TaTLP1 interacts with TaPR1 to contribute to wheat defense responses to leaf rust fungus

English version

Autoři: Fei Wang ^aff001; Shitao Yuan ^aff001; Wenyue Wu ^aff001; Yiqing Yang ^aff001; Zhongchi Cui ^aff001; Haiyan Wang ^aff001; Daqun Liu ^aff001
Působiště autorů: Center of Plant Disease and Plant Pests of Hebei Province, College of Plant Protection, Hebei Agricultural University, Baoding, China ^aff001; Graduate School of Chinese Academy of Agricultural Sciences, Beijing, China ^aff002
Vyšlo v časopise: TaTLP1 interacts with TaPR1 to contribute to wheat defense responses to leaf rust fungus. PLoS Genet 16(7): e32767. doi:10.1371/journal.pgen.1008713
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008713

Souhrn

Thaumatin-like proteins (TLPs), which are defined as pathogenesis-related protein family 5 (PR5) members, are common plant proteins involved in defense responses and confer antifungal activity against many plant pathogens. Our earlier studies have reported that the TaTLP1 gene was isolated from wheat and proved to be involved in wheat defense in response to leaf rust attack. The present study aims to identify the interacting proteins of TaTLP1 and characterize the role of the interaction between wheat and Puccinia triticina (Pt). Pull-down experiments designed to isolate the molecular target of TaTLP1 in tobacco resulted in the identification of TaPR1, a pathogenesis-related protein of family 1, and the interaction between TaTLP1 and TaPR1 was confirmed by yeast two-hybrid experiments (Y2H), bimolecular fluorescence complementation (BiFC), and co-immunoprecipitation (Co-IP). In vitro, TaTLP1 and TaPR1 together increased antifungal activity against Pt. In vivo, the disease resistance phenotype, histological observations of fungal growth and host responses, and accumulation of H₂O₂ in TaTLP1-TaPR1 in co-silenced plants indicated that co-silencing significantly enhanced wheat susceptibility compared to single knockdown TaTLP1 or TaPR1 plants. The accumulation of reactive oxygen species (ROS) was significantly reduced in co-silenced plants compared to controls during Pt infection, which suggested that the TaTLP1-TaPR1 interaction positively modulates wheat resistance to Pt in an ROS-dependent manner. Our findings provide new insights for understanding the roles of two different PRs, TaTLP1 and TaPR1, in wheat resistance to leaf rust.

Klíčová slova:

Antifungals – Antimicrobial resistance – Cysteine – Leaves – Plant defenses – Plant pathogens – Protein interactions – Wheat

Zdroje

1. Hamamouch N, Li C, Seo PJ, Park CM, Davis EL. Expression of Arabidopsis pathogenesis-related genes during nematode infection. Molecular Plant Pathology. 2011; 12:355–364. doi: 10.1111/j.1364-3703.2010.00675.x 21453430.

2. Van Loon LC, Rep M, Pieterse CM. Significance of inducible defense-related proteins in infected plants. Annual Review of Phytopathology. 2006; 44:135–162. doi: 10.1146/annurev.phyto.44.070505.143425 16602946.

3. Ferreira RB, Monteiro S, Freitas R, Santos CN, Chen Z, Batista LM, et al. The role of plant defence proteins in fungal pathogenesis. Molecular Plant Pathology. 2007; 8:677–700. doi: 10.1111/j.1364-3703.2007.00419.x 20507530

4. Sels J, Mathys J, De Coninck BM, Cammue BP, De Bolle MF. Plant pathogenesis-related (PR) proteins: A focus on PR peptides. Plant Physiology and Biochemistry. 2008; 46:941–950. doi: 10.1016/j.plaphy.2008.06.011 18674922.

5. Petre B, Major I, Rouhier N, Duplessis S. Genome-wide analysis of eukaryote thaumatin-like proteins (TLPs) with an emphasis on poplar. BMC Plant Biology. 2011; 11:33–48. doi: 10.1186/1471-2229-11-33 21324123.

6. Fierens E, Gebruers K, Voet AR, De Maeyer M, Courtin CM, Delcour JA. Biochemical and structural characterization of TLXI, the Triticum aestivum L. thaumatin-like xylanase inhibitor. Journal of Enzyme Inhibition and Medicinal Chemistry. 2009; 24:646–654. doi: 10.1080/14756360802321831 18951281.

7. Cao J, Lv Y, Hou Z, Li X, Ding L. Expansion and evolution of thaumatin-like protein (TLP) gene family in six plants. Plant Growth Regulation. 2016; 79:299–307. http://doi.org/10.1007/s10725-015-0134-y.

8. Jesus-Pires CD, Ferreira-Neto JR, Bezerra-Neto JP, Kido EA, Oliveira Silva RL, Pandolfi V, et al. Plant thaumatin-like proteins: function, evolution and biotechnological applications. Current Protein and Peptide Science. 2020; 21:36–51. doi: 10.2174/1389203720666190318164905 30887921

9. González M, Brito N, González C. The Botrytis cinerea elicitor protein BcIEB1 interacts with the tobacco PR5-family protein osmotin and protects the fungus against its antifungal activity. New Phytologist. 2017; 215:397–410. doi: 10.1111/nph.14588 28480965.

10. Zhang Y, Gao Y, Liang Y, Dong Y, Yang X, Qiu D. Verticillium dahliae PevD1, an Alt a 1-like protein, targets cotton PR5-like protein and promotes fungal infection. Journal of Experimental Botany. 2019; 70:613–626. doi: 10.1093/jxb/ery351 30295911.

11. Chowdhury S, Basu A, Kundu S. Cloning, characterization and bacterial over-expression of an osmotin-like protein gene from Solanum nigrum L. with antifungal activity against three necrotrophic fungi. Molecular Biotechnology. 2015; 57:371–381. doi: 10.1007/s12033-014-9831-4 25572937

12. Chowdhury S, Basu A, Kundu S. Overexpression of a new osmotin-like protein gene (SindOLP) confers tolerance against biotic and abiotic stresses in sesame. Frontiers in Plant Science. 2017; 8:410–425. doi: 10.3389/fpls.2017.00410 28400780.

13. Gamir J, Darwiche R, Van’t Hof P, Choudhary V, Stumpe M, Schneiter R, et al. The sterol-binding activity of pathogenesis-related protein 1 reveals the mode of action of an antimicrobial protein. The Plant Journal. 2017; 89:502–509. doi: 10.1111/tpj.13398 27747953.

14. Lu S, Faris JD, Sherwood R, Friesen TL, Edwards MC. A dimeric PR-1-type pathogenesis-related protein interacts with ToxA and potentially mediates ToxA-induced necrosis in sensitive wheat. Molecular Plant Pathology. 2014; 15:650–663. doi: 10.1111/mpp.12122 24433289.

15. Breen S, Williams SJ, Winterberg B, Kobe B, Solomon PS. Wheat PR-1 proteins are targeted by necrotrophic pathogen effector proteins. The Plant Journal. 2016; 88:13–25. doi: 10.1111/tpj.13228 27258471.

16. Yang G, Tang L, Gong Y, Xie J, Fu Y, Jiang D, et al. A cerato-platanin protein SsCP1 targets plant PR1 and contributes to virulence of Sclerotinia sclerotiorum. New Phytologist. 2018; 217:739–755. doi: 10.1111/nph.14842 29076546.

17. Kolmer JA. Genetics of resistance to wheat leaf rust. Annual Review of Phytopathology. 1996; 34:435–455. doi: 10.1146/annurev.phyto.34.1.435 15012551.

18. Flor HH. Current status of the gene-for-gene concept. Annual Review of Phytopathology. 1971; 9:275–296. http://doi.org/10.1146/annurev.py.09.090171.001423.

19. Jones JD, Dangl JL. The plant immune system. Nature. 2006; 444:323–329. doi: 10.1038/nature05286 17108957.

20. Lagudah ES. Molecular genetics of race non-specific rust resistance in wheat. Euphytica. 2011; 179:81–91. http://doi.org/10.1007/s10681-010-0336-3.

21. Singh RP, Huerta-Espino J, Bhavani S, Herrera-Foessel SA, Singh D, Singh PK, et al. Race non-specific resistance to rust diseases in CIMMYT spring wheats. Euphytica. 2011; 179:175–186. http://doi.org/10.1007/s10681-010-0322-9.

22. Li X, Gao L, Zhang W, Liu J, Zhang Y, Wang H, et al. Characteristic expression of wheat PR5 gene in response to infection by the leaf rust pathogen, Puccinia triticina. Journal of Plant Interactions. 2015; 10:132–141. http://doi.org/10.1080/17429145.2015.1036140.

23. Gao L, Wang S, Zhang Y, Li X, Wang H, Liu D. Identification and characterization of a β-1, 3-glucanase gene, TcLr19Glu, involved in wheat resistance against Puccinia triticina. Journal of Plant Biochemistry and Biotechnology. 2016; 25:319–326. https://doi.org/10.1007/s13562-015-0344-4.

24. Zhang J, Wang F, Liang F, Zhang Y, Ma L, Wang H, et al. Functional analysis of a pathogenesis-related thaumatin-like protein gene TaLr35PR5 from wheat induced by leaf rust fungus. BMC Plant Biology. 2018; 18:76–87. doi: 10.1186/s12870-018-1297-2 29728059.

25. Yang Q, Huai B, Lu Y, Cai K, Guo J, Zhu X, et al. A stripe rust effector Pst18363 targets and stabilizes TaNUDX23 that promotes stripe rust disease. New Phytologist. 2020; 225:880–895. doi: 10.1111/nph.16199 31529497.

26. Huai B, Yang Q, Qian Y, Qian W, Kang Z, Liu J. ABA-induced sugar transporter TaSTP6 promotes wheat susceptibility to stripe rust. Plant Physiology. 2019; 181:1328–1343. doi: 10.1104/pp.19.00632 31540949.

27. Cristea IM, Williams R, Chait BT, Rout MP. Fluorescent proteins as proteomic probes. Molecular & Cellular Proteomics. 2005; 4:1933‒1941. doi: 10.1074/mcp.M500227-MCP200 16155292.

28. Rothbauer U, Zolghadr K, Muyldermans S, Schepers A, Cardoso MC, Leonhardt H. A versatile nanotrap for biochemical and functional studies with fluorescent fusion proteins. Molecular & Cellular Proteomics. 2008; 7:282‒289. doi: 10.1074/mcp.M700342-MCP200 17951627.

29. Gao L, Wang S, Li X, Wei X, Zhang Y, Wang H, et al. Expression and functional analysis of a pathogenesis-related protein 1 gene, TcLr19PR1, involved in wheat resistance against leaf rust fungus. Plant Molecular Biology Reporter. 2015; 33:797–805. http://doi.org/10.1007/s11105-014-0790-5.

30. Long DL, Kolmer JA. A North American system of nomenclature for Puccinia recondita f. sp. tritici. Phytopathology. 1989; 79:525–529. http://doi.org/10.1094/Phyto-79-525.

31. Gehl C, Waadt R, Kudla J, Mendel RR, Hänsch R. New gateway vectors for high throughput analyses of protein-protein interactions by bimolecular fluorescence complementation. Molecular Plant. 2009; 2:1051–1058. doi: 10.1093/mp/ssp040 19825679.

32. Dreher K, Callis J. Ubiquitin, hormones and biotic stress in plants. Annals of Botany. 2007; 99:787–822. doi: 10.1093/aob/mcl255 17220175.

33. Ghosh R, Chakrabarti C. Crystal structure analysis of NP24-I: a thaumatin like protein. Planta. 2008; 228: 883–890. doi: 10.1007/s00425-008-0790-5 18651170.

34. Anil Kumar S, Hima Kumari P, Shravan Kumar G, Mohanalatha C, Kavi Kishor PB. Osmotin: a plant sentinel and a possible agonist of mammalian adiponectin. Frontiers in Plant Science. 2015; 6:163–178. doi: 10.3389/fpls.2015.00163 25852715.

35. Petrov VD, Van Breusegem F. Hydrogen peroxide—a central hub for information flow in plant cells. AoB Plants. 2012; 2012:pls014. doi: 10.1093/aobpla/pls014 22708052.

36. Orozco-Cardenas M, Ryan CA. Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proceedings of the National Academy of Sciences of the United States of America. 1999; 96:6553–6557. doi: 10.1073/pnas.96.11.6553 10339626.

37. Chen YL, Lee CY, Cheng KT, Chang WH, Huang RN, Nam HG, et al. Quantitative peptidomics study reveals that a wound-induced peptide from PR-1 regulates immune signaling in tomato. The Plant Cell. 2014; 26:4135–4148. doi: 10.1105/tpc.114.131185 25361956.

38. Chien PS, Nam HG, Chen YR. A salt-regulated peptide derived from the CAP superfamily protein negatively regulates salt-stress tolerance in Arabidopsis. Journal of Experimental Botany. 2015; 66:5301–5313. doi: 10.1093/jxb/erv263 26093145.

39. Liu JJ, Sturrock R, Ekramoddoullah AK. The superfamily of thaumatin-like proteins: its origin, evolution, and expression towards biological function. Plant Cell Reports. 2010; 29: 419–436. doi: 10.1007/s00299-010-0826-8 20204373.

40. Panstruga R, Dodds PN. Terrific protein traffic: the mystery of effector protein delivery by filamentous plant pathogens. Science. 2009; 324:748–750. doi: 10.1126/science.1171652 19423815.

41. Scofield SR, Huang L, Brandt AS, Gill BS. Development of a virus-induced gene-silencing system for hexaploid wheat and its use in functional analysis of the Lr21-mediated leaf rust resistance pathway. Plant Physiology. 2005; 138:2165–2173. doi: 10.1104/pp.105.061861 16024691.

42. Liu P, Guo J, Zhang R, Zhao J, Liu C, Qi T, et al. TaCIPK10 interacts with and phosphorylates TaNH2 to activate wheat defense responses to stripe rust. 2019; 17: 956–968. Plant Biotechnology Journal. doi: 10.1111/pbi.13031 30451367.

43. Anand A, Zhou T, Trick HN, Gill BS, Bockus WW, Muthukrishnan S. Greenhouse and field testing of transgenic wheat plants stably expressing genes for thaumatin-like protein, chitinase and glucanase against Fusarium graminearum. Journal of Experimental Botany. 2003; 54: 1101–1111. doi: 10.1093/jxb/erg110 12598580.

44. Roelfs AP, Martell LB. Uredospore dispersal from a point source within a wheat canopy. Phytopathology. 1984; 74:1262–1267. http://doi.org/10.1094/Phyto-74-1262.

45. Ma L, Lukasik E, Gawehns F, Takken FL. The use of agroinfiltration for transient expression of plant resistance and fungal effector proteins in Nicotiana benthamiana leaves. Methods in Molecular Biology. 2012; 835:61–74. doi: 10.1007/978-1-61779-501-5_4 22183647.

46. Ma L, Cornelissen BJ, Takken FL. A nuclear localization for Avr2 from Fusarium oxysporum is required to activate the tomato resistance protein I-2. Frontiers in Plant Science. 2013; 4:94–105. doi: 10.3389/fpls.2013.00094 23596453.

47. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods. 2001; 25:402–408. doi: 10.1006/meth.2001.1262 11846609.

48. Ma L, Djavaheri M, Wang H, Larkan NJ, Haddadi P, Beynon E, et al. Leptosphaeria maculans effector protein AvrLm1 modulates plant immunity by enhancing MAP Kinase 9 phosphorylation. iScience. 2018; 3:177–191. doi: 10.1016/j.isci.2018.04.015 30428318.

49. Holzberg S, Brosio P, Gross C, Pogue GP. Barley stripe mosaic virus-induced gene silencing in a monocot plant. The Plant Journal. 2002; 30:315–327. doi: 10.1046/j.1365-313x.2002.01291.x 12000679.

50. Panwar V, McCallum B, Bakkeren G. Host-induced gene silencing of wheat leaf rust fungus Puccinia triticina pathogenicity genes mediated by the barley stripe mosaic virus. Plant Molecular Biology. 2013; 81:595–608. doi: 10.1007/s11103-013-0022-7 23417582.

51. Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB. Subcellular localization of H2O2 in plants, H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. The Plant Journal. 1997; 11:1187–1194. http://doi.org/10.1046/j.1365-313X.1997.11061187.x.

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