Mycobiology

The Korean Society of Mycology (한국균학회)
권호 표지
DOI QR코드

DOI QR Code

A PAS-Containing Histidine Kinase is Required for Conidiation, Appressorium Formation, and Disease Development in the Rice Blast Fungus, Magnaporthe oryzae

  • Shin, Jong-Hwan (Division of Bio-Resource Sciences and BioHerb Research Institute, Kangwon National University) ;
  • Gumilang, Adiyantara (Division of Bio-Resource Sciences and BioHerb Research Institute, Kangwon National University) ;
  • Kim, Moon-Jong (Division of Bio-Resource Sciences and BioHerb Research Institute, Kangwon National University) ;
  • Han, Joon-Hee (Division of Bio-Resource Sciences and BioHerb Research Institute, Kangwon National University) ;
  • Kim, Kyoung Su (Division of Bio-Resource Sciences and BioHerb Research Institute, Kangwon National University)
  • Received : 2019.08.29
  • Accepted : 2019.10.31
  • Published : 2019.12.01
Download PDF
⟨ Previous Next ⟩

Abstract

Rice blast disease, caused by the ascomycete fungus Magnaporthe oryzae, is one of the most important diseases in rice production. PAS (period circadian protein, aryl hydrocarbon receptor nuclear translocator protein, single-minded protein) domains are known to be involved in signal transduction pathways, but their functional roles have not been well studied in fungi. In this study, targeted gene deletion was carried out to investigate the functional roles of the PAS-containing gene MoPAS1 (MGG_02665) in M. oryzae. The deletion mutant ΔMopas1 exhibited easily wettable mycelia, reduced conidiation, and defects in appressorium formation and disease development compared to the wild type and complemented transformant. Exogenous cAMP restored appressorium formation in ΔMopas1, but the shape of the restored appressorium was irregular, indicating that MoPAS1 is involved in sensing the hydrophobic surface. To examine the expression and localization of MoPAS1 in M. oryzae during appressorium development and plant infection, we constructed a MoPAS1:GFP fusion construct. MoPAS1:GFP was observed in conidia and germ tubes at 0 and 2 h post-infection (hpi) on hydrophobic cover slips. By 8 hpi, most of the GFP signal was observed in the appressoria. During invasive growth in host cells, MoPAS1:GFP was found to be fully expressed in not only the appressoria but also invasive hyphae, suggesting that MoPAS may contribute to disease development in host cells. These results expand our knowledge of the roles of PAS-containing regulatory genes in the plant-pathogenic fungus M. oryzae.

Keywords

References

  1. van der Does HC, Rep M. Adaptation to the host environment by plant-pathogenic fungi. Ann Rev Phytopathol. 2017;55(1):427-450. https://doi.org/10.1146/annurev-phyto-080516-035551
  2. Kulkarni RD, Thon MR, Pan H, et al. Novel Gprotein-coupled receptor-like proteins in the plant pathogenic fungus Magnaporthe grisea. Genome Biol. 2005;6(3):R24. https://doi.org/10.1186/gb-2005-6-3-r24
  3. Taylor BL, Zhulin IB. PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol Mol Biol Rev. 1999;63(2):479-506. https://doi.org/10.1128/mmbr.63.2.479-506.1999
  4. Vreede J, van der Horst MA, Hellingwerf KJ, et al. PAS domains. Common structure and common flexibility. J Biol Chem. 2003;278(20):18434-18439. https://doi.org/10.1074/jbc.M301701200
  5. Rojas-Pirela M, Rigden DJ, Michels PA, et al. Structure and function of per-ARNT-sim domains and their possible role in the life-cycle biology of Trypanosoma cruzi. Mol Biochem Parasitol. 2018;219:52-66. https://doi.org/10.1016/j.molbiopara.2017.11.002
  6. Gilles-Gonzalez M, Gonzalez G. Signal transduction by heme-containing PAS-domain proteins. J Appl Physiol. 2004;96(2):774-783. https://doi.org/10.1152/japplphysiol.00941.2003
  7. Herivaux A, So YS, Gastebois A, et al. Major sensing proteins in pathogenic fungi: the hybrid histidine kinase family. PLoS Pathog. 2016;12:e1005683. https://doi.org/10.1371/journal.ppat.1005683
  8. Moglich A, Ayers RA, Moffat K. Structure and signaling mechanism of Per-ARNT-Sim domains. Structure. 2009;17(10):1282-1294. https://doi.org/10.1016/j.str.2009.08.011
  9. Grose JH, Smith TL, Sabic H, et al. Yeast PAS kinase coordinates glucose partitioning in response to metabolic and cell integrity signaling. EMBO J. 2007;26(23):4824-4830. https://doi.org/10.1038/sj.emboj.7601914
  10. Huang M, Xu Q, Mitsui K, et al. PSK1 regulates expression of SOD1 involved in oxidative stress tolerance in yeast. FEMS Microbiol Lett. 2014;350(2):154-160. https://doi.org/10.1111/1574-6968.12329
  11. Barba-Ostria C, Lledias F, Georgellis D. The Neurospora crassa DCC-1 protein, a putative histidine kinase, is required for normal sexual and asexual development and carotenogenesis. Eukaryot Cell. 2011;10(12):1733-1739. https://doi.org/10.1128/EC.05223-11
  12. Purschwitz J, Muller S, Kastner C, et al. Functional and physical interaction of blue- and red-light sensors in Aspergillus nidulans. Curr Biol. 2008;18(4):255-259. https://doi.org/10.1016/j.cub.2008.01.061
  13. Dean RA, Talbot NJ, Ebbole DJ, et al. The genome sequence of the rice blast fungus Magnaporthe grisea. Nature. 2005;434(7036):980-986. https://doi.org/10.1038/nature03449
  14. Kang SH, Khang CH, Lee YG. Regulation of cAMP-dependent protein kinase during appressorium formation in Magnaporthe grisea. FEMS Microbiol Lett. 1999;170(2):419-423. https://doi.org/10.1016/S0378-1097(98)00576-X
  15. Lee YH, Dean RA. Hydrophobicity of contact surface induces appressorium formation in Magnaporthe grisea. FEMS Microbiol Lett. 1994;115(1):71-75. https://doi.org/10.1016/0378-1097(94)90463-4
  16. Liu W, Zhou X, Li G, et al. Multiple plant surface signals are sensed by different mechanisms in the rice blast fungus for appressorium formation. PLoS Pathog. 2011;7(1):e1001261. https://doi.org/10.1371/journal.ppat.1001261
  17. Wilson RA, Talbot NJ. Under pressure: investigating the biology of plant infection by Magnaporthe oryzae. Nat Rev Microbiol. 2009;7(3):185-195. https://doi.org/10.1038/nrmicro2032
  18. Jacob S, Foster AJ, Yemelin A, et al. Histidine kinases mediate differentiation, stress response, and pathogenicity in Magnaporthe oryzae. Microbiologyopen. 2014;3(5):668-687. https://doi.org/10.1002/mbo3.197
  19. Kim KS, Lee YH. Gene expression profiling during condiation in the rice blast pathogen Magnaporthe oryzae. PLoS One. 2012;7(8):e43202. https://doi.org/10.1371/journal.pone.0043202
  20. Tamura K, Peterson D, Peterson N, et al. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011;28(10):2731-2739. https://doi.org/10.1093/molbev/msr121
  21. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994;22(22):4673-4680. https://doi.org/10.1093/nar/22.22.4673
  22. Mulder NJ, Apweiler R, Attwood TK, et al. InterPro, progress and status in 2005. Nucleic Acids Res. 2004;33(Database issue):D201-205. https://doi.org/10.1093/nar/gki106
  23. Yu JH, Hamari Z, Han KH, et al. Double-joint PCR: a PCR-based molecular tool for gene manipulations in filamentous fungi. Fungal Genet Biol. 2004;41(11):973-981. https://doi.org/10.1016/j.fgb.2004.08.001
  24. Sweigard JA, Chumley FG, Valent B. Cloning and analysis of CUT1, a cutinase gene from Magnaporthe grisea. Mol Gen Genet. 1992;232(2):174-182. https://doi.org/10.1007/BF00279994
  25. Han JH, Lee HM, Shin JH, et al. Role of the MoYAK1 protein kinase gene in Magnaporthe oryzae development and pathogenicity. Environ Microbiol. 2015;17(11):4672-4689. https://doi.org/10.1111/1462-2920.13010
  26. Sambrook J, Fritsch EF, Maniatis T. Molecular cloning: a laboratory manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 1989.
  27. Fu T, Kim JO, Han JH, et al. A small GTPase RHO2 plays an important role in pre-infection development in the rice blast pathogen Magnaporthe oryzae. Plant Pathol J. 2018;34(6):470. https://doi.org/10.5423/PPJ.OA.04.2018.0069
  28. Park J, Kong S, Kim S, et al. Roles of forkheadbox transcription factors in controlling development, pathogenicity, and stress response in Magnaporthe oryzae. Plant Pathol J. 2014;30(2):136-150. https://doi.org/10.5423/PPJ.OA.02.2014.0018
  29. Bayry J, Aimanianda V, Guijarro JI, et al. Hydrophobins-unique fungal proteins. PLoS Pathog. 2012;8(5):e1002700. https://doi.org/10.1371/journal.ppat.1002700
  30. Li D, Agrellos OA, Calderone R. Histidine kinases keep fungi safe and vigorous. Curr Opin Microbiol. 2010;13(4):424-430. https://doi.org/10.1016/j.mib.2010.04.007
  31. Li X, Zhong K, Yin Z, et al. The seven transmembrane domain protein MoRgs7 functions in surface perception and undergoes coronin MoCrn1-dependent endocytosis in complex with Ga subunit MoMagA to promote cAMP signaling and appressorium formation in Magnaporthe oryzae. PLoS Pathog. 2019;15(2):e1007382. https://doi.org/10.1371/journal.ppat.1007382
  32. Xu X, Li G, Li L, et al. Genome-wide comparative analysis of putative Pth11-related G proteincoupled receptors in fungi belonging to Pezizomycotina. BMC Microbiol. 2017;17(1):166. https://doi.org/10.1186/s12866-017-1076-5
  33. Sabnam N, Roy Barman S. WISH, a novel CFEM GPCR is indispensable for surface sensing, asexual and pathogenic differentiation in rice blast fungus. Fungal Genet Biol. 2017;105:37-51. https://doi.org/10.1016/j.fgb.2017.05.006
  34. Lee YH, Dean RA. cAMP regulates infection structure formation in the plant pathogenic fungus Magnaporthe grisea. Plant Cell. 1993;5(6):693-700. https://doi.org/10.1105/tpc.5.6.693
  35. Kim S, Ahn IP, Rho HS, et al. MHP1, a Magnaporthe grisea hydrophobin gene, is required for fungal development and plant colonization. Mol Microbiol. 2005;57(5):1224-1237. https://doi.org/10.1111/j.1365-2958.2005.04750.x

Cited by

  1. Red light‐regulated interaction of Per‐Arnt‐Sim histidine kinases with partner histidine‐containing phosphotransfer proteins in Physcomitrium patens vol.26, pp.9, 2021, https://doi.org/10.1111/gtc.12878