Host-induced gene silencing compromises Verticillium wilt in tomato and Arabidopsis

Molecular Plant Pathology

Volumn 19, Issue 1, 2018, Pages 77-89

  Song, Yin ^a   Thomma, Bart P H J ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

HIGS; RNAi; Verticillium; Virulence gene

Indexed keywords

BACTERIAL DNA; PLANT PROTEIN; T-DNA;

ARABIDOPSIS; GENE SILENCING; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PLANT DISEASE; PLANT IMMUNITY; PLANT VIRUS; TOMATO; TRANSGENIC PLANT; VERTICILLIUM;

ARABIDOPSIS; DNA, BACTERIAL; GENE SILENCING; HOST-PATHOGEN INTERACTIONS; LYCOPERSICON ESCULENTUM; PLANT DISEASES; PLANT IMMUNITY; PLANT PROTEINS; PLANT VIRUSES; PLANTS, GENETICALLY MODIFIED; VERTICILLIUM;

EID: 85006356909     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/mpp.12500     Document Type: Article

References (70)

1. Andrade, C., Tinoco, M., Rieth, A., Maia, F. and Aragão, F. (2015) Host-induced gene silencing in the necrotrophic fungal pathogen Sclerotinia sclerotiorum. Plant Pathol. 65, 626–632.
2. Antanaviciute, L., Šurbanovski, N., Harrison, N., McLeary, K., Simpson, D., Wilson, F., Sargent, D. and Harrison, R. (2015) Mapping QTL associated with Verticillium dahliae resistance in the cultivated strawberry (Fragaria3ananassa). Hortic. Res. 2, 15 009.
3. Barrow, J.R. (1970) Heterozygosity in inheritance of Verticillium wilt tolerance in cotton. Phytopathology, 60, 301–303.
4. Baulcombe, D. (2005) RNA silencing. Trends Biochem. Sci. 30, 290–293.
5. Baum, J.A., Bogaert, T., Clinton, W., Heck, G.R., Feldmann, P., Ilagan, O., Johnson, S., Plaetinck, G., Munyikwa, T. and Pleau, M. (2007) Control of coleopteran insect pests through RNA interference. Nat. Biotechnol. 25, 1322–1326.
6. Bolek, Y., El-Zik, K.M., Pepper, A.E., Bell, A.A., Magill, C.W., Thaxton, P.M. and Reddy, O.U.K. (2005) Mapping of Verticillium wilt resistance genes in cotton. Plant Sci. 168, 1581–1590.
7. Chaloner, T., van Kan, J.A. and Grant-Downton, R.T. (2016) RNA ‘Information Warfare’ in pathogenic and mutualistic interactions. Trends Plant Sci. 21, 738–748.
8. Chen, W., Kastner, C., Nowara, D., Oliveira-Garcia, E., Rutten, T., Zhao, Y., Deising, H.B., Kumlehn, J. and Schweizer, P. (2016) Host-induced silencing of Fusarium culmorum genes protects wheat from infection. J. Exp. Bot. 67, 4979–4991.
9. Cheng, W., Song, X.S., Li, H.P., Cao, L.H., Sun, K., Qiu, X.L., Xu, Y.B., Yang, P., Huang, T. and Zhang, J.B. (2015) Host-induced gene silencing of an essential chitin synthase gene confers durable resistance to Fusarium head blight and seedling blight in wheat. Plant Biotechnol. J. 13, 1335–1345.
10. Christopoulou, M., Wo, S.R.C., Kozik, A., McHale, L.K., Truco, M.J., Wroblewski, T. and Michelmore, R. (2015) Genome-wide architecture of disease resistance genes in lettuce. G3 (Bethesda), 5, 2655–2669.
11. Clough, S.J. and Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium- mediated transformation of Arabidopsis thaliana. Plant J. 16, 735–743.
12. de Jonge, R., van Esse, H.P., Maruthachalam, K., Bolton, M.D., Santhanam, P., Saber, M.K., Zhang, Z., Usami, T., Lievens, B., Subbarao, K.V. and Thomma, B.P.H.J. (2012) Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proc. Natl. Acad. Sci. USA, 109, 5110–5115.
13. Dobinson, K., Tenuta, G. and Lazarovits, G. (1996) Occurrence of race 2 of Verticillium dahliae in processing tomato fields in southwestern Ontario. Can. J. Plant Pathol. 18, 55–58.
14. Duan, C.G., Wang, C.H. and Guo, H.S. (2012) Application of RNA silencing to plant disease resistance. Silence, 3, 5.
15. Ellendorff, U., Fradin, E.F., De Jonge, R. and Thomma, B.P.H.J. (2009) RNA silencing is required for Arabidopsis defence against Verticillium wilt disease. J. Exp. Bot. 60, 591–602.
16. Escobar, M.A., Civerolo, E.L., Summerfelt, K.R. and Dandekar, A.M. (2001) RNAi-mediated oncogene silencing confers resistance to crown gall tumorigenesis. Proc. Natl. Acad. Sci. USA, 98, 13 437–13 442.
17. Escobar, M.A., Leslie, C.A., McGranahan, G.H. and Dandekar, A.M. (2002) Silencing crown gall disease in walnut (Juglans regia L.). Plant Sci. 163, 591–597.
18. Faino, L., Seidl, M.F., Datema, E., van den Berg, G.C., Janssen, A., Wittenberg, A.H. and Thomma, B.P.H.J. (2015) Single-molecule real-time sequencing combined with optical mapping yields completely finished fungal genome. MBio, 6, e00936–e00915.
19. Fradin, E.F. and Thomma, B.P.H.J. (2006) Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. albo-atrum. Mol. Plant Pathol. 7, 71–86.
20. Fradin, E.F., Zhang, Z., Ayala, J.C.J., Castroverde, C.D., Nazar, R.N., Robb, J., Liu, C.-M. and Thomma, B.P.H.J. (2009) Genetic dissection of Verticillium wilt resistance mediated by tomato Ve1. Plant Physiol. 150, 320–332.
21. Fradin, E.F., Abd-El-Haliem, A., Masini, L., van den Berg, G.C., Joosten, M.H. and Thomma, B.P.H.J. (2011) Interfamily transfer of tomato Ve1 mediates Verticillium resistance in Arabidopsis. Plant Physiol. 156, 2255–2265.
22. Fradin, E.F., Zhang, Z., Rovenich, H., Song, Y., Liebrand, T.W., Masini, L., van den Berg, G.C., Joosten, M.H. and Thomma, B.P.H.J. (2014) Functional analysis of the tomato immune receptor Ve1 through domain swaps with its non-functional homolog Ve2. PLoS One, 9, e88208.
23. Ghag, S.B., Shekhawat, U.K. and Ganapathi, T.R. (2014) Host-induced posttranscriptional hairpin RNA-mediated gene silencing of vital fungal genes confers efficient resistance against Fusarium wilt in banana. Plant Biotechnol. J. 12, 541–553.
24. Govindarajulu, M., Epstein, L., Wroblewski, T. and Michelmore, R.W. (2015) Host-induced gene silencing inhibits the biotrophic pathogen causing downy mildew of lettuce. Plant Biotechnol. J. 13, 875–883.
25. Hayes, R.J., McHale, L.K., Vallad, G.E., Truco, M.J., Michelmore, R.W., Klosterman, S.J., Maruthachalam, K. and Subbarao, K.V. (2011) The inheritance of resistance to Verticillium wilt caused by race 1 isolates of Verticillium dahliae in the lettuce cultivar La Brillante. Theor. Appl. Genet. 123, 509–517.
26. Helliwell, C. and Waterhouse, P. (2003) Constructs and methods for highthroughput gene silencing in plants. Methods, 30, 289–295.
27. Hu, Z., Parekh, U., Maruta, N., Trusov, Y. and Botella, J.R. (2015) Down-regulation of Fusarium oxysporum endogenous genes by host-delivered RNA interference enhances disease resistance. Front. Chem. 3, 1. doi:10.3389/fchem.2015.00001.
28. Huang, G., Allen, R., Davis, E.L., Baum, T.J. and Hussey, R.S. (2006) Engineering broad root-knot resistance in transgenic plants by RNAi silencing of a conserved and essential root-knot nematode parasitism gene. Proc. Natl. Acad. Sci. USA, 103, 14 302–14 306.
29. Inderbitzin, P., Bostock, R.M., Davis, R.M., Usami, T., Platt, H.W. and Subbarao, K.V. (2011a) Phylogenetics and taxonomy of the fungal vascular wilt pathogen Verticillium, with the descriptions of five new species. PLoS One, 6, e28341.
30. Jahan, S.N., Åsman, A.K., Corcoran, P., Fogelqvist, J., Vetukuri, R.R. and Dixelius, C. (2015) Plant-mediated gene silencing restricts growth of the potato late blight pathogen Phytophthora infestans. J. Exp. Bot. 66, 2785–2794.
31. Jakse, J., Cerenak, A., Radisek, S., Satovic, Z., Luthar, Z. and Javornik, B. (2013) Identification of quantitative trait loci for resistance to Verticillium wilt and yield parameters in hop (Humulus lupulus L.). Theor. Appl. Genet. 126, 1431–1443.
32. Kawchuk, L.M., Hachey, J., Lynch, D.R., Kulcsar, F., van Rooijen, G., Waterer, D.R., Robertson, A., Kokko, E., Byers, R. and Howard, R.J. (2001) Tomato Ve disease resistance genes encode cell surface-like receptors. Proc. Natl. Acad. Sci. USA, 98, 6511–6515.
33. Klimes, A., Dobinson, K.F., Thomma, B.P.H.J. and Klosterman, S.J. (2015) Genomics spurs rapid advances in our understanding of the biology of vascular wilt pathogens in the genus Verticillium. Annu. Rev. Phytopathol. 53, 181–198.
34. Klosterman, S.J., Atallah, Z.K., Vallad, G.E. and Subbarao, K.V. (2009) Diversity, pathogenicity, and management of Verticillium species. Annu. Rev. Phytopathol. 47, 39–62.
35. Knip, M., Constantin, M.E. and Thordal-Christensen, H. (2014) Trans-kingdom cross-talk: small RNAs on the move. PLoS Genet. 10, e1004602.
36. Koch, A., Kumar, N., Weber, L., Keller, H., Imani, J. and Kogel, K.H. (2013) Hostinduced gene silencing of cytochrome P450 lanosterol C14a-demethylaseencoding genes confers strong resistance to Fusarium species. Proc. Natl. Acad. Sci. USA, 110, 19 324–19 329.
37. Liu, Y., Schiff, M. and Dinesh-Kumar, S. (2002) Virus-induced gene silencing in tomato. Plant J. 31, 777–786.
38. Lynch, D., Kawchuk, L., Hachey, J., Bains, P. and Howard, R. (1997) Identification of a gene conferring high levels of resistance to Verticillium wilt in Solanum chacoense. Plant Dis. 81, 1011–1014.
39. Mao, Y.B., Cai, W.J., Wang, J.W., Hong, G.J., Tao, X.Y., Wang, L.J., Huang, Y.P. and Chen, X.Y. (2007) Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nat. Biotechnol. 25, 1307–1313.
40. Mascia, T., Nigro, F., Abdallah, A., Ferrara, M., De Stradis, A., Faedda, R., Palukaitis, P. and Gallitelli, D. (2014) Gene silencing and gene expression in phytopathogenic fungi using a plant virus vector. Proc. Natl. Acad. Sci. USA, 111, 4291–4296.
41. Mert, M., Kurt, S., Gencer, O., Akiscan, Y., Boyaci, K. and Tok, F. (2005) Inheritance of resistance to Verticillium wilt (Verticillium dahliae) in cotton (Gossypium hirsutum L.). Plant Breed. 124, 102–104.
42. 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.
43. Panwar, V., McCallum, B. and Bakkeren, G. (2013) Host-induced gene silencing of wheat leaf rust fungus Puccinia triticina pathogenicity genes mediated by the Barley stripe mosaic virus. Plant Mol. Biol. 81, 595–608.
44. Pegg, G.F. (1974) Verticillium diseases. Rev. Plant Pathol. 53, 157–182.
45. Pegg, G.F. and Brady, B.L. (2002) Verticillium Wilts. Wallingford, Oxfordshire: CABI Publishing.
46. Putt, E.D. (1964) Breeding behaviour of resistance to leaf mottle or Verticillium in sunflowers. Crop Sci. 4, 177–179.
47. Ruiz-Ferrer, V. and Voinnet, O. (2009) Roles of plant small RNAs in biotic stress responses. Annu. Rev. Plant Biol. 60, 485–510.
48. Sanju, S., Siddappa, S., Thakur, A., Shukla, P.K., Srivastava, N., Pattanayak, D., Sharma, S. and Singh, B. (2015) Host-mediated gene silencing of a single effector gene from the potato pathogen Phytophthora infestans imparts partial resistance to late blight disease. Funct. Integr. Genomics, 15, 697–706.
49. Santhanam, P. and Thomma, B.P.H.J. (2013) Verticillium dahliae Sge1 differentially regulates expression of candidate effector genes. Mol. Plant–Microbe Interact. 26, 249–256.
50. Santhanam, P., van Esse, H.P., Albert, I., Faino, L., Nürnberger, T. and Thomma, B.P.H.J. (2013) Evidence for functional diversification within a fungal NEP1-like protein family. Mol. Plant–Microbe Interact. 26, 278–286.
51. Schaible, L., Cannon, O.S. and Waddoups, V. (1951) Inheritance of resistance to Verticillium wilt in a tomato cross. Phytopathology, 41, 986–990.
52. Senthil-Kumar, M., Hema, R., Anand, A., Kang, L., Udayakumar, M. and Mysore, K.S. (2007) A systematic study to determine the extent of gene silencing in Nicotiana benthamiana and other Solanaceae species when heterologous gene sequences are used for virus-induced gene silencing. New Phytol. 176, 782–791.
53. Shimada, T.L., Shimada, T. and Hara-Nishimura, I. (2010) A rapid and nondestructive screenable marker, FAST, for identifying transformed seeds of Arabidopsis thaliana. Plant J. 61, 519–528.
54. Simko, I., Costanzo, S., Haynes, K., Christ, B. and Jones, R. (2004) Linkage disequilibrium mapping of a Verticillium dahliae resistance quantitative trait locus in tetraploid potato (Solanum tuberosum) through a candidate gene approach. Theor. Appl. Genet. 108, 217–224.
55. Song, Y., Zhang, Z., Seidl, M.F., Majer, A., Jakse, J., Javornik, B. and Thomma, B.P.H.J. (2016) Broad taxonomic characterization of Verticillium wilt resistance genes reveals ancient origin of the tomato Ve1 immune receptor. Mol. Plant Pathol. doi: 10.1111/mpp.12390.
56. Thomma, B.P.H.J., Nürnberger, T. and Joosten, M.H. (2011) Of PAMPs and effectors: the blurred PTI–ETI dichotomy. Plant Cell, 23, 4–15.
57. Tinoco, M.L., Dias, B.B., Dall’astta, R.C., Pamphile, J.A. and Aragão, F.J. (2010) In vivo trans-specific gene silencing in fungal cells by in planta expression of a double-stranded RNA. BMC Biol. 8, 27. DOI: 10.1186/1741-7007-8-27.
58. Tomilov, A.A., Tomilova, N.B., Wroblewski, T., Michelmore, R. and Yoder, J.I. (2008) Trans-specific gene silencing between host and parasitic plants. Plant J. 56, 389–397.
59. Wang, G., Fiers, M., Ellendorff, U., Wang, Z., de Wit, P.J., Angenent, G.C. and Thomma, B.P.H.J. (2010) The diverse roles of extracellular leucine-rich repeatcontaining receptor-like proteins in plants. Crit. Rev. Plant Sci. 29, 285–299.
60. Wang, H.M., Lin, Z.X., Zhang, X.L., Chen, W., Guo, X.P., Nie, Y.C. and Li, Y.H. (2008) Mapping and quantitative trait loci analysis of Verticillium wilt resistance genes in cotton. J. Integr. Plant Biol. 50, 174–182.
61. Wang, M., Weiberg, A., Lin, F.M., Thomma, B.P.H.J., Huang, H.D. and Jin, H.L. (2016) Bidirectional cross-kingdom RNAi and fungal uptake of external RNAs confer plant protection. Nat. Plants, 2, 16151.
62. Weiberg, A., Wang, M., Lin, F.M., Zhao, H., Zhang, Z., Kaloshian, I., Huang, H.D. and Jin, H.L. (2013) Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science, 342, 118–123.
63. Weiberg, A., Bellinger, M. and Jin, H.L. (2015) Conversations between kingdoms: small RNAs. Curr. Opin. Biotechnol. 32, 207–215.
64. Yang, C., Guo, W., Li, G., Gao, F., Lin, S. and Zhang, T. (2008) QTLs mapping for Verticillium wilt resistance at seedling and maturity stages in Gossypium barbadense L. Plant Sci. 174, 290–298.
65. Yin, C.T., Jurgenson, J.E. and Hulbert, S.H. (2011) Development of a host-induced RNAi system in the wheat stripe rust fungus Puccinia striiformis f. sp. tritici. Mol. Plant–Microbe Interact. 24, 554–561.
66. Yin, C.T., Downey, S.I., Klages-Mundt, N.L., Ramachandran, S., Chen, X., Szabo, L.J., Pumphrey, M. and Hulbert, S.H. (2015) Identification of promising host-induced silencing targets among genes preferentially transcribed in haustoria of Puccinia. BMC Genomics, 16, 579. DOI: 10.1186/s12864-015-1791-y.
67. Zhang, H., Guo, J., Voegele, R.T., Zhang, J., Duan, Y., Luo, H. and Kang, Z. (2012) Functional characterization of calcineurin homologs PsCNA1/PsCNB1 in Puccinia striiformis f. sp. tritici using a host-induced RNAi system. PLoS One, 7, e49262.
68. Zhang, T., Jin, Y., Zhao, J.H., Gao, F., Zhou, B.J., Fang, Y.Y. and Guo, H.S. (2016) Host-induced gene silencing of the target gene in fungal cells confers effective resistance to the cotton wilt disease pathogen Verticillium dahliae. Mol. Plant, 9, 939–942.
69. Zhang, Z., Song, Y., Liu, C.M. and Thomma, B.P.H.J. (2014) Mutational analysis of the Ve1 immune receptor that mediates Verticillium resistance in tomato. PLoS One, 9, e99511.
70. Zhou, B., Bailey, A., Niblett, C. and Qu, R. (2016) Control of brown patch (Rhizoctonia solani) in tall fescue (Festuca arundinacea Schreb.) by host induced gene silencing. Plant Cell Rep. 35, 791–802.