Host-induced gene silencing of an essential chitin synthase gene confers durable resistance to Fusarium head blight and seedling blight in wheat

Plant Biotechnology Journal

Volumn 13, Issue 9, 2015, Pages 1335-1345

  Cheng, Wei ^a   Song, Xiu Shi ^a   Li, He Ping ^a   Cao, Le Hui ^a   Sun, Ke ^a   Qiu, Xiao Li ^a   Xu, Yu Bin ^a   Yang, Peng ^a   Huang, Tao ^a   Zhang, Jing Bo ^a   Qu, Bo ^a   Liao, Yu Cai ^a  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

Author keywords

Chitin synthase; Fusarium graminearum; RNAi; Triticum aestivum

Indexed keywords

CHITIN SYNTHASE;

FUSARIUM; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PLANT DISEASE; PLANT IMMUNITY; SEEDLING; WHEAT;

CHITIN SYNTHASE; FUSARIUM; GENE EXPRESSION REGULATION, PLANT; GENE SILENCING; PLANT DISEASES; PLANT IMMUNITY; SEEDLINGS; TRITICUM;

EID: 84955200534     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12352     Document Type: Article

References (45)

1. Anand, A., Zhou, T., Trick, H.N., Gill, B.S., Bockus, W.W. and Muthukrishnan, S. (2003) Greenhouse and field testing of transgenic wheat plants stably expressing genes for thaumatin-like protein, chitinase and glucanase against Fusarium graminearum. J. Exp. Bot. 54, 1101-1111.
2. Bai, G. and Shaner, G. (2004) Management and resistance in wheat and barley to Fusarium head blight. Annu. Rev. Phytopathol. 42, 135-161.
3. Baulcombe, D. (2004) RNA silencing in plants. Nature, 431, 356-363.
4. Baum, J.A., Bogaert, T., Clinton, W., Heck, G.R., Feldmann, P., Ilagan, O., Johnson, S., Plaetinck, G., Munyikwa, T., Pleau, M., Vaughn, T. and Roberts, J. (2007) Control of coleopteran insect pests through RNA interference. Nat. Biotechnol. 25, 1322-1326.
5. Chen, L.F., Bai, G.H. and Desjardins, A.E. (2000) Recent advances in wheat head scab research in China. In Proceedings of the International Symposium on Wheat Improvement for Scab Resistance (Raupp, W.J., Ma, Z.Q., Chen, P.D. and Liu, D.J., eds), pp. 258-273. Manhattan: The Kansas State University Printing Services.
6. Chen, C., Wang, J., Luo, Q., Yuan, S. and Zhou, M. (2007) Characterization and fitness of carbendazim-resistant strains of Fusarium graminearum (wheat scab). Pest Manag. Sci. 63, 1201-1207.
7. Christensen, A.H., Sharrock, R.A. and Quail, P.H. (1992) Maize polyubiquitin genes: structure, thermal perturbation of expression and transcript splicing, and promoter activity following transfer to protoplasts by electroporation. Plant Mol. Biol. 18, 675-689.
8. Duvick, J.P., Rood, T., Rao, G. and Marshak, D.R. (1992) Purification and characterization of a novel antimicrobial peptide from maize (Zea mays L.) kernels. J. Biol. Chem. 267, 18814-18820.
9. Eichmann, R., Bischof, M., Weis, C., Shaw, J., Lacomme, C., Schweizer, P., Duchkov, D., Hensel, G., Kumlehn, J. and Hückelhoven, R. (2010) BAX INHIBITOR-1 is required for full susceptibility of barley to powdery mildew. Mol. Plant Microbe Interact. 23, 1217-1227.
10. Fire, A.Z. (2007) Gene silencing by double-stranded RNA. Cell Death Differ. 14, 1998-2012.
11. Gao, C.S., Kou, X.J., Li, H.P., Zhang, J.B., Saad, A.S.I. and Liao, Y.C. (2013) Inverse effects of Arabidopsis NPR1 gene on Fusarium seedling blight and Fusarium head blight in transgenic wheat. Plant. Pathol. 62, 383-392.
12. Ghag, S.B., Shekhawat, U.K.S. and Ganapathi, T.R. (2014) Host-induced post-transcriptional hairpin RNA-mediated gene silencing of vital fungal genes confers efficient resistance against Fusarium wilt in banana. Plant Biotechnol. J. 12, 541-553.
13. Jansen, C., von Wettstein, D., Schafer, W., Kogel, K.H., Felk, A. and Maier, F.J. (2005) Infection patterns in barley and wheat spikes inoculated with wild-type and trichodiene synthase gene disrupted Fusarium graminearum. Proc. Natl Acad. Sci. USA, 102, 16892-16897.
14. Kazan, K., Gardiner, D.M. and Manners, J.M. (2012) On the trail of a cereal killer: recent advances in Fusarium graminearum pathogenomics and host resistance. Mol. Plant Pathol. 13, 399-413.
15. Kim, J.E., Lee, H.J., Lee, J., Kim, K.W., Yun, S.H., Shim, W.B. and Lee, Y.W. (2009) Gibberella zeae chitin synthase genes, GzCHS5 and GzCHS7, are required for hyphal growth, perithecia formation, and pathogenicity. Curr. Genet. 55, 449-459.
16. Koch, A., Kumar, N., Weber, L., Keller, H., Imani, J. and Kogel, K.H. (2013) Host-induced gene silencing of cytochrome P450 lanosterol C14α-demethylase-encoding genes confers strong resistance to Fusarium species. Proc. Natl Acad. Sci. USA, 110, 19324-19329.
17. Kong, L.A., Yang, J., Li, G.T., Qi, L.L., Zhang, Y.J., Wang, C.F., Zhao, W.S., Xu, J.R. and Peng, Y.L. (2012) Different chitin synthase genes are required for various developmental and plant infection processes in the rice blast fungus Magnaporthe oryzae. PLoS Pathog. 8, e1002526.
18. Latgé, J.P. (2007) The cell wall: a carbohydrate armour for the fungal cell. Mol. Microbiol. 66, 279-290.
19. Lee, W.S., Hammond-Kosack, K.E. and Kanyuka, K. (2012) Barley stripe mosaic virus-mediated tools for investigating gene function in cereal plants and their pathogens: virus-induced gene silencing, host-mediated gene silencing, and virus-mediated overexpression of heterologous protein. Plant Physiol. 160, 582-590.
20. Lenardon, M.D., Munro, C.A. and Gow, N.A. (2010) Chitin synthesis and fungal pathogenesis. Curr. Opin. Microbiol. 13, 416-423.
21. Li, H.P., Zhang, J.B., Shi, R.P., Huang, T., Fischer, R. and Liao, Y.C. (2008) Engineering Fusarium head blight resistance in wheat by expression of a fusion protein containing a Fusarium-specific antibody and an antifungal peptide. Mol. Plant Microbe Interact. 21, 1242-1248.
22. Li, H.B., Xie, G.Q., Ma, J., Liu, G.R., Wen, S.M., Ban, T., Chakraborty, S. and Liu, C.J. (2010a) Genetic relationships between resistances to Fusarium head blight and crown rot in bread wheat (Triticum aestivum L.). Theor. Appl. Genet. 121, 941-950.
23. Li, X., Zhang, J.B., Song, B., Li, H.P., Xu, H.Q., Qu, B., Dang, F.J. and Liao, Y.C. (2010b) Resistance to Fusarium head blight and seedling blight in wheat is associated with activation of a cytochrome p450 gene. Phytopathology, 100, 183-191.
24. Liu, D.J. (2001) Breeding wheat for scab resistance-a worldwide hard nut to crack. In Proceedings of International Conference on Wheat Genetics and Breeding-Perspectives of the 21st Century for Wheat Genetics and Breeding (Zhang, X.A., Gou, H.Q., Liu, R.Z. Yang, L., eds), pp. 4-7. Beijing: Agriculture Publisher.
25. Lu, W.Z., Chen, S.H. and Wang, Y.Z. (2001) Research on Wheat Scab. pp. 3-34. Beijing: Science Publisher.
26. Maier, F.J., Maiz, S., Losch, A.P., Lacour, T. and Schafer, W. (2005) Development of a highly efficient gene targeting system for Fusarium graminearum using the disruption of a polyketide synthase gene as a visible marker. FEMS Yeast Res. 5, 653-662.
27. Melnyk, C.W., Molnar, A. and Baulcombe, D.C. (2011) Intercellular and systemic movement of RNA silencing signals. EMBO J. 30, 3553-3563.
28. Nicholson, P., Rezanoor, H.N., Simpson, D.R. and Joyce, D. (1997) Differentiation and quantification of the cereal eyespot fungi Tapesia yallundae and Tapesia acuformis using a PCR assay. Plant. Pathol. 46, 842-856.
29. Nowara, D., Gay, A., Lacomme, C., Shaw, J., Ridout, C., Douchkov, D., Hensel, G., Kumlehn, J. and Schweizer, P. (2010) HIGS: host-induced gene silencing in the obligate biotrophic fungal pathogen Blumeria graminis. Plant Cell, 22, 3130-3141.
30. Pestka, J.J. and Smolinski, A.T. (2005) Deoxynivalenol: toxicology and potential effects on humans. J. Toxicol. Environ. Health B Crit. Rev. 8, 39-69.
31. Pooggin, M. and Hohn, T. (2003) RNAi targeting of DNA virus in plants. Nat. Biotechnol. 21, 131-132.
32. Qu, B., Li, H.P., Zhang, J.B., Xu, Y.B., Huang, T., Wu, A.B., Zhao, C.S., Carter, J., Nicholson, P. and Liao, Y.C. (2008) Geographic distribution and genetic diversity of Fusarium graminearum and F. asiaticum on wheat spikes throughout China. Plant. Pathol. 57, 15-24.
33. Ridout, C.J., Skamnioti, P., Porritt, O., Sacristan, S., Jones, J.D. and Brown, J.K. (2006) Multiple avirulence paralogues in cereal powdery mildew fungi may contribute to parasite fitness and defeat of plant resistance. Plant Cell, 18, 2402-2414.
34. Rittenour, W.R. and Harris, S.D. (2008) Characterization of Fusarium graminearum Mes1 reveals roles in cell-surface organization and virulence. Fungal Genet. Biol. 45, 933-946.
35. Schussler, M.D., Alexandersson, E., Bienert, G.P., Kichey, T., Laursen, K.H., Johanson, U., Kjellbom, P., Schjoerring, J.K. and Jahn, T.P. (2008) The effects of the loss of TIP1;1 and TIP1;2 aquaporins in Arabidopsis thaliana. Plant J. 56, 756-767.
36. Simpson, D., Weston, G., Turner, J., Jennings, P. and Nicholson, P. (2001) Differential control of head blight pathogens of wheat by fungicides and consequences for mycotoxin contamination of grain. Eur. J. Plant Pathol. 107, 421-431.
37. Song, X.S., Li, H.P., Zhang, J.B., Song, B., Huang, T., Du, X.M., Gong, A.D., Liu, Y.K., Feng, Y.N., Agboola, R.S. and Liao, Y.C. (2014) Trehalose 6-phosphate phosphatase is required for development, virulence and mycotoxin biosynthesis apart from trehalose biosynthesis in Fusarium graminearum. Fungal Genet. Biol. 63, 24-41.
38. de Souza, N. (2014) Off-targets in RNAi screens. Nat. Methods, 11, 480.
39. Tinoco, M.L.P., Dias, B.B.A., Dall'Astta, R.C., Pamphile, J.A. and Aragao, F.J.L. (2010) In vivo trans-specific gene silencing in fungal cells by in planta expression of a double-stranded RNA. BMC Biol. 8, 27.
40. Waterhouse, P.M. and Fusaro, A.F. (2006) Viruses face a double defense by plant small RNAs. Science, 313, 54-55.
41. Wesley, S.V., Helliwell, C.A., Smith, N.A., Wang, M.B., Rouse, D.T., Liu, Q., Gooding, P.S., Singh, S.P., Abbott, D., Stoutjesdijk, P.A., Robinson, S.P., Gleave, A.P., Green, A.G. and Waterhouse, P.M. (2001) Construct design for efficient, effective and high-throughput gene silencing in plants. Plant J. 27, 581-590.
42. Wu, A.B., Li, H.P., Zhao, C.S. and Liao, Y.C. (2005) Comparative pathogenicity of Fusarium graminearum isolates from China revealed by wheat coleoptile and floret inoculations. Mycopathologia, 160, 75-83.
43. Xu, X.M. and Nicholson, P. (2009) Community ecology of fungal pathogens causing wheat head blight. Annu. Rev. Phytopathol. 47, 83-103.
44. Xu, Y.B., Li, H.P., Zhang, J.B., Song, B., Chen, F.F., Duan, X.J., Xu, H.Q. and Liao, Y.C. (2010) Disruption of the chitin synthase gene CHS1 from Fusarium asiaticum results in an altered structure of cell walls and reduced virulence. Fungal Genet. Biol. 47, 205-215.
45. Zhang, J.B., Wang, J.H., Gong, A.D., Chen, F.F., Song, B., Li, X., Li, H.P., Peng, C.H. and Liao, Y.C. (2013) Natural occurrence of Fusarium head blight, mycotoxins and mycotoxin-producing isolates of Fusarium in commercial fields of wheat in Hubei. Plant. Pathol. 62, 92-102.