#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

A fungal ABC transporter FgAtm1 regulates iron homeostasis via the transcription factor cascade FgAreA-HapX


Autoři: Zhihui Wang aff001;  Tianling Ma aff001;  Yunyan Huang aff001;  Jing Wang aff001;  Yun Chen aff001;  H. Corby Kistler aff003;  Zhonghua Ma aff001;  Yanni Yin aff001
Působiště autorů: State Key Laboratory of Rice Biology, Zhejiang University, Hangzhou, China aff001;  Institute of Biotechnology, Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Zhejiang University, Hangzhou, China aff002;  United States Department of Agriculture, Agricultural Research Service, St. Paul, Minnesota, United States of America aff003
Vyšlo v časopise: A fungal ABC transporter FgAtm1 regulates iron homeostasis via the transcription factor cascade FgAreA-HapX. PLoS Pathog 15(9): e32767. doi:10.1371/journal.ppat.1007791
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.ppat.1007791

Souhrn

Iron homeostasis is important for growth, reproduction and other metabolic processes in all eukaryotes. However, the functions of ATP-binding cassette (ABC) transporters in iron homeostasis are largely unknown. Here, we found that one ABC transporter (named FgAtm1) is involved in regulating iron homeostasis, by screening sensitivity to iron stress for 60 ABC transporter mutants of Fusarium graminearum, a devastating fungal pathogen of small grain cereal crops worldwide. The lack of FgAtm1 reduces the activity of cytosolic Fe-S proteins nitrite reductase and xanthine dehydrogenase, which causes high expression of FgHapX via activating transcription factor FgAreA. FgHapX represses transcription of genes for iron-consuming proteins directly but activates genes for iron acquisition proteins by suppressing another iron regulator FgSreA. In addition, the transcriptional activity of FgHapX is regulated by the monothiol glutaredoxin FgGrx4. Furthermore, the phosphorylation of FgHapX, mediated by the Ser/Thr kinase FgYak1, is required for its functions in iron homeostasis. Taken together, this study uncovers a novel regulatory mechanism of iron homeostasis mediated by an ABC transporter in an important pathogenic fungus.

Klíčová slova:

DNA transcription – Fluorescence microscopy – Homeostasis – Mitochondria – Phosphorylation – Saccharomyces cerevisiae – Transcription factors – Transcriptional control


Zdroje

1. Aisen P, Enns C, Wessling-Resnick M. 2001. Chemistry and biology of eukaryotic iron metabolism. Int J Biochem Cell Biol 33: 940–959. https://doi.org/10.1016/S1357-2725(01)00063-2. 11470229

2. Kobayashi T, Nishizawa NK. 2012. Iron uptake, translocation, and regulation in higher plants. Annu Rev Plant Biol 63: 131–152. doi: 10.1146/annurev-arplant-042811-105522 22404471

3. Philpott CC, Ryu MS. 2014. Special delivery: distributing iron in the cytosol of mammalian cells. Front Pharmacol 5: 173. doi: 10.3389/fphar.2014.00173 25101000

4. Huma N, Salim UrR, Anjum FM, Murtaza MA, Sheikh MA. 2007. Food fortification strategy-preventing iron deficiency anemia: a review. Crit Rev Food Sci Nutr 47: 259–265. doi: 10.1080/10408390600698262 17453923

5. Zimmermann MB, Hurrell RF 2007. Nutritional iron deficiency. The Lancet 370: 511–520. https://doi.org/10.1016/S0140-6736(07)61235-5.

6. Oide S, Moeder W, Krasnoff S, Gibson D, Haas H, Yoshioka K, Turgeon BG. 2006. NPS6, encoding a nonribosomal peptide synthetase involved in siderophore-mediated iron metabolism, is a conserved virulence determinant of plant pathogenic ascomycetes. Plant Cell 18: 2836–2853. doi: 10.1105/tpc.106.045633 17056706

7. Schrettl M, Bignell E, Kragl C, Joechl C, Rogers T, Arst HN, Haynes K, Haas H. 2004. Siderophore biosynthesis but not reductive iron assimilation is essential for Aspergillus fumigatus virulence. J Exp Med 200: 1213–1219. doi: 10.1084/jem.20041242 15504822

8. Ehrensberger KM, Bird AJ. 2011. Hammering out details: regulating metal levels in eukaryotes. Trends Biochem Sci 36: 524–531. doi: 10.1016/j.tibs.2011.07.002 21840721

9. Ganz T, Nemeth E. 2011. Hepcidin and disorders of iron metabolism. Annu Rev Med 62: 347–360. doi: 10.1146/annurev-med-050109-142444 20887198

10. Hentze MW, Muckenthaler MU, Galy B, Camaschella C. 2010. Two to tango: regulation of Mammalian iron metabolism. Cell 142: 24–38. doi: 10.1016/j.cell.2010.06.028 20603012

11. Del Sorbo G, Schoonbeek Hj, De Waard MA. 2000. Fungal transporters involved in efflux of natural toxic compounds and fungicides. Fungal Genet Biol 30: 1–15. https://doi.org/10.1006/fgbi.2000.1206. 10955904

12. Klein C, Kuchler K, Valachovic M. 2011. ABC proteins in yeast and fungal pathogens. Essays Biochem 50: 101–119. doi: 10.1042/bse0500101 21967054

13. Perlin MH, Andrews J, Toh SS. 2014. Essential letters in the fungal alphabet: ABC and MFS transporters and their roles in survival and pathogenicity. Adv Genet 85: 201–253. doi: 10.1016/B978-0-12-800271-1.00004-4 24880736

14. Khandelwal NK, Kaemmer P, Forster TM, Singh A, Coste AT, Andes DR, Hube B, Sanglard D, Chauhan N, Kaur R, d'Enfert C, Mondal AK, Prasad R. 2016. Pleiotropic effects of the vacuolar ABC transporter MLT1 of Candida albicans on cell function and virulence. Biochem J 473: 1537–1552. doi: 10.1042/BCJ20160024 27026051

15. Desideri E, Filomeni G, Ciriolo MR. 2012. Glutathione participates in the modulation of starvation-induced autophagy in carcinoma cells. Autophagy 8: 1769–1781. doi: 10.4161/auto.22037 22964495

16. Ding R, Jin S, Pabon K, Scotto KW. 2016. A role for ABCG2 beyond drug transport: Regulation of autophagy. Autophagy 12: 737–751. doi: 10.1080/15548627.2016.1155009 26983466

17. Huang H, Lu-Bo Y, Haddad GG. 2014. A Drosophila ABC transporter regulates lifespan. PLoS Genet 10: e1004844. doi: 10.1371/journal.pgen.1004844 25474322

18. Hwang JU, Song WY, Hong D, Ko D, Yamaoka Y, Jang S, Yim S, Lee E, Khare D, Kim K, Palmgren M, Yoon HS, Martinoia E, Lee Y. 2016. Plant ABC transporters enable many unique aspects of a terrestrial plant's lifestyle. Mol. Plant 9: 338–355. doi: 10.1016/j.molp.2016.02.003 26902186

19. Li J, Cowan JA. 2015. Glutathione-coordinated [2Fe-2S] cluster: a viable physiological substrate for mitochondrial ABCB7 transport. Chem Commun 51: 2253–2255. https://doi.org/10.1039/C4CC09175B.

20. Qi W, Li J, Cowan JA. 2014. A structural model for glutathione-complexed iron-sulfur cluster as a substrate for ABCB7-type transporters. Chem Commun 50: 3795–3798. https://doi.org/10.1039/C3CC48239A.

21. Young L, Leonhard K, Tatsuta T, Trowsdale J, Langer T. 2001. Role of the ABC transporter Mdl1 in peptide export from mitochondria. Science 291: 2135–2138. doi: 10.1126/science.1056957 11251115

22. Chloupková M, LeBard LS, Koeller DM. 2003. MDL1 is a high copy suppressor of ATM1: evidence for a role in resistance to oxidative stress. J Mol Biol 331: 155–165. doi: 10.1016/s0022-2836(03)00666-1 12875842

23. Zwiers LH, Roohparvar R, de Waard MA. 2007. MgAtr7, a new type of ABC transporter from Mycosphaerella graminicola involved in iron homeostasis. Fungal Genet Biol 44: 853–863. doi: 10.1016/j.fgb.2007.02.001 17379549

24. Bekri S, Kispal G, Lange H, Fitzsimons E, Tolmie J, Lill R, Bishop DF. 2000. Human ABC7 transporter: gene structure and mutation causing X-linked sideroblastic anemia with ataxia with disruption of cytosolic iron-sulfur protein maturation. Blood 96: 3256–3264. 11050011

25. Bernard DG, Cheng Y, Zhao Y, Balk J. 2009. An allelic mutant series of ATM3 reveals its key role in the biogenesis of cytosolic iron-sulfur proteins in Arabidopsis. Plant Physiol 151: 590–602. doi: 10.1104/pp.109.143651 19710232

26. Kispal G, Csere P, Prohl C, Lill R. 1999. The mitochondrial proteins Atm1p and Nfs1p are essential for biogenesis of cytosolic Fe/S proteins. EMBO J 18: 3981–3989. doi: 10.1093/emboj/18.14.3981 10406803

27. Kumanovics A, Chen OS, Li L, Bagley D, Adkins EM, Lin H, Dingra NN, Outten CE, Keller G, Winge D, Ward D, Kaplan J. 2008. Identification of FRA1 and FRA2 as genes involved in regulating the yeast iron regulon in response to decreased mitochondrial iron-sulfur cluster synthesis. J Biol Chem 283: 10276–10286. doi: 10.1074/jbc.M801160200 18281282

28. Li H, Mapolelo DT, Dingra NN, Keller G, Riggs-Gelasco PJ, Winge DR, Johnson MK, Outten CE. 2011. Histidine 103 in Fra2 is an iron-sulfur cluster ligand in the [2Fe-2S] Fra2-Grx3 complex and is required for in vivo iron signaling in yeast. J Biol Chem 286: 867–876. doi: 10.1074/jbc.M110.184176 20978135

29. Li H, Mapolelo DT, Dingra NN, Naik SG, Lees NS, Hoffman BM, Riggs-Gelasco PJ, Huynh BH, Johnson MK, Outten CE. 2009. The yeast iron regulatory proteins Grx3/4 and Fra2 form heterodimeric complexes containing a [2Fe-2S] cluster with cysteinyl and histidyl ligation. Biochemistry 48: 9569–9581. doi: 10.1021/bi901182w 19715344

30. Ueta R, Fujiwara N, Iwai K, Yamaguchi-Iwai Y. 2012. Iron-induced dissociation of the Aft1p transcriptional regulator from target gene promoters is an initial event in iron-dependent gene suppression. Mol Cell Biol 32: 4998–5008. doi: 10.1128/MCB.00726-12 23045394

31. Mühlenhoff U, Molik S, Godoy JR, Uzarska MA, Richter N, Seubert A, Zhang Y, Stubbe J, Pierrel F, Herrero E, Lillig CH, Lill R. 2010. Cytosolic monothiol glutaredoxins function in intracellular iron sensing and trafficking via their bound iron-sulfur cluster. Cell metab 12: 373–385. https://doi.org/10.1016/j.cmet.2010.08.001.

32. Goswami RS, Kistler HC. 2004. Heading for disaster: Fusarium graminearum on cereal crops. Mol Plant Pathol 5: 515–525. doi: 10.1111/j.1364-3703.2004.00252.x 20565626

33. Pestka JJ, Smolinski AT. 2005 Deoxynivalenol: toxicology and potential effects on humans. J Toxicol Env Heal B 8: 39–69. https://doi.org/10.1080/10937400590889458.

34. Kovalchuk A, Driessen AJ. 2010. Phylogenetic analysis of fungal ABC transporters. BMC genomics 11: 177. doi: 10.1186/1471-2164-11-177 20233411

35. Yin Y, Wang Z, Cheng D, Chen X, Chen Y, Ma Z. 2018. The ATP-binding protein FgArb1 is essential for penetration, infectious and normal growth of Fusarium graminearum. New Phytol 219: 1447–1466. doi: 10.1111/nph.15261 29932228

36. Gardiner DM, Osborne S, Kazan K, Manners JM. 2009. Low pH regulates the production of deoxynivalenol by Fusarium graminearum. Microbiology 155: 3149–3156. doi: 10.1099/mic.0.029546-0 19497949

37. Regev-Rudzki N, Battat E, Goldberg I, Pines O. 2009. Dual localization of fumarase is dependent on the integrity of the glyoxylate shunt. Mol Microbiol 72: 297–306. doi: 10.1111/j.1365-2958.2009.06659.x 19415796

38. Regev-Rudzki N, Karniely S, Ben-Haim NN, Pines O. 2005. Yeast aconitase in two locations and two metabolic pathways: seeing small amounts is believing. Mol Biol Cell 16: 4163–4171. doi: 10.1091/mbc.E04-11-1028 15975908

39. Lill R, Muhlenhoff U. 2005. Iron-sulfur-protein biogenesis in eukaryotes. Trends Biochem Sci 30: 133–141. doi: 10.1016/j.tibs.2005.01.006 15752985

40. Takaya N. 2009. Response to hypoxia, reduction of electron acceptors, and subsequent survival by filamentous fungi. Biosci Biotechnol Biochem 73: 1–8. doi: 10.1271/bbb.80487 19129650

41. Kispal G, Csere P, Guiard B, Lill R. 1997. The ABC transporter Atm1p is required for mitochondrial iron homeostasis. FEBS Letters 418: 346–50. doi: 10.1016/s0014-5793(97)01414-2 9428742

42. Frey PA, Hegeman AD, Ruzicka FJ. 2008. The radical SAM superfamily. Crit Rev Biochem Mol 43: 63–88. https://doi.org/10.1080/10409230701829169.

43. Mulliez E, Duarte V, Arragain S, Fontecave M, Atta M. 2017. On the role of additional [4Fe-4S] clusters with a free coordination site in radical-SAM enzymes. Front Chem 5: 17. doi: 10.3389/fchem.2017.00017 28361051

44. Berger H, Basheer A, Bock S, Reyes-Dominguez Y, Dalik T, Altmann F, Strauss J. 2008. Dissecting individual steps of nitrogen transcription factor cooperation in the Aspergillus nidulans nitrate cluster. Mol Microbiol 69: 1385–1398. doi: 10.1111/j.1365-2958.2008.06359.x 18673441

45. Giese H, Sondergaard TE, Sorensen JL. 2013. The AreA transcription factor in Fusarium graminearum regulates the use of some nonpreferred nitrogen sources and secondary metabolite production. Fungal Biol 117: 814–821. doi: 10.1016/j.funbio.2013.10.006 24295920

46. Lopez-Berges MS, Rispail N, Prados-Rosales RC, Di Pietro A. 2010. A nitrogen response pathway regulates virulence functions in Fusarium oxysporum via the protein kinase TOR and the bZIP protein MeaB. Plant Cell 22: 2459–2475. doi: 10.1105/tpc.110.075937 20639450

47. Lopez-Berges MS, Schafer K, Hera C, Di Pietro A. 2014. Combinatorial function of velvet and AreA in transcriptional regulation of nitrate utilization and secondary metabolism. Fungal Genet Biol 62: 78–84. doi: 10.1016/j.fgb.2013.11.002 24240057

48. Hesberg C, Hansch R, Mendel RR, Bittner F. 2004. Tandem orientation of duplicated xanthine dehydrogenase genes from Arabidopsis thaliana: differential gene expression and enzyme activities. J Biol Chem 279: 13547–13554. doi: 10.1074/jbc.M312929200 14726515

49. Hortschansky P, Eisendle M, Al-Abdallah Q, Schmidt AD, Bergmann S, Thon M, Kniemeyer O, Abt B, Seeber B, Werner ER, Kato M, Brakhage AA, Haas H. 2007. Interaction of HapX with the CCAAT-binding complex–a novel mechanism of gene regulation by iron. EMBO J 26: 3157–3168. doi: 10.1038/sj.emboj.7601752 17568774

50. Schrettl M, Beckmann N, Varga J, Heinekamp T, Jacobsen ID, Jochl C, Moussa TA, Wang S, Gsaller F, Blatzer M, Werner ER, Niermann WC, Brakhage AA, Haas H. 2010. HapX-mediated adaption to iron starvation is crucial for virulence of Aspergillus fumigatus. PLoS Pathog 6: e1001124. doi: 10.1371/journal.ppat.1001124 20941352

51. Schrettl M, Kim HS, Eisendle M, Kragl C, Nierman WC, Heinekamp T, Werner ER, Jacobsen I, Illmer P, Yi H, Brakhage AA, Haas H. 2008. SreA-mediated iron regulation in Aspergillus fumigatus. Mol Microbiol 70:27–43. doi: 10.1111/j.1365-2958.2008.06376.x 18721228

52. Pujol-Carrion N, Belli G, Herrero E, Nogues A, de la Torre-Ruiz MA. 2006. Glutaredoxins Grx3 and Grx4 regulate nuclear localisation of Aft1 and the oxidative stress response in Saccharomyces cerevisiae. J Cell Sci 119:4554–64. doi: 10.1242/jcs.03229 17074835

53. Ojeda L, Keller G, Muhlenhoff U, Rutherford JC, Lill R, Winge DR. 2006. Role of glutaredoxin-3 and glutaredoxin-4 in the iron regulation of the Aft1 transcriptional activator in Saccharomyces cerevisiae. J Biol Chem 281: 17661–17669. doi: 10.1074/jbc.M602165200 16648636

54. Tudzynski B. 2014. Nitrogen regulation of fungal secondary metabolism in fungi. Front Microbiol 5: 656. doi: 10.3389/fmicb.2014.00656 25506342

55. Todd RB, Fraser JA, Wong KH, Davis MA, Hynes MJ. 2005. Nuclear accumulation of the GATA factor AreA in response to complete nitrogen starvation by regulation of nuclear export. Eukaryot Cell 4: 1646–1653. doi: 10.1128/EC.4.10.1646-1653.2005 16215172

56. Min K, Shin Y, Son H, Lee J, Kim JC, Choi GJ, Lee YW. 2012. Functional analyses of the nitrogen regulatory gene areA in Gibberella zeae. FEMS Microbiol Lett 334: 66–73. doi: 10.1111/j.1574-6968.2012.02620.x 22702217

57. Hou R, Jiang C, Zheng Q, Wang C, Xu JR. 2015. The AreA transcription factor mediates the regulation of deoxynivalenol (DON) synthesis by ammonium and cyclic adenosine monophosphate (cAMP) signalling in Fusarium graminearum. Mol Plant Pathol 16: 987–999. doi: 10.1111/mpp.12254 25781642

58. Michielse CB, Pfannmuller A, Macios M, Rengers P, Dzikowska A, Tudzynski B. 2014. The interplay between the GATA transcription factors AreA, the global nitrogen regulator and AreB in Fusarium fujikuroi. Mol Microbiol 91: 472–493. doi: 10.1111/mmi.12472 24286256

59. Hortschansky P, Haas H, Huber EM, Groll M, Brakhage AA. 2017. The CCAAT-binding complex (CBC) in Aspergillus species. Biochim Biophys Acta 1860: 560–570. https://doi.org/10.1016/j.bbagrm.2016.11.008.

60. Lopez-Berges MS, Capilla J, Turra D, Schafferer L, Matthijs S, Jochl C, Cornelis P, Guarro J, Haas H, Di Pietro A. 2012. HapX-mediated iron homeostasis is essential for rhizosphere competence and virulence of the soilborne pathogen Fusarium oxysporum. Plant Cell 24: 3805–3822. doi: 10.1105/tpc.112.098624 22968717

61. Chen C, Pande K, French SD, Tuch BB, Noble SM. 2011. An iron homeostasis regulatory circuit with reciprocal roles in Candida albicans commensalism and pathogenesis. Cell Host Microbe 10: 118–135. doi: 10.1016/j.chom.2011.07.005 21843869

62. Schrettl M, Haas H. 2011. Iron homeostasis–Achilles' heel of Aspergillus fumigatus? Curr Opin Microbiol 14: 400–405. doi: 10.1016/j.mib.2011.06.002 21724450

63. Caza M, Hu G, Price M, Perfect JR, Kronstad JW. 2016. The Zinc Finger Protein Mig1 Regulates Mitochondrial Function and Azole Drug Susceptibility in the Pathogenic Fungus Cryptococcus neoformans. mSphere 1: e00080–15. https://doi.org/10.1128/mSphere.00080-15.

64. Jbel M, Mercier A, Labbe S. 2011. Grx4 monothiol glutaredoxin is required for iron limitation-dependent inhibition of Fep1. Eukaryot Cell 10: 629–645. doi: 10.1128/EC.00015-11 21421748

65. Kim KD, Kim HJ, Lee KC, Roe JH. 2011. Multi-domain CGFS-type glutaredoxin Grx4 regulates iron homeostasis via direct interaction with a repressor Fep1 in fission yeast. Biochem Bioph Res Co 408: 609–614. https://doi.org/10.1016/j.bbrc.2011.04.069.

66. Mercier A, Labbe S. 2009. Both Php4 function and subcellular localization are regulated by iron via a multistep mechanism involving the glutaredoxin Grx4 and the exportin Crm1. J Biol Chem 284: 20249–20262. doi: 10.1074/jbc.M109.009563 19502236

67. Li B, Jiang S, Yu X, Cheng C, Chen S, Cheng Y, Yuan JS, Jiang D, He P, Shan L. 2015. Phosphorylation of trihelix transcriptional repressor ASR3 by MAP KINASE4 negatively regulates Arabidopsis immunity. Plant Cell 27: 839–856. doi: 10.1105/tpc.114.134809 25770109

68. Webb AE, Brunet A. 2014. FOXO transcription factors: key regulators of cellular quality control. Trends Biochem Sci 39: 159–169. doi: 10.1016/j.tibs.2014.02.003 24630600

69. Ni W, Xu SL, Chalkley RJ, Pham TN, Guan S, Maltby DA, Burlingame AL, Wang ZY, Quail PH. 2013. Multisite light-induced phosphorylation of the transcription factor PIF3 is necessary for both its rapid degradation and concomitant negative feedback modulation of photoreceptor phyB levels in Arabidopsis. Plant Cell 25: 2679–2698. doi: 10.1105/tpc.113.112342 23903316

70. Brookheart RT, Lee CY, Espenshade PJ. 2014. Casein kinase 1 regulates sterol regulatory element-binding protein (SREBP) to control sterol homeostasis. J Biol Chem 289: 2725–2735. doi: 10.1074/jbc.M113.511899 24327658

71. Singh S, Katzer K, Lambert J, Cerri M, Parniske M. 2014. CYCLOPS, a DNA-binding transcriptional activator, orchestrates symbiotic root nodule development. Cell Host Microbe 15: 139–152. doi: 10.1016/j.chom.2014.01.011 24528861

72. Lee P, Cho BR, Joo HS, Hahn JS. 2008. Yeast Yak1 kinase, a bridge between PKA and stress-responsive transcription factors, Hsf1 and Msn2/Msn4. Mol Microbiol 70: 882–895. doi: 10.1111/j.1365-2958.2008.06450.x 18793336

73. Goyard S, Knechtle P, Chauvel M, Mallet A, Prevost MC, Proux C, Coppee JY, Schwarz P, Dromer F, Park H, Filler SG, Janbon G, d'Enfert C, 2008. The Yak1 kinase is involved in the initiation and maintenance of hyphal growth in Candida albicans. Mol Biol Cell 19: 2251–2266. doi: 10.1091/mbc.E07-09-0960 18321992

74. Teschner J, Lachmann N, Schulze J, Geisler M, Selbach K, Santamaria-Araujo J, Balk J, Mendel RR, Bittner F. 2010. A novel role for Arabidopsis mitochondrial ABC transporter ATM3 in molybdenum cofactor biosynthesis. Plant Cell 22:468–80. doi: 10.1105/tpc.109.068478 20164445

75. Miao R, Kim H, Koppolu UM, Ellis EA, Scott RA, Lindahl PA. 2009. Biophysical characterization of the iron in mitochondria from Atm1p-depleted Saccharomyces cerevisiae. Biochemistry 48: 9556–68. doi: 10.1021/bi901110n 19761223

76. Do E, Park S, Li MH, Wang JM, Ding C, Kronstad JW, Jung WH. 2017. The mitochondrial ABC transporter Atm1 plays a role in iron metabolism and virulence in the human fungal pathogen Cryptococcus neoformans. Med Mycol 56: 458–468. https://doi.org/10.1093/mmy/myx073.

77. Turrens JF. 1997. Superoxide production by the mitochondrial respiratory chain. Bioscience reports 17: 3–8. doi: 10.1023/a:1027374931887 9171915

78. Gu Q, Chen Y, Liu Y, Zhang C, Ma Z. 2015. The transmembrane protein FgSho1 regulates fungal development and pathogenicity via the MAPK module Ste50-Ste11-Ste7 in Fusarium graminearum. New Phytol 206: 315–328. doi: 10.1111/nph.13158 25388878

79. Zhang X, Chen X, Jiang J, Yu M, Yin Y, Ma Z. 2015. The tubulin cofactor A is involved in hyphal growth, conidiation and cold sensitivity in Fusarium asiaticum. BMC Microbiol 15: 35. doi: 10.1186/s12866-015-0374-z 25886735

80. Yu JH, Hamari Z, Han KH, Seo JA, Reyes-Domínguez Y, Scazzocchio C. 2004. Double-joint PCR: a PCR-based molecular tool for gene manipulations in filamentous fungi. Fungal Genet Biol 41: 973–981. doi: 10.1016/j.fgb.2004.08.001 15465386

81. Liu XH, Lu JP, Zhang L, Dong B, Min H, Lin FC. 2007. Involvement of a Magnaporthe grisea serine/threonine kinase gene, MgATG1, in appressorium turgor and pathogenesis. Eukaryot Cell 6: 997–1005. doi: 10.1128/EC.00011-07 17416896

82. Yu F, Gu Q, Yun Y, Yin Y, Xu JR, Shim WB, Ma Z. 2014. The TOR signaling pathway regulates vegetative development and virulence in Fusarium graminearum. New Phytol 203: 219–232. doi: 10.1111/nph.12776 24684168

83. Park G, Bruno KS, Staiger CJ, Talbot NJ, Xu JR. 2004. Independent genetic mechanisms mediate turgor generation and penetration peg formation during plant infection in the rice blast fungus. Mol Microbiol 53: 1695–1707. doi: 10.1111/j.1365-2958.2004.04220.x 15341648

84. Bruno KS, Tenjo F, Li L, Hamer JE, Xu JR. 2004. Cellular localization and role of kinase activity of PMK1 in Magnaporthe grisea. Eukaryot Cell 3: 1525–1532. doi: 10.1128/EC.3.6.1525-1532.2004 15590826

85. Riemer J, Hoepken HH, Czerwinska H, Robinson SR, Dringen R. 2004. Colorimetric ferrozine-based assay for the quantitation of iron in cultured cells. Anal Biochem 331: 370–375. doi: 10.1016/j.ab.2004.03.049 15265744

86. Machuca A, Milagres AMF. 2003. Use of CAS-agar plate modified to study the effect of different variables on the siderophore production by Aspergillus. Lett Appl Microbiol 36: 177–181. doi: 10.1046/j.1472-765x.2003.01290.x 12581379

87. Wang C, Zhang S, Hou R, Zhao Z, Zheng Q, Xu Q, Zheng D, Wang G, Liu H, Gao X, Ma JW, Kistler HC, Kang Z, Xu JR. 2011. Functional analysis of the kinome of the wheat scab fungus Fusarium graminearum. PLoS Pathog 7: e1002460. doi: 10.1371/journal.ppat.1002460 22216007

88. Hirayama T, Okuda K, Nagasawa H. 2013. A highly selective turn-on fluorescent probe for iron (II) to visualize labile iron in living cells. Chem Sci 4: 1250–1256. https://doi.org/10.1039/C2SC21649C.

89. Kamihara Y, Takada K, Sato T, Kawano Y, Murase K, Arihara Y, Kikuchi S, Hayasaka N, Usami M, Iyama S, Miyanishi K, Sato Y, Kobune M, Miyanishi K, Kato J. 2016. The iron chelator deferasirox induces apoptosis by targeting oncogenic Pyk2/β-catenin signaling in human multiple myeloma. Oncotarget 7: 64330–64341. doi: 10.18632/oncotarget.11830 27602957

90. Chaudhary K, Promsote W, Ananth S, Veeranan-Karmegam R, Tawfik A, Arjunan P, Martin P, Smith SB, Thangaraju M, Kisselev O, Ganapathy V, Gnana-Prakasam JP. 2018. Iron overload accelerates the progression of diabetic retinopathy in association with increased retinal renin expression. Sci Rep-UK 8: 3025. https://doi.org/10.1038/s41598-018-21276-2.

91. Smith M, Rimdeika A, Siow R, Naftalin R. 2018. Zinc attenuates UVA-dependent labile iron increase in human dermal fibroblasts: implications for skin ageing. Postgrad Med J 94: A7. http://dx.doi.org/10.1136/postgradmedj-2018-fpm.17.

92. Pierik AJ, Netz DJ, Lill R. 2009. Analysis of iron-sulfur protein maturation in eukaryotes. Nat Protoc 4: 753–766. doi: 10.1038/nprot.2009.39 19528951

93. Weerapana E, Wang C, Simon GM, Richter F, Khare S, Dillon MB, Bachovchin DA, Mowen K, Baker D, Cravatt BF. 2010. Quantitative reactivity profiling predicts functional cysteines in proteomes. Nature 468: 790–795. doi: 10.1038/nature09472 21085121

94. Nasmith CG, Walkowiak S, Wang L, Leung WW, Gong Y, Johnston A, Harris LJ, Guttman DS, Subramaniam R. 2011. Tri6 is a global transcription regulator in the phytopathogen Fusarium graminearum. PLoS Pathog 7: e1002266. doi: 10.1371/journal.ppat.1002266 21980289

95. Saleh A, Alvarez-Venegas R, Avramova Z. 2008. An efficient chromatin immunoprecipitation (ChIP) protocol for studying histone modifications in Arabidopsis plants. Nat Protoc 3: 1018–1025. doi: 10.1038/nprot.2008.66 18536649

96. Gu Q, Zhang C, Yu F, Yin Y, Shim WB, Ma Z. 2015. Protein kinase FgSch9 serves as a mediator of the target of rapamycin and high osmolarity glycerol pathways and regulates multiple stress responses and secondary metabolism in Fusarium graminearum. Environ Microbiol 17: 2661–2676. doi: 10.1111/1462-2920.12522 24903410

97. Liu Z, Wang Z, Huang M, Yan L, Ma Z, Yin Y. 2017. The FgSsb-FgZuo-FgSsz complex regulates multiple stress responses and mycotoxin production via folding the soluble SNARE Vam7 and beta2-tubulin in Fusarium graminearum. Environ Microbiol 19: 5040–5059. doi: 10.1111/1462-2920.13968 29076607

98. Carapito C, Klemm C, Aebersold R, Domon B. 2009. Systematic LC-MS analysis of labile post-translational modifications in complex mixtures. J Proteome Res 8: 2608–2614. doi: 10.1021/pr800871n 19284785

99. Jiao X, Sherman BT, Huang da W, Stephens R, Baseler MW, Lane HC, Lempicki RA. 2012. DAVID-WS: a stateful web service to facilitate gene/protein list analysis. Bioinformatics 28: 1805–1806. doi: 10.1093/bioinformatics/bts251 22543366

100. Wang W, Ye R, Xin Y, Fang X, Li C, Shi H, Zhou X, Qi Y. 2011. An importin beta protein negatively regulates MicroRNA activity in Arabidopsis. Plant Cell 23: 3565–3576. doi: 10.1105/tpc.111.091058 21984696

Štítky
Hygiena a epidemiologie Infekční lékařství Laboratoř

Článek vyšel v časopise

PLOS Pathogens


2019 Číslo 9
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autoři: MUDr. Tomáš Ürge, PhD.

Střevní příprava před kolonoskopií
Autoři: MUDr. Klára Kmochová, Ph.D.

Závislosti moderní doby – digitální závislosti a hypnotika
Autoři: MUDr. Vladimír Kmoch

Aktuální možnosti diagnostiky a léčby AML a MDS nízkého rizika
Autoři: MUDr. Natália Podstavková

Jak diagnostikovat a efektivně léčit CHOPN v roce 2024
Autoři: doc. MUDr. Vladimír Koblížek, Ph.D.

Všechny kurzy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#