リケラボ論文検索は、全国の大学リポジトリにある学位論文・教授論文を一括検索できる論文検索サービスです。

リケラボ 全国の大学リポジトリにある学位論文・教授論文を一括検索するならリケラボ論文検索大学・研究所にある論文を検索できる

リケラボ 全国の大学リポジトリにある学位論文・教授論文を一括検索するならリケラボ論文検索大学・研究所にある論文を検索できる

大学・研究所にある論文を検索できる 「A blast fungus zinc-finger fold effector binds to a hydrophobic pocket in host Exo70 proteins to modulate immune recognition in rice」の論文概要。リケラボ論文検索は、全国の大学リポジトリにある学位論文・教授論文を一括検索できる論文検索サービスです。

コピーが完了しました

URLをコピーしました

論文の公開元へ論文の公開元へ
書き出し

A blast fungus zinc-finger fold effector binds to a hydrophobic pocket in host Exo70 proteins to modulate immune recognition in rice

De la Concepcion, Juan Carlos Fujisaki, Koki Bentham, Adam R. Cruz Mireles, Neftaly Sanchez de Medina Hernandez, Victor Shimizu, Motoki Lawson, David M. Kamoun, Sophien Terauchi, Ryohei Banfield, Mark J. 京都大学 DOI:10.1073/pnas.2210559119

2022.10.25

概要

Exocytosis plays an important role in plant–microbe interactions, in both pathogenesis and symbiosis. Exo70 proteins are integral components of the exocyst, an octameric complex that mediates tethering of vesicles to membranes in eukaryotes. Although plant Exo70s are known to be targeted by pathogen effectors, the underpinning molecular mechanisms and the impact of this interaction on infection are poorly understood. Here, we show the molecular basis of the association between the effector AVR-Pii of the blast fungus Maganaporthe oryzae and rice Exo70 alleles OsExo70F2 and OsExo70F3, which is sensed by the immune receptor pair Pii via an integrated RIN4/NOI domain. The crystal structure of AVR-Pii in complex with OsExo70F2 reveals that the effector binds to a conserved hydrophobic pocket in Exo70, defining an effector/target binding interface. Structure-guided and random mutagenesis validates the importance of AVR-Pii residues at the Exo70 binding interface to sustain protein association and disease resistance in rice when challenged with fungal strains expressing effector mutants. Furthermore, the structure of AVR-Pii defines a zinc-finger effector fold (ZiF) distinct from the MAX (Magnaporthe Avrs and ToxB-like) fold previously described for a majority of characterized M. oryzae effectors. Our data suggest that blast fungus ZiF effectors bind a conserved Exo70 interface to manipulate plant exocytosis and that these effectors are also baited by plant immune receptors, pointing to new opportunities for engineering disease resistance.

この論文で使われている画像

参考文献

1. M. R. Heider, M. Munson, Exorcising the exocyst complex. Traffic 13, 898–907 (2012).

2. B. Wu, W. Guo, The exocyst at a glance. J. Cell Sci. 128, 2957–2964 (2015).

3. D. R. TerBush, T. Maurice, D. Roth, P. Novick, The exocyst is a multiprotein complex required for exocytosis in Saccharomyces cerevisiae. EMBO J. 15, 6483–6494 (1996).

4. K. Mei et al., Cryo-EM structure of the exocyst complex. Nat. Struct. Mol. Biol. 25, 139–146 (2018).

5. M. R. Heider et al., Subunit connectivity, assembly determinants and architecture of the yeast exocyst complex. Nat. Struct. Mol. Biol. 23, 59–66 (2016).

6. A. Picco et al., The in vivo architecture of the exocyst provides structural basis for exocytosis. Cell168, 400–412.e18 (2017).

7. H. Maib, D. H. Murray, A mechanism for exocyst-mediated tethering via Arf6 and PIP5K1C driven phosphoinositide conversion. Curr. Biol. 32, 2821–2833. e2826 (2022).

8. L. Synek et al., Plasma membrane phospholipid signature recruits the plant exocyst complex via the EXO70A1 subunit. Proc. Natl. Acad. Sci. U.S.A. 118, e2105287118 (2021).

9. S. J. An et al., An active tethering mechanism controls the fate of vesicles. Nat. Commun. 12, 5434(2021).

10. B. Saeed, C. Brillada, M. Trujillo, Dissecting the plant exocyst. Curr. Opin. Plant Biol. 52, 69–76 (2019).

11. S. M. Ahmed et al., Exocyst dynamics during vesicle tethering and fusion. Nat. Commun. 9, 5140(2018).

12. F. Cvrˇckov´a et al., Evolution of the land plant exocyst complexes. Front. Plant Sci. 3, 159 (2012).

13. S. Holden et al., A lineage-specific Exo70 is required for receptor kinase-mediated immunity in barley. Sci. Adv. 8, eabn7258.

14. L. Kalmbach et al., Transient cell-specific EXO70A1 activity in the CASP domain and Casparian strip localization. Nat. Plants 3, 17058 (2017).

15. T. Ogura et al., Root system depth in Arabidopsis is shaped by EXOCYST70A3 via the dynamic modulation of auxin transport. Cell 178, 400–412.e16 (2019).

16. I. Kulich et al., Cell wall maturation of Arabidopsis trichomes is dependent on exocyst subunit EXO70H4 and involves callose deposition. Plant Physiol. 168, 120–131 (2015).

17. I. Kulich et al., Exocyst subunit EXO70H4 has a specific role in callose synthase secretion and silica accumulation. Plant Physiol. 176, 2040–2051 (2018).

18. X. Zhang, N. Pumplin, S. Ivanov, M. J. Harrison, EXO70I is required for development of a sub- domain of the periarbuscular membrane during arbuscular mycorrhizal symbiosis. Curr. Biol. 25, 2189–2195 (2015).

19. A. K. Acheampong et al., EXO70D isoforms mediate selective autophagic degradation of type-A ARR proteins to regulate cytokinin sensitivity. Proc. Natl. Acad. Sci. U.S.A. 117, 27034–27043 (2020).

20. I. Kulich et al., Arabidopsis exocyst subcomplex containing subunit EXO70B1 is involved in autophagy-related transport to the vacuole. Traffic 14, 1155–1165 (2013).

21. C. Brillada et al., Exocyst subunit Exo70B2 is linked to immune signaling and autophagy. Plant Cell33, 404–419 (2021).

22. Y. Du, E. J. R. Overdijk, J. A. Berg, F. Govers, K. Bouwmeester, Solanaceous exocyst subunits are involved in immunity to diverse plant pathogens. J. Exp. Bot. 69, 655–666 (2018).

23. J. Guo et al., Bph6 encodes an exocyst-localized protein and confers broad resistance to planthoppers in rice. Nat. Genet. 50, 297–306 (2018).

24. M. Stegmann et al., The exocyst subunit Exo70B1 is involved in the immune response of Arabidopsis thaliana to different pathogens and cell death. Plant Signal. Behav. 8, e27421 (2013).

25. T. Pecenkov´a et al., The role for the exocyst complex subunits Exo70B2 and Exo70H1 in the plant-pathogen interaction. J. Exp. Bot. 62, 2107–2116 (2011).

26. T. Zhao et al., A truncated NLR protein, TIR-NBS2, is required for activated defense responses in the exo70B1 mutant. PLoS Genet. 11, e1004945 (2015).

27. N. Liu et al., CALCIUM-DEPENDENT PROTEIN KINASE5 associates with the truncated NLR protein TIR-NBS2 to contribute to exo70B1-mediated immunity. Plant Cell 29, 746–759 (2017).

28. K. Fujisaki et al., Rice Exo70 interacts with a fungal effector, AVR-Pii, and is required for AVR-Pii-triggered immunity. Plant J. 83, 875–887 (2015).

29. P. Sabol, I. Kulich, V. ˇZ´arsk´y, RIN4 recruits the exocyst subunit EXO70B1 to the plasma membrane.J. Exp. Bot. 68, 3253–3265 (2017).

30. T. J. Redditt et al., AvrRpm1 functions as an ADP-ribosyl transferase to modify NOIdomain-containing proteins, including Arabidopsis and soybean RPM1-interacting Protein4.Plant Cell 31, 2664–2681 (2019).

31. M. S. Mukhtar et al.; European Union Effectoromics Consortium, Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 333, 596–601 (2011).

32. R. Weßling et al., Convergent targeting of a common host protein-network by pathogen effectors from three kingdoms of life. Cell Host Microbe 16, 364–375 (2014).

33. P. C. Bailey et al., Dominant integration locus drives continuous diversification of plant immune receptors with exogenous domain fusions. Genome Biol. 19, 23 (2018).

34. H. J. Brabham, I. Hern´andez-Pinz´on, S. Holden, J. Lorang, M. J. Moscou, An ancient integration ina plant NLR is maintained as a trans-species polymorphism. bioRxiv [Preprint] (2018). https://doi. org/10.1101/239541 (Accessed 6 October 2022).

35. T. Kroj, E. Chanclud, C. Michel-Romiti, X. Grand, J. B. Morel, Integration of decoy domains derived from protein targets of pathogen effectors into plant immune receptors is widespread. New Phytol. 210, 618–626 (2016).

36. P. F. Sarris, V. Cevik, G. Dagdas, J. D. Jones, K. V. Krasileva, Comparative analysis of plant immune receptor architectures uncovers host proteins likely targeted by pathogens. BMC Biol. 14, 8 (2016).

37. C. H. Khang et al., Translocation of Magnaporthe oryzae effectors into rice cells and their subsequent cell-to-cell movement. Plant Cell 22, 1388–1403 (2010).

38. M. C. Giraldo et al., Two distinct secretion systems facilitate tissue invasion by the rice blast fungusMagnaporthe oryzae. Nat. Commun. 4, 1996 (2013).

39. R. A. Dean et al., The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434,980–986 (2005).

40. K. Yoshida et al., Association genetics reveals three novel avirulence genes from the rice blast fungal pathogen Magnaporthe oryzae. Plant Cell 21, 1573–1591 (2009).

41. K. de Guillen et al., Structure analysis uncovers a highly diverse but structurally conserved effector family in phytopathogenic fungi. PLoS Pathog. 11, e1005228 (2015).

42. S. Cesari, M. Bernoux, P. Moncuquet, T. Kroj, P. N. Dodds, A novel conserved mechanism for plant NLR protein pairs: The “integrated decoy” hypothesis. Front. Plant Sci. 5, 606 (2014).

43. A. Maqbool et al., Structural basis of pathogen recognition by an integrated HMA domain in a plant NLR immune receptor. eLife 4, e08709 (2015).

44. L. Guo et al., Specific recognition of two MAX effectors by integrated HMA domains in plant immune receptors involves distinct binding surfaces. Proc. Natl. Acad. Sci. U.S.A. 115, 11637–11642 (2018).

45. D. Ortiz et al., Recognition of the Magnaporthe oryzae effector AVR-pia by the decoy domain of the rice NLR immune receptor RGA5. Plant Cell 29, 156–168 (2017).

46. J. C. De la Concepcion et al., Polymorphic residues in rice NLRs expand binding and response to effectors of the blast pathogen. Nat. Plants 4, 576–585 (2018).

47. J. C. De la Concepcion et al., The allelic rice immune receptor Pikh confers extended resistance to strains of the blast fungus through a single polymorphism in the effector binding interface. PLoS Pathog. 17, e1009368 (2021).

48. J. C. De la Concepcion et al., Functional diversification gave rise to allelic specialization in a rice NLR immune receptor pair. eLife 10, e71662 (2021).

49. A. Białas et al., Lessons in effector and NLR biology of plant-microbe systems. Mol. Plant Microbe Interact. 31, 34–45 (2018).

50. Y. Liu et al., A designer rice NLR immune receptor confers resistance to the rice blast fungus carrying noncorresponding avirulence effectors. Proc. Natl. Acad. Sci. U.S.A. 118, e2110751118 (2021).

51. J. Kourelis, C. Marchal, S. Kamoun, NLR immune receptor-nanobody fusions confer plant disease resistance. bioRxiv [Preprint] (2021). https://doi.org/10.1101/2021.10.24.465418 (Accessed 6 October 2022).

52. J. C. De la Concepcion et al., Protein engineering expands the effector recognition profile of a rice NLR immune receptor. eLife 8, e47713 (2019).

53. S. Cesari et al., New recognition specificity in a plant immune receptor by molecular engineering of its integrated domain. Nat. Commun. 13, 1524 (2022).

54. J. H. Maidment et al., Effector target-guided engineering of an integrated domain expands the disease resistance profile of a rice NLR immune receptor. bioRxiv [Preprint] (2022). https://doi.org/ 10.1101/2022.06.14.496076 (Accessed 6 October 2022).

55. G. Dong, A. H. Hutagalung, C. Fu, P. Novick, K. M. Reinisch, The structures of exocyst subunit Exo70p and the Exo84p C-terminal domains reveal a common motif. Nat. Struct. Mol. Biol. 12, 1094–1100 (2005).

56. B. A. Moore, H. H. Robinson, Z. Xu, The crystal structure of mouse Exo70 reveals unique features of the mammalian exocyst. J. Mol. Biol. 371, 410–421 (2007).

57. C. Zhang et al., Endosidin2 targets conserved exocyst complex subunit EXO70 to inhibit exocytosis.Proc. Natl. Acad. Sci. U.S.A. 113, E41–E50 (2016).

58. H. Takagi et al., MutMap-Gap: Whole-genome resequencing of mutant F2 progeny bulk combined with de novo assembly of gap regions identifies the rice blast resistance gene Pii. New Phytol. 200, 276–283 (2013).

59. K. Fujisaki et al., An unconventional NOI/RIN4 domain of a rice NLR protein binds host EXO70 protein to confer fungal immunity. bioRxiv [Preprint] (2017). https://doi.org/10.1101/239400 (Accessed 6 October 2022).

60. M. Franceschetti et al., Effectors of filamentous plant pathogens: Commonalities amid diversity.Microbiol. Mol. Biol. Rev. 81, e00066 (2017).

61. E. F. Pettersen et al., UCSF ChimeraX: Structure visualization for researchers, educators, and developers. Protein Sci. 30, 70–82 (2021).

62. E. Krissinel, K. Henrick, Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr. D Biol. Crystallogr. 60, 2256–2268 (2004).

63. E. Krissinel, Stock-based detection of protein oligomeric states in jsPISA. Nucleic Acids Res. 43, W314–W319 (2015).

64. H. Ashkenazy et al., ConSurf 2016: An improved methodology to estimate and visualize evolutionary conservation in macromolecules. Nucleic Acids Res. 44, W344–W350 (2016).

65. J. Jumper et al., Highly accurate protein structure prediction with AlphaFold. Nature 596, 583–589(2021).

66. M. Mirdita, S. Ovchinnikov, M. Steinegger, ColabFold—Making protein folding accessible to all.Nat. Methods, 19, 679–682 (2022).

67. Y. Du, M. H. Mpina, P. R. Birch, K. Bouwmeester, F. Govers, Phytophthora infestans RXLR effector AVR1 interacts with exocyst component Sec5 to manipulate plant immunity. Plant Physiol. 169, 1975–1990 (2015).

68. T. B. Frailie, R. W. Innes, Engineering healthy crops: Molecular strategies for enhancing the plant immune system. Curr. Opin. Biotechnol. 70, 151–157 (2021).

69. A. R. Bentham et al., A single amino acid polymorphism in a conserved effector of the multihost blast fungus pathogen expands host-target binding spectrum. PLoS Pathog. 17, e1009957 (2021).

70. X. Zhang et al., A positive-charged patch and stabilized hydrophobic core are essential for avirulence function of AvrPib in the rice blast fungus. Plant J. 96, 133–146 (2018).

71. Z.-M. Zhang et al., Solution structure of the Magnaporthe oryzae avirulence protein AvrPiz-t.J. Biomol. NMR 55, 219–223 (2013).

72. R. Gamsjaeger, C. K. Liew, F. E. Loughlin, M. Crossley, J. P. Mackay, Sticky fingers: Zinc-fingers as protein-recognition motifs. Trends Biochem. Sci. 32, 63–70 (2007).

73. J. M. Matthews, M. Sunde, Zinc fingers–Folds for many occasions. IUBMB Life 54, 351–355 (2002).

74. X. Zhang et al., Crystal structure of the Melampsora lini effector AvrP reveals insights into a possible nuclear function and recognition by the flax disease resistance protein P. Mol. Plant Pathol. 19, 1196–1209 (2018).

75. A. R. Bentham et al., A molecular roadmap to the plant immune system. J. Biol. Chem. 295,14916–14935 (2020).

76. J. H. R. Maidment et al., Multiple variants of the fungal effector AVR-Pik bind the HMA domain of the rice protein OsHIPP19, providing a foundation to engineer plant defense. J. Biol. Chem. 296, 100371 (2021).

77. K. Oikawa et al., The blast pathogen effector AVR-Pik binds and stabilizes rice heavymetal-associated (HMA) proteins to co-opt their function in immunity. bioRxiv [Preprint] (2020). https://doi.org/10.1101/2020.12.01.406389 (Accessed 6 October 2022).

78. ´A. Pi~neiro et al., AFFINImeter: A software to analyze molecular recognition processes fromexperimental data. Anal. Biochem. 577, 117–134 (2019).

79. H. Kanzaki et al., Arms race co-evolution of Magnaporthe oryzae AVR-Pik and rice Pik genes driven by their physical interactions. Plant J. 72, 894–907 (2012).

80. J. C. De la Concepcion, A. R. Bentham, D. Lawson, M. J. Banfield, Complex of rice blast (Magnaporthe oryzae) effector protein AVR-Pii with the host target Exo70F2 from Rice (Oryza sativa). Protein Data Bank. https://www.rcsb.org/structure/7PP2. Deposited 13 September 2021.

参考文献をもっと見る

全国の大学の
卒論・修論・学位論文

一発検索!

この論文の関連論文を見る