Skip to main content

Advertisement

SpringerLink
Log in

Qualitative ubiquitome unveils the potential significances of protein lysine ubiquitination in hyphal growth of Aspergillus nidulans

  • Original Article
  • Published:
Current Genetics Aims and scope Submit manuscript

Abstract

Protein ubiquitination is an evolutionarily conserved post-translational modification process in eukaryotes, and it plays an important role in many biological processes. Aspergillus nidulans, a model filamentous fungus, contributes to our understanding of cellular physiology, metabolism and genetics, but its ubiquitination is not completely revealed. In this study, the ubiquitination sites in the proteome of A. nidulans were identified using a highly sensitive mass spectrometry combined with immuno-affinity enrichment of the ubiquitinated peptides. The 4816 ubiquitination sites were identified in 1913 ubiquitinated proteins, accounting for 18.1 % of total proteins in A. nidulans. Bioinformatic analysis suggested that the ubiquitinated proteins associated with a number of biological functions and displayed various sub-cellular localisations. Meanwhile, seven motifs were revealed from the ubiquitinated peptides, and significantly over-presented in the different pathways. Comparison of the enriched functional catalogues indicated that the ubiquitination functions divergently during growth of A. nidulans and Saccharomyces cerevisiae. Additionally, the proteins in A. nidulans-specific sub-category (cell growth/morphogenesis) were subjected to the protein interaction analysis which demonstrated that ubiquitination is involved in the comprehensive protein interactions. This study presents a first proteomic view of ubiquitination in the filamentous fungus, and provides an initial framework for exploring the physiological roles of ubiquitination in A. nidulans.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29:1165–1188

    Article  Google Scholar 

  • Berepiki A, Lichius A, Read ND (2011) Actin organization and dynamics in filamentous fungi. Nat Rev Microbiol 9:876–887

    Article  CAS  PubMed  Google Scholar 

  • Brown NA, dos Reis TF, Goinski AB, Savoldi M, Menino J, Almeida MT, Rodrigues F, Goldman GH (2014) The Aspergillus nidulans signalling mucin MsbA regulates starvation responses, adhesion and affects cellulase secretion in response to environmental cues. Mol Microbiol 94:1103–1120

    Article  CAS  Google Scholar 

  • Chen Z, Luo X, Lu Y, Zhu T, Wang J, Tsun A, Li B (2013) Ubiquitination signals critical to regulatory T cell development and function. Int Immunopharmacol 16:348–352

    Article  CAS  PubMed  Google Scholar 

  • Chinnici JL, Fu C, Caccamise LM, Arnold JW, Free SJ (2014) Neurospora crassa female development requires the PACC and other signal transduction pathways, transcription factors, chromatin remodeling, cell-to-cell fusion, and autophagy. PLoS One 9:e110603

    Article  PubMed Central  PubMed  Google Scholar 

  • Colabardini AC, Humanes AC, Gouvea PF, Savoldi M, Goldman MHS, von Zeska Kress MR, Bayram Ö, de Castro Oliveira JV, Gomes MD, Braus GH (2012) Molecular characterization of the Aspergillus nidulans fbxA encoding an F-box protein involved in xylanase induction. Fungal Genet Biol 49:130–140

    Article  CAS  PubMed  Google Scholar 

  • David H, Krogh AM, Roca C, Åkesson M, Nielsen J (2005) CreA influences the metabolic fluxes of Aspergillus nidulans during growth on glucose and xylose. Microbiology 151:2209–2221

    Article  CAS  PubMed  Google Scholar 

  • Dikic I, Robertson M (2012) Ubiquitin ligases and beyond. BMC Biol 10:22

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Galagan JE, Calvo SE, Cuomo C et al (2005) Sequencing of Aspergillus nidulans and comparative analysis with A. fumigates and A. oryzae. Nature 438:1105–1115

    Article  CAS  PubMed  Google Scholar 

  • Glickman MH, Ciechanover A (2002) The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 82:373–428

    Article  CAS  PubMed  Google Scholar 

  • Hapala I, Griač P, Nosek J, Sychrová H, Tomáška L (2013) Yeast membranes and cell wall: from basics to applications. Curr Genet 59:167–169

    Article  CAS  PubMed  Google Scholar 

  • Harris SD, Turner G, Meyer V, Espeso EA, Specht T, Takeshita N, Helmstedt K (2009) Morphology and development in Aspergillus nidulans: a complex puzzle. Fungal Genet Biol 46:S82–S92

    Article  CAS  PubMed  Google Scholar 

  • Herranz S, Rodriguez JM, Bussink HJ, Sanchez-Ferrero JC, Arst HN, Penalva MA, Vincent O (2005) Arrestin-related proteins mediate pH signaling in fungi. Proc Natl Acad Sci USA 102:12141–12146

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hervás-Aguilar A, Peñalva MA (2010) Endocytic machinery protein SlaB is dispensable for polarity establishment but necessary for polarity maintenance in hyphal tip cells of Aspergillus nidulans. Eukaryot Cell 10:1504–1518

    Article  Google Scholar 

  • Hervás-Aguilar A, Galindo A, Peñalva MA (2010) Receptor-independent ambient pH signaling by ubiquitin attachment to fungal arrestin-like PalF. J Biochem 285:18095–18102

    Google Scholar 

  • Karachaliou M, Amillis S, Evangelinos M, Kokotos AC, Yalelis V, Diallinas G (2013) The arrestin-like protein ArtA is essential for ubiquitination and endocytosis of the UapA transporter in response to both broad-range and specific signals. Mol Microbiol 88:301–317

    Article  CAS  PubMed  Google Scholar 

  • Lamoth F, Juvvadi PR, Fortwendel JR, Steinbach WJ (2012) Heat shock protein 90 is required for conidiation and cell wall integrity in Aspergillus fumigates. Eukaryot Cell 11:1324–1332

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Leach MD, Brown AJP (2012) Posttranslational modifications of proteins in the pathobiology of medically relevant fungi. Eukaryot Cell 11:98–108

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Leach MD, Stead DA, Argo E, Brown AJ (2011) Identification of sumoylation targets, combined with inactivation of SMT3, reveals the impact of sumoylation upon growth, morphology, and stress resistance in the pathogen Candida albicans. Mol Biol Cell 22:687–702

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ling Q, Jarvis P (2013) Dynamic regulation of endosymbiotic organelles by ubiquitination. Trends Cell Biol 23:399–408

    Article  CAS  PubMed  Google Scholar 

  • Lyzenga WJ, Stone SL (2012) Abiotic stress tolerance mediated by protein ubiquitination. J Exp Bot 63:599–616

    Article  CAS  PubMed  Google Scholar 

  • Mayer MP, Le Breton L (2015) Hsp90: breaking the symmetry. Mol Cell 58:8–20

    Article  CAS  PubMed  Google Scholar 

  • Noventa-Jordão MA, do Nascimento AM, Goldman MHS, Terenzi HF, Goldman GH (2000) Molecular characterization of ubiquitin genes from Aspergillus nidulans: mRNA expression on different stress and growth conditions. Biochim Biophys Acta 1490:237–244

    Article  PubMed  Google Scholar 

  • Osherov N, May G (2000) Conidial germination in Aspergillus nidulans requires RAS signaling and protein synthesis. Genetics 155:647–656

    PubMed Central  CAS  PubMed  Google Scholar 

  • Peng J, Schwartz D, Elias JE, Thoreen CC, Cheng D, Marsischky G, Roelofs J, Finley D, Gygi SP (2003) A proteomics approach to understanding protein ubiquitination. Nat Biotechnol 21:921–926

    Article  CAS  PubMed  Google Scholar 

  • Röhrig J, Kastner C, Fischer R (2013) Light inhibits spore germination through phytochrome in Aspergillus nidulans. Curr Genet 59:55–62

    Article  PubMed  Google Scholar 

  • Ronen R, Sharon H, Levdansky E, Romano J, Shadkchan Y, Osherov N (2007) The Aspergillus nidulans pkcA gene is involved in polarized growth, morphogenesis and maintenance of cell wall integrity. Curr Genet 51:321–329

    Article  CAS  PubMed  Google Scholar 

  • Ruepp A, Zollner A, Maier D, Albermann K, Hani J, Mokrejs M, Tetko I, Güldener U, Mannhaupt G, Münsterkötter M, Mewes HW (2004) The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res 32:5539–5545

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schnell JD, Hicke L (2003) Non-traditional functions of ubiquitin and ubiquitin-binding proteins. J Biol Chem 278:35857–35860

    Article  CAS  PubMed  Google Scholar 

  • Stavreva DA, Kawasaki M, Dundr M, Koberna K, Müller WG, Tsujimura-Takahashi T, Komatsu W, Hayano T, Isobe T, Raska I, Misteli T, Takahashi N, McNally JG (2006) Potential roles for ubiquitin and the proteasome during ribosome biogenesis. Mol Cell Biol 26:5131–5145

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tamayo D, Muñoz JF, Torres I, Almeida AJ, Restrepo A, McEwen JG, Hernández O (2013) Involvement of the 90 kDa heat shock protein during adaptation of Paracoccidioides brasiliensis to different environmental conditions. Fungal Genet Biol 51:34–41

    Article  CAS  PubMed  Google Scholar 

  • Teparić R, Mrsa V (2013) Proteins involved in building, maintaining and remodeling of yeast cell walls. Curr Genet 59:171–185

    Article  PubMed  Google Scholar 

  • Todd RB, Davis MA, Hynes MJ (2007) Genetic manipulation of Aspergillus nidulans: meiotic progeny for genetic analysis and strain construction. Nat Protoc 2:811–821

    Article  CAS  PubMed  Google Scholar 

  • Upadhyay S, Shaw BD (2008) The role of actin, fimbrin and endocytosis in growth of hyphae in Aspergillus nidulans. Mol Microbiol 68:690–705

    Article  CAS  PubMed  Google Scholar 

  • Veide VJ, Dahal S, Ljungdahl T, Grøtli M, Tamás MJ (2014) Application of a peptide-based assay to characterize inhibitors targeting protein kinases from yeast. Curr Genet 60:193–200

    Article  Google Scholar 

  • Virag A, Lee MP, Si H, Harris SD (2007) Regulation of hyphal morphogenesis by cdc42 and rac1 homologues in Aspergillus nidulans. Mol Microbiol 66:1579–1596

    CAS  PubMed  Google Scholar 

  • Vizcaíno JA, Deutsch EW, Wang R et al (2014) ProteomeXchange provides globally co-ordinated proteomics data submission and dissemination. Nat Biotechnol 30:223–226

    Article  Google Scholar 

  • Xie X, Kang H, Liu W, Wang GL (2015) Comprehensive profiling of the rice ubiquitome reveals the significance of lysine ubiquitination in young leaves. J Proteome Res 14:2017–2025

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We greatly appreciate Dr. Jianyi Pan (Zhejiang Sci-Tech University, Hangzhou, China) for his kind help with the data upload. This work was supported jointly by two Grants (31171898 and 31371990) from the National Natural Science Foundation of China.

Author information

Authors and Affiliations

  1. Institute of Microbiology, College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang, 310058, People’s Republic of China

    Xin-Ling Chu, Ming-Guang Feng & Sheng-Hua Ying

Authors
  1. Xin-Ling Chu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ming-Guang Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sheng-Hua Ying
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sheng-Hua Ying.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by M. Kupiec.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chu, XL., Feng, MG. & Ying, SH. Qualitative ubiquitome unveils the potential significances of protein lysine ubiquitination in hyphal growth of Aspergillus nidulans . Curr Genet 62, 191–201 (2016). https://doi.org/10.1007/s00294-015-0517-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00294-015-0517-7

Keywords

Search

Navigation