82] Wang, T., Zhang, E.H., Chen, X.P., Li, L., Liang, X.Q., Identification of seed proteins associated with resistance to pre-harvested aflatoxin contamination in peanut (Arachis hypogaea L.). BMC Plant Biol. 10 (2010), 267–278.
83. [83] Wang, Z., Yan, S., Liu, C., Chen, F., Wang, T., Proteomic analysis reveals an aflatoxin-triggered immune response in cotyledons of Arachis hypogaea infected with Aspergillus flavus. J. Proteome 11 (2012), 2739–2753.
84. [84] Holbrook, C.C., Kvien, C.K., Rucker, K.S., Wilson, D.W., Hook, J.E., Preharvest aflatoxin contamination in drought tolerant and intolerant peanut genotypes. Peanut Sci. 27 (2000), 45–48.
85. [85] Hamidou, F., Rathore, A., Waliyar, F., Vadez, V., Although drought intensity increases aflatoxin contamination, drought tolerance does not lead to less aflatoxin contamination. Field Crops Res. 156 (2014), 103–110.
86. [86] Holbrook, C.C., Guo, B.Z., Wilson, D.M., Timper, P., The U.S. breeding program to develop peanut with drought tolerance and reduced aflatoxin contamination. Peanut Sci. 36 (2009), 50–53.
87. [87] Nigam, S.N., Waliyar, F., Aruna, R., Reddy, S.V., Kumar, P.L., Craufurd, P.Q., Diallo, A.T., Ntare, B.R., Upadhyaya, H.D., Breeding peanut for resistance to aflatoxin contamination at ICRISAT. Peanut Sci. 36 (2009), 42–49.
88. [88] Milla, S.R., Isleib, T.G., Tallury, S.P., Identification of AFLP markers linked to reduced aflatoxin accumulation in A. cardenasii-derived germplasm lines of peanut. Proc. Am. Peanut Res. Educ. Soc., 37, 2005, 90.
89. [89] Liang, X., Zhou, G., Hong, Y., Chen, X., Liu, H., Li, S., Overview of research progress on peanut (Arachis hypogaea L.) host resistance to aflatoxin contamination and genomics at the Guangdong Academy of Agricultural Sciences. Peanut Sci. 36 (2009), 29–34.