DOI QR코드

DOI QR Code

Nuclear Effectors in Plant Pathogenic Fungi

  • Surajit De Mandal (Department of Biotechnology, College of Life and Applied Sciences, Yeungnam University) ;
  • Junhyun Jeon (Department of Biotechnology, College of Life and Applied Sciences, Yeungnam University)
  • Received : 2022.07.25
  • Accepted : 2022.08.25
  • Published : 2022.10.31

Abstract

The nuclear import of proteins is a fundamental process in the eukaryotes including plant. It has become evident that such basic process is exploited by nuclear effectors that contain nuclear localization signal (NLS) and are secreted into host cells by fungal pathogens of plants. However, only a handful of nuclear effectors have been known and characterized to date. Here, we first summarize the types of NLSs and prediction tools available, and then delineate examples of fungal nuclear effectors and their roles in pathogenesis. Based on the knowledge on NLSs and what has been gleaned from the known nuclear effectors, we point out the gaps in our understanding of fungal nuclear effectors that need to be filled in the future researches.

Keywords

Acknowledgement

This work was supported by a grant from National Research Foundation of Korea [NRF-2021R1A2C2012002].

References

  1. Strambio-De-Castillia C, Niepel M, Rout MP. The nuclear pore complex: bridging nuclear transport and gene regulation. Nat Rev Mol Cell Biol. 2010;11(7):490-501. https://doi.org/10.1038/nrm2928
  2. Cronshaw JM, Krutchinsky AN, Zhang W, et al. Proteomic analysis of the mammalian nuclear pore complex. J Cell Biol. 2002;158(5):915-927. https://doi.org/10.1083/jcb.200206106
  3. Rout MP, Aitchison JD, Suprapto A, et al. The yeast nuclear pore complex: composition, architecture, and transport mechanism. J Cell Biol. 2000; 148(4):635-51651. https://doi.org/10.1083/jcb.148.4.635
  4. Lu J, Wu T, Zhang B, et al. Types of nuclear localization signals and mechanisms of protein import into the nucleus. Cell Commun Signal. 2021;19(1):1-10. https://doi.org/10.1186/s12964-020-00683-x
  5. Sonah H, Deshmukh RK, B elanger RR. Computational prediction of effector proteins in fungi: opportunities and challenges. Front Plant Sci. 2016;7:126.
  6. Rivas S, Genin S. A plethora of virulence strategies hidden behind nuclear targeting of microbial effectors. Front Plant Sci. 2011;2:104.
  7. Petre B, Kamoun S. How do filamentous pathogens deliver effector proteins into plant cells? PLoS Biol. 2014;12(2):e1001801.
  8. He Q, McLellan H, Boevink PC, et al. All roads lead to susceptibility: the many modes of action of fungal and oomycete intracellular effectors. Plant Commun. 2020;1(4):100050.
  9. Presti LL, Lanver D, Schweizer G, et al. Fungal effectors and plant susceptibility. Annu Rev Plant Biol. 2015;66(1):513-545. https://doi.org/10.1146/annurev-arplant-043014-114623
  10. Jaswal R, Kiran K, Rajarammohan S, et al. Effector biology of biotrophic plant fungal pathogens: Current advances and future prospects. Microbiol Res. 2020;241:126567.
  11. Figueroa M, Ortiz D, Henningsen EC. Tactics of host manipulation by intracellular effectors from plant pathogenic fungi. Curr Opin Plant Biol. 2021;62:102054.
  12. Tariqjaveed M, Mateen A, Wang S, et al. Versatile effectors of phytopathogenic fungi target host immunity. J Integr Plant Biol. 2021;63(11):1856-1873. https://doi.org/10.1111/jipb.13162
  13. Wu Y, Xie L, Jiang Y, et al. Prediction of effector proteins and their implications in pathogenicity of phytopathogenic filamentous fungi: a review. Int J Biol Macromol. 2022;206:188-202. https://doi.org/10.1016/j.ijbiomac.2022.02.133
  14. Qin J, Wang K, Sun L, et al. The plant-specific transcription factors CBP60g and SARD1 are targeted by a Verticillium secretory protein VdSCP41 to modulate immunity. elife. 2018;7:e34902.
  15. Kim S, Kim C-Y, Park S-Y, et al. Two nuclear effectors of the rice blast fungus modulate host immunity via transcriptional reprogramming. Nat Commun. 2020;11(1):1-11.
  16. Kosugi S, Hasebe M, Matsumura N, et al. Six classes of nuclear localization signals specific to different binding grooves of importin α. J Biol Chem. 2009;284(1):478-485.
  17. Fontes MRM, Teh T, Kobe B. Structural basis of recognition of monopartite and bipartite nuclear localization sequences by mammalian importin-a. J Mol Biol. 2000;297(5):1183-1194. https://doi.org/10.1006/jmbi.2000.3642
  18. Christie M, Chang C-W, Rona G, et al. Structural biology and regulation of protein import into the nucleus. J Mol Biol. 2016;428(10 Pt A):2060-2090. https://doi.org/10.1016/j.jmb.2015.10.023
  19. Bernardes NE, Fukuda CA, da Silva TD, et al. Comparative study of the interactions between fungal transcription factor nuclear localization sequences with mammalian and fungal importin-alpha. Sci Rep. 2020;10(1):1-13. https://doi.org/10.1038/s41598-019-56847-4
  20. Marfori M, Mynott A, Ellis JJ, et al. Molecular basis for specificity of nuclear import and prediction of nuclear localization. Biochim Biophys Acta. 2011;1813(9):1562-1577. https://doi.org/10.1016/j.bbamcr.2010.10.013
  21. Lee BJ, Cansizoglu AE, Suel KE, et al. Rules for € nuclear localization sequence recognition by karyopherinβ2. Cell. 2006;126(3):543-558. https://doi.org/10.1016/j.cell.2006.05.049
  22. Wang L, Li M, Cai M, et al. A PY-nuclear localization signal is required for nuclear accumulation of HCMV UL79 protein. Med Microbiol Immunol. 2012;201(3):381-387. https://doi.org/10.1007/s00430-012-0243-4
  23. Steidl S, Tuncher A, Goda H, et al. A single subunit of a heterotrimeric CCAAT-binding complex carries a nuclear localization signal: piggy back transport of the pre-assembled complex to the nucleus. J Mol Biol. 2004;342(2):515-524. https://doi.org/10.1016/j.jmb.2004.07.011
  24. Imagawa M, Sakaue R, Tanabe A, et al. Two nuclear localization signals are required for nuclear translocation of nuclear factor 1-A. FEBS Lett. 2000;484(2):118-124. https://doi.org/10.1016/S0014-5793(00)02119-0
  25. Chen C-F, Li S, Chen Y, et al. The nuclear localization sequences of the BRCA1 protein interact with the importin-α subunit of the nuclear transport signal receptor. J Biol Chem. 1996;271(51):32863-32868. https://doi.org/10.1074/jbc.271.51.32863
  26. Yano K-i, Morotomi K, Saito H, et al. Nuclear localization signals of the BRCA2 protein. Biochem Biophys Res Commun. 2000;270(1):171-175. https://doi.org/10.1006/bbrc.2000.2392
  27. Burich R, Lei M. Two bipartite NLSs mediate constitutive nuclear localization of Mcm10. Curr Genet. 2003;44(4):195-201.
  28. Tuncher A, Spr € ote P, Gehrke A, et al. The CCAAT-binding complex of eukaryotes: evolution of a second NLS in the HapB subunit of the filamentous fungus Aspergillus nidulans despite functional conservation at the molecular level between yeast, A. nidulans and human. J Mol Biol. 2005;352(3):517-533. https://doi.org/10.1016/j.jmb.2005.06.068
  29. Luo M, Pang CWM, Gerken AE, et al. Multiple nuclear localization sequences allow modulation of 5-lipoxygenase nuclear import. Traffic. 2004;5(11):847-854. https://doi.org/10.1111/j.1600-0854.2004.00227.x
  30. Reisenauer MR, Wang SW, Xia Y, et al. Dot1a contains three nuclear localization signals and regulates the epithelial Na + channel (ENaC) at multiple levels. Am J Physiol Renal Physiol. 2010;299(1):F63-F76. https://doi.org/10.1152/ajprenal.00105.2010
  31. Nadler SG, Tritschler D, Haffar OK, et al. Differential expression and sequence-specific interaction of karyopherin α with nuclear localization sequences. J Biol Chem. 1997;272(7):4310-4315. https://doi.org/10.1074/jbc.272.7.4310
  32. Liu M-T, Hsu T-Y, Chen J-Y, et al. Epstein-Barr virus DNase contains two nuclear localization signals, which are different in sensitivity to the hydrophobic regions. Virology. 1998;247(1):62-73. https://doi.org/10.1006/viro.1998.9228
  33. Nakai K, Horton P. PSORT: a program for detecting the sorting signals of proteins and predicting their subcellular localization. Trends Biochem Sci. 1999;24(1):34-636. https://doi.org/10.1016/S0968-0004(98)01336-X
  34. Cokol M, Nair R, Rost B. Finding nuclear localization signals. EMBO Rep. 2000;1(5):411-415. https://doi.org/10.1093/embo-reports/kvd092
  35. Nguyen Ba AN, Pogoutse A, Provart N, et al. NLStradamus: a simple hidden markov model for nuclear localization signal prediction. BMC Bioinformatics. 2009;10(1):202-211.
  36. Kosugi S, Hasebe M, Tomita M, et al. Systematic identification of cell cycle-dependent yeast nucleocytoplasmic shuttling proteins by prediction of composite motifs. Proc Natl Acad Sci USA. 2009;106(25):10171-10176. https://doi.org/10.1073/pnas.0900604106
  37. Bernhofer M, Goldberg T, Wolf S, et al. NLSdb-major update for database of nuclear localization signals and nuclear export signals. Nucleic Acids Res. 2018;46(D1):D503-D508. https://doi.org/10.1093/nar/gkx1021
  38. Hicks GR, Raikhel NV. Protein import into the nucleus: an integrated view. Annu Rev Cell Dev Biol. 1995;11(1):155-188. https://doi.org/10.1146/annurev.cb.11.110195.001103
  39. Brameier M, Krings A, MacCallum RM. NucPred-predicting nuclear localization of proteins. Bioinformatics. 2007;23(9):1159-1160. https://doi.org/10.1093/bioinformatics/btm066
  40. Guo Y, Yang Y, Huang Y, et al. Discovering nuclear targeting signal sequence through protein language learning and multivariate analysis. Anal Biochem. 2020;591:113565.
  41. Ahmed MB, Santos K, Sanchez IB, et al. A rust fungal effector binds plant DNA and modulates transcription. Sci Rep. 2018;8(1):1-14.
  42. Vargas WA, Sanz-Mart in JM, Rech GE, et al. A fungal effector with host nuclear localization and DNA-binding properties is required for maize anthracnose development. Mol Plant Microbe Interact. 2016;29(2):83-95. https://doi.org/10.1094/MPMI-09-15-0209-R
  43. Qi T, Guo J, Liu P, et al. Stripe rust effector PstGSRE1 disrupts nuclear localization of ROS-promoting transcription factor TaLOL2 to defeat ROS-induced defense in wheat. Mol Plant. 2019;12(12):1624-1638. https://doi.org/10.1016/j.molp.2019.09.010
  44. Qi M, Link TI, Muller M, et al. A small cysteine-rich protein from the asian soybean rust fungus, Phakopsora pachyrhizi, suppresses plant immunity. PLoS Pathog. 2016;12(9):e1005827.
  45. Wang X, Yang B, Li K, et al. A conserved Puccinia striiformis protein interacts with wheat NPR1 and reduces induction of pathogenesis-related genes in response to pathogens. Mol Plant Microbe Interact. 2016;29(12):977-989. https://doi.org/10.1094/MPMI-10-16-0207-R
  46. Redkar A, Hoser R, Schilling L, et al. A secreted effector protein of Ustilago maydis guides maize leaf cells to form tumors. Plant Cell. 2015;27(4):1332-1351. https://doi.org/10.1105/tpc.114.131086
  47. Chang P, Fan X, Chen J. Function and subcellular localization of Gcn5, a histone acetyltransferase in Candida albicans. Fungal Genet Biol. 2015;81:132-141. https://doi.org/10.1016/j.fgb.2015.01.011
  48. Zhang S, Liang M, Naqvi NI, et al. Phototrophy and starvation-based induction of autophagy upon removal of Gcn5-catalyzed acetylation of Atg7 in Magnaporthe oryzae. Autophagy. 2017;13(8):1318-1330. https://doi.org/10.1080/15548627.2017.1327103
  49. Chen X, Duan Y, Qiao F, et al. A secreted fungal effector suppresses rice immunity through host histone hypoacetylation. New Phytologist. 2022;235(5):1977-1994. https://doi.org/10.1111/nph.18265
  50. Zhu C, Liu J-H, Zhao J-H, et al. A fungal effector suppresses the nuclear export of AGO1-miRNA complex to promote infection in plants. Proc Natl Acad Sci USA. 2022;119(12):e2114583119.
  51. Pennington HG, Jones R, Kwon S, et al. The fungal ribonuclease-like effector protein CSEP0064/ BEC1054 represses plant immunity and interferes with degradation of host ribosomal RNA. PLoS Pathog. 2019;15(3):e1007620.
  52. Yin CM, Li JJ, Wang D, et al. A secreted ribonuclease effector from Verticillium dahliae localizes in the plant nucleus to modulate host immunity. Molecular Plant Pathology. 2022;23(8):1122-1140. https://doi.org/10.1111/mpp.13213
  53. Singh SK, Verma S, Singh K, et al. The nuclear effector ArPEC25 from the necrotrophic fungus Ascochyta rabiei targets the chickpea transcription factor CaβLIM1a and negatively modulates lignin biosynthesis for host susceptibility. bioRxiv. 2021. DOI:10.1101/2021.09.02.458738
  54. Rafiei V, V el€ez H, Tzelepis G. The phospholipase VlsPLA2 from the plant pathogen Verticillium longisporum is a virulence factor targeting host nuclei and suppressing PTI-related hypersensitive response. bioRxiv. 2022. DOI:10.1101/2022.03.19.484916
  55. Li T, Wu Y, Wang Y, et al. Secretome profiling reveals virulence-associated proteins of Fusarium proliferatum during interaction with banana fruit. Biomolecules. 2019;9(6):246.
  56. Hoang CV, Bhaskar CK, Ma L-S. A novel core effector Vp1 promotes fungal colonization and virulence of Ustilago maydis. JoF. 2021;7(8):589.
  57. Han Z, Xiong D, Xu Z, et al. The Cytospora chrysosperma virulence effector CcCAP1 mainly localizes to the plant nucleus to suppress plant immune responses. Msphere. 2021;6(1):e00883-00820.
  58. Xu Z, Xiong D, Han Z, et al. A putative effector CcSp84 of Cytospora chrysosperma localizes to the plant nucleus to trigger plant immunity. IJMS. 2022;23(3):1614.
  59. Zhang L, Ni H, Du X, et al. The Verticillium-specific protein VdSCP7 localizes to the plant nucleus and modulates immunity to fungal infections. New Phytol. 2017;215(1):368-381.
  60. Liu L, Wang Z, Li J, et al. Verticillium dahliae secreted protein Vd424Y is required for full virulence, targets the nucleus of plant cells, and induces cell death. Mol Plant Pathol. 2021;22(9):1109-1120. https://doi.org/10.1111/mpp.13100
  61. Voss S, Betz R, Heidt S, et al. RiCRN1, a crinkler effector from the arbuscular mycorrhizal fungus Rhizophagus irregularis, functions in arbuscule development. Front Microbiol. 2018;9:2068.
  62. Kanneganti TD, Bai X, Tsai CW, et al. A functional genetic assay for nuclear trafficking in plants. Plant J. 2007;50(1):149-158. https://doi.org/10.1111/j.1365-313X.2007.03029.x
  63. Chen T, Peng J, Yin X, et al. Importin-as are required for the nuclear localization and function of the Plasmopara viticola effector PvAVH53. Hortic Res. 2021;8(1):46.
  64. Scott MS, Boisvert F-M, McDowall MD, et al. Characterization and prediction of protein nucleolar localization sequences. Nucleic Acids Res. 2010;38(21):7388-7399. https://doi.org/10.1093/nar/gkq653
  65. Caly L, Druce JD, Catton MG, et al. The FDA-approved drug ivermectin inhibits the replication of SARS-CoV-2 in vitro. Antiviral Res. 2020;178:104787.
  66. Wolff B, Sanglier J-J, Wang Y. Leptomycin B is an inhibitor of nuclear export: inhibition of nucleocytoplasmic translocation of the human immunodeficiency virus type 1 (HIV-1) rev protein and rev-dependent mRNA. Chem Biol. 1997;4(2):139-147. https://doi.org/10.1016/S1074-5521(97)90257-X