Aspergillus nidulans transcription factor AtfA interacts with the MAPK SakA to regulate general stress responses, development and spore functions

Abstract

Summary Fungi utilize a phosphorelay system coupled to a MAP kinase module for sensing and processing environmental signals. In Aspergillus nidulans , response regulator SskA transmits osmotic and oxidative stress signals to the stress MAPK (SAPK) SakA. Using a genetic approach together with GFP tagging and molecular bifluorescence we show that SakA and ATF/CREB transcription factor AtfA define a general stress‐signalling pathway that plays differential roles in oxidative stress responses during growth and development. AtfA is permanently localized in the nucleus, while SakA accumulates in the nucleus in response to oxidative or osmotic stress signals or during normal spore development, where it physically interacts with AtfA. AtfA is required for expression of several genes, the conidial accumulation of SakA and the viability of conidia. Furthermore, SakA is active (phosphorylated) in asexual spores, remaining phosphorylated in dormant conidia and becoming dephosphorylated during germination. SakA phosphorylation in spores depends on certain (SskA) but not other (SrrA and NikA) components of the phosphorelay system. Constitutive phosphorylation of SakA induced by the fungicide fludioxonil prevents both, germ tube formation and nuclear division. Similarly, Neurospora crassa SakA orthologue OS‐2 is phosphorylated in intact conidia and gets dephosphorylated during germination. We propose that SakA–AtfA interaction regulates gene expression during stress and conidiophore development and that SAPK phosphorylation is a conserved mechanism to regulate transitions between non‐growing (spore) and growing (mycelia) states.

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References 73

1. 1.

   Adams TH, Wieser JK, Yu JH. Asexual sporulation in Aspergillus nidulans. Microbiol Mol Biol Rev. 1998;62:35-54.

   Not in our library10.1128/mmbr.62.1.35-54.1998

2. 2.

   Aguirre J, Lambeth JD. Nox enzymes from fungus to fly to fish and what they tell us about Nox function in mammals. Free Radic Biol Med. 2010;49:1342-1353.

   Not in our library10.1016/j.freeradbiomed.2010.07.027

3. 3.

   Aguirre J, Rios-Momberg M, Hewitt D, Hansberg W. Reactive oxygen species and development in microbial eukaryotes. Trends Microbiol. 2005;13:111-118.

   Not in our library10.1016/j.tim.2005.01.007

4. 4.

   Aguirre J, Hansberg W, Navarro R. Fungal responses to reactive oxygen species. Med Mycol. 2006;44:S101-S107.

   Not in our library10.1080/13693780600900080

5. 5.

   Balazs A, Pocsi I, Hamari Z, Leiter E, Emri T, Miskei M, et al. AtfA bZIP-type transcription factor regulates oxidative and osmotic stress responses in Aspergillus nidulans. Mol Genet Genomics. 2010;283:289-303.

   Not in our library10.1007/s00438-010-0513-z

6. 6.

   Bergen LG, Morris NR. Kinetics of the nuclear division cycle of Aspergillus nidulans. J Bacteriol. 1983;156:155-160.

   Not in our library10.1128/jb.156.1.155-160.1983

7. 7.

   Brody H, Griffith J, Cuticchia AJ, Arnold J, Timberlake WE. Chromosome-specific recombinant DNA libraries from the fungus Aspergillus nidulans. Nucleic Acids Res. 1991;19:3105-3109.

   Not in our library10.1093/nar/19.11.3105

8. 8.

   Buck V, Quinn J, Pino TS, Martin H, Saldanha J, Makino K, et al. Peroxide sensors for the fission yeast stress-activated mitogen-activated protein kinase pathway. Mol Biol Cell. 2001;12:407-419.

   Not in our library10.1091/mbc.12.2.407

9. 9.

   Cano-Dominguez N, Alvarez-Delfin K, Hansberg W, Aguirre J. NADPH oxidases NOX-1 and NOX-2 require the regulatory subunit NOR-1 to control cell differentiation and growth in Neurospora crassa. Eukaryot Cell. 2008;7:1352-1361.

   Not in our library10.1128/ec.00137-08

10. 10.

    Chen D, Toone WM, Mata J, Lyne R, Burns G, Kivinen K, et al. Global transcriptional responses of fission yeast to environmental stress. Mol Biol Cell. 2003;14:214-229.

    Not in our library10.1091/mbc.e02-08-0499

11. 11.

    Chen D, Wilkinson CR, Watt S, Penkett CJ, Toone WM, Jones N, Bahler J. Multiple pathways differentially regulate global oxidative stress responses in fission yeast. Mol Biol Cell. 2008;19:308-317.

    Not in our library10.1091/mbc.e07-08-0735

12. 12.

    Clutterbuck AJ. A mutational analysis of conidial development in Aspergillus nidulans. Genetics. 1969;63:317-327.

    Not in our library10.1093/genetics/63.2.317

13. 13.

    Dayton JS, Sumi M, Nanthakumar NN, Means AR. Expression of a constitutively active Ca2+/calmodulin-dependent kinase in Aspergillus nidulans spores prevents germination and entry into the cell cycle. J Biol Chem. 1997;272:3223-3230.

    Not in our library10.1074/jbc.272.6.3223

14. 14.

    Eaton CJ, Jourdain I, Foster SJ, Hyams JS, Scott B. Functional analysis of a fungal endophyte stress-activated MAP kinase. Curr Genet. 2008;53:163-174.

    Not in our library10.1007/s00294-007-0174-6

15. 15.

    Flohe L, Otting F. Superoxide dismutase assays. Methods Enzymol. 1984;105:93-104.

    Not in our library10.1016/s0076-6879(84)05013-8

16. 16.

    Furukawa K, Hoshi Y, Maeda T, Nakajima T, Abe K. Aspergillus nidulans HOG pathway is activated only by two-component signalling pathway in response to osmotic stress. Mol Microbiol. 2005;56:1246-1261.

    Not in our library10.1111/j.1365-2958.2005.04605.x

17. 17.

    Gaits F, Russell P. Active nucleocytoplasmic shuttling required for function and regulation of stress-activated kinase Spc1/StyI in fission yeast. Mol Biol Cell. 1999;10:1395-1407.

    Not in our library10.1091/mbc.10.5.1395

18. 18.

    Gaits F, Degols G, Shiozaki K, Russell P. Phosphorylation and association with the transcription factor Atf1 regulate localization of Spc1/Sty1 stress-activated kinase in fission yeast. Genes Dev. 1998;12:1464-1473.

    Not in our library10.1101/gad.12.10.1464

19. 19.

    Galagan JE, Calvo SE, Cuomo C, Ma LJ, Wortman JR, Batzoglou S, et al. Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature. 2005;438:1105-1115.

    Not in our library10.1038/nature04341

20. 20.

    Hagiwara D, Asano Y, Yamashino T, Mizuno T. Characterization of bZip-type transcription factor AtfA with reference to stress responses of conidia of Aspergillus nidulans. Biosci Biotechnol Biochem. 2008;72:2756-2760.

    Not in our library10.1271/bbb.80001

21. 21.

    Hagiwara D, Asano Y, Marui J, Yoshimi A, Mizuno T, Abe K. Transcriptional profiling for Aspergillus nidulans HogA MAPK signaling pathway in response to fludioxonil and osmotic stress. Fungal Genet Biol. 2009;46:868-878.

    Not in our library10.1016/j.fgb.2009.07.003

22. 22.

    Han KH, Prade RA. Osmotic stress-coupled maintenance of polar growth in Aspergillus nidulans. Mol Microbiol. 2002;43:1065-1078.

    Not in our library10.1046/j.1365-2958.2002.02774.x

23. 23.

    Hansberg W, Aguirre J. Hyperoxidant states cause microbial cell differentiation by cell isolation from dioxygen. J Theor Biol. 1990;142:201-221.

    Not in our library10.1016/s0022-5193(05)80222-x

24. 24.

    Harris SD. Morphogenesis is coordinated with nuclear division in germinating Aspergillus nidulans conidiospores. Microbiology. 1999;145:2747-2756.

    Not in our library10.1099/00221287-145-10-2747

25. 25.

    Hartmuth S, Petersen J. Fission yeast Tor1 functions as part of TORC1 to control mitotic entry through the stress MAPK pathway following nutrient stress. J Cell Sci. 2009;122:1737-1746.

    Not in our library10.1242/jcs.049387

26. 26.

    Hill TW, Käfer E. Improved protocols for Aspergillus minimal medium: trace element and minimal medium stock solution. Fungal Genet Newsl. 2001;48:20-21.

    Not in our library

27. 27.

    Ikner A, Shiozaki K. Yeast signaling pathways in the oxidative stress response. Mutat Res. 2005;569:13-27.

    Not in our library10.1016/j.mrfmmm.2004.09.006

28. 28.

    Jones CA, Greer-Phillips SE, Borkovich KA. The response regulator RRG-1 functions upstream of a mitogen-activated protein kinase pathway impacting asexual development, female fertility, osmotic stress, and fungicide resistance in Neurospora crassa. Mol Biol Cell. 2007;18:2123-2136.

    Not in our library10.1091/mbc.e06-03-0226

29. 29.

    Kawasaki L, Aguirre J. Multiple catalase genes are differentially regulated in Aspergillus nidulans. J Bacteriol. 2001;183:1434-1440.

    Not in our library10.1128/jb.183.4.1434-1440.2001

30. 30.

    Kawasaki L, Wysong D, Diamond R, Aguirre J. Two divergent catalase genes are differentially regulated during Aspergillus nidulans development and oxidative stress. J Bacteriol. 1997;179:3284-3292.

    Not in our library10.1128/jb.179.10.3284-3292.1997

31. 31.

    Kawasaki L, Sanchez O, Shiozaki K, Aguirre J. SakA MAP kinase is involved in stress signal transduction, sexual development and spore viability in Aspergillus nidulans. Mol Microbiol. 2002;45:1153-1163.

    Not in our library10.1046/j.1365-2958.2002.03087.x

32. 32.

    Kojima K, Takano Y, Yoshimi A, Tanaka C, Kikuchi T, Okuno T. Fungicide activity through activation of a fungal signalling pathway. Mol Microbiol. 2004;53:1785-1796.

    Not in our library10.1111/j.1365-2958.2004.04244.x

33. 33.

    Lara-Ortiz T, Riveros-Rosas H, Aguirre J. Reactive oxygen species generated by microbial NADPH oxidase NoxA regulate sexual development in Aspergillus nidulans. Mol Microbiol. 2003;50:1241-1255.

    Not in our library10.1046/j.1365-2958.2003.03800.x

34. 34.

    Lee BN, Adams TH. FluG and flbA function interdependently to initiate conidiophore development in Aspergillus nidulans through brlA beta activation. EMBO J. 1996;15:299-309.

    Not in our library

35. 35.

    Lee BN, Kroken S, Chou DY, Robbertse B, Yoder OC, Turgeon BG. Functional analysis of all nonribosomal peptide synthetases in Cochliobolus heterostrophus reveals a factor, NPS6, involved in virulence and resistance to oxidative stress. Eukaryot Cell. 2005;4:545-555.

    Not in our library10.1128/ec.4.3.545-555.2005

36. 36.

    Marhoul J. Isolation and characterization of developmental regulatory genes. 1996;136.

    Not in our library

37. 37.

    Marquez-Fernandez O, Trigos A, Ramos-Balderas JL, Viniegra-Gonzalez G, Deising HB, Aguirre J. Phosphopantetheinyl transferase CfwA/NpgA is required for Aspergillus nidulans secondary metabolism and asexual development. Eukaryot Cell. 2007;6:710-720.

    Not in our library10.1128/ec.00362-06

38. 38.

    Munhoz DC, Netto LE. Cytosolic thioredoxin peroxidase I and II are important defenses of yeast against organic hydroperoxide insult: catalases and peroxiredoxins cooperate in the decomposition of H2O2 by yeast. J Biol Chem. 2004;279:35219-35227.

    Not in our library10.1074/jbc.m313773200

39. 39.
    CPTF1, a CREB-Like Transcription Factor, Is Involved in the Oxidative Stress Response in the Phytopathogen Claviceps purpurea and Modulates ROS Level in Its Host Secale cereale · 2004

    Not checked
40. 40.

    Navarro RE, Aguirre J. Posttranscriptional control mediates cell type-specific localization of catalase A during Aspergillus nidulans development. J Bacteriol. 1998;180:5733-5738.

    Not in our library10.1128/jb.180.21.5733-5738.1998

Cited by papers we hold 4

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• Oxidant-Sensing Pathways in the Responses of Fungal Pathogens to Chemical Stress Signals · 2019
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• Osmotic-Adaptation Response of sakA/hogA Gene to Aflatoxin Biosynthesis, Morphology Development and Pathogenicity in Aspergillus flavus · 2019
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• Oxidative Stress-Related Transcription Factors in the Regulation of Secondary Metabolism · 2013
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