Advertisement

Genome-wide identification and expression profile analysis of the HOG gene family in Aspergillus oryzae

  • Bin He
  • Yayi Tu
  • Zhihong Hu
  • Long Ma
  • Jing Dai
  • Xiaojie Cheng
  • Haoran Li
  • Lanlan Liu
  • Bin Zeng
Original Paper

Abstract

The High osmolarity glycerol (HOG) gene family plays crucial roles in various developmental and physiological processes in fungi, such as the permeability of cell membrane, chlamydospore formation and stress signaling. Although the function of HOG genes has been investigated in Saccharomyces cerevisiae and some filamentous fungi, a comprehensive analysis of HOG gene family has not been performed in Aspergillus oryzae, a fungi mainly used for the production of soy sauce. In this study, we identified and corrected a total of 90 HOG genes from the A. oryzae genome. According to the phylogenetic relationship, they were divided into four discrete groups (Group A–D) comprising of 16, 24, 30 and 20 proteins, respectively. Six conserved motifs and exon–intron structures were examined among all HOG proteins to reveal the diversity of AoHOG genes. Based on transcriptome technology, the expression patterns of AoHOG genes across all developmental stages was identified, suggesting that the AoHOG gene family mainly functions in the logarithmic phase of development. The expression profiles of AoHOG genes under different concentrations of salt stress indicated that AoHOG genes are extensively involved in salt stress response, with possibly different mechanisms. The genome-wide identification, evolutionary, gene structures and expression analyses of AoHOG genes provide a comprehensive overview of this gene family as well as their potential involvements in development and stress responses. Our results will facilitate further research on HOG gene family regarding their physiological and biochemical functions.

Keywords

HOG gene family Aspergillus oryzae Gene expression Salt stress response 

Notes

Acknowledgements

This study was funded by National Natural Science Foundation of China (NSFC) (Grant Nos. 31171731 and 31460447), International S&T Cooperation Project of Jiangxi Provincial (Grant No. 20142BDH80003), General Science and Technology Project of Nanchang City (Grant No. 3000035402), “555 Talent Project” of Jiangxi Province and Science, the Science Funds of Natural Science Foundation of Jiangxi Province (20114BAB205039) and Technology Research Project of Jiangxi Provincial Department of Education (Grant Nos. GJJ160765, GJJ160795 and GJJ160794).

Compliance with ethical standards

Conflict of interest

We declare that we have no conflict of interest.

Research involving animal and human rights

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

11274_2018_2419_MOESM1_ESM.xlsx (15 kb)
Expression profiles of AoHOG genes at different stages. (XLSX 15 KB)
11274_2018_2419_MOESM2_ESM.xlsx (13 kb)
Expression patterns of AoHOG genes under salt stresses (XLSX 12 KB)

References

  1. Altshuler I, Mcleod AM, Colbourne JK, Yan ND, Cristescu ME (2015) Synergistic interactions of biotic and abiotic environmental stressors on gene expression. Genome 58:99–109CrossRefGoogle Scholar
  2. Altwasser R, Baldin C, Weber J, Guthke R, Kniemeyer O, Brakhage AA, Linde J, Valiante V (2015) Network modeling reveals cross talk of MAP kinases during adaptation to caspofungin stress in Aspergillus fumigatus. PLoS ONE 10:e0136932CrossRefGoogle Scholar
  3. Babazadeh R, Furukawa T, Hohmann S, Furukawa K (2014) Rewiring yeast osmostress signalling through the MAPK network reveals essential and non-essential roles of Hog1 in osmoadaptation. Sci Rep 4:4697CrossRefGoogle Scholar
  4. Bon E, Casaregola S, Blandin G, Llorente B, Neuveglise C, Munsterkotter M, Guldener U, Mewes HW, Van Helden J, Dujon B, Gaillardin C (2003) Molecular evolution of eukaryotic genomes: hemiascomycetous yeast spliceosomal introns. Nucleic Acids Res 31:1121–1135CrossRefGoogle Scholar
  5. Bondarenko VS, Gelfand MS (2016) Evolution of the exon-intron structure in ciliate genomes. PLoS ONE 11:e0161476CrossRefGoogle Scholar
  6. Chen RE, Thorner J (2007) Function and regulation in MAPK signaling pathways: lessons learned from the yeast Saccharomyces cerevisiae. Biochim Biophys Acta 1773:1311–1340CrossRefGoogle Scholar
  7. Cheng XJ, He B, Chen L, Xiao SQ, Fu J, Chen Y, Yu TQ, Cheng ZQ, Feng H (2016) Transcriptome analysis confers a complex disease resistance network in wild rice Oryza meyeriana against Xanthomonas oryzae pv. oryzae. Sci Rep 6:38215CrossRefGoogle Scholar
  8. Eisman B, Alonsomonge R, Román E, Arana D, Nombela C, Pla J (2006) The Cek1 and Hog1 mitogen-activated protein kinases play complementary roles in cell wall biogenesis and chlamydospore formation in the fungal pathogen Candida albicans. Eukaryot Cell 5:347CrossRefGoogle Scholar
  9. Fedorova ND, Khaldi N, Joardar VS, Maiti R, Amedeo P, Anderson MJ, Crabtree J, Silva JC, Badger JH, Albarraq A, Angiuoli S, Bussey H, Bowyer P, Cotty PJ, Dyer PS, Egan A, Galens K, Fraser-Liggett CM, Haas BJ, Inman JM, Kent R, Lemieux S, Malavazi I, Orvis J, Roemer T, Ronning CM, Sundaram JP, Sutton G, Turner G, Venter JC, White OR, Whitty BR, Youngman P, Wolfe KH, Goldman GH, Wortman JR, Jiang B, Denning DW, Nierman WC (2008) Genomic islands in the pathogenic filamentous fungus Aspergillus fumigatus. PLoS Genet 4:e1000046CrossRefGoogle Scholar
  10. Fitzgibbon GJ, Morozov IY, Jones MG, Caddick MX (2005) Genetic analysis of the TOR pathway in Aspergillus nidulans. Eukaryot Cell 4:1595–1598CrossRefGoogle Scholar
  11. Furukawa K, Yoshimi A, Furukawa T, Hoshi Y, Hagiwara D, Sato N, Fujioka T, Mizutani O, Mizuno T, Kobayashi T, Abe K (2007) Novel reporter gene expression systems for monitoring activation of the Aspergillus nidulans HOG pathway. Biosci Biotechnol Biochem 71:1724–1730CrossRefGoogle Scholar
  12. Galagan JE, Calvo SE, Cuomo C, Ma LJ, Wortman JR, Batzoglou S, Lee SI, Baştürkmen M, Spevak CC, Clutterbuck J, Kapitonov V, Jurka J, Scazzocchio C, Farman M, Butler J, Purcell S, Harris S, Braus GH, Draht O, Busch S, D’Enfert C, Bouchier C, Goldman GH, Bell-Pedersen D, Griffiths-Jones S, Doonan JH, Yu J, Vienken K, Pain A, Freitag M, Selker EU, Archer DB, Peñalva MA, Oakley BR, Momany M, Tanaka T, Kumagai T, Asai K, Machida M, Nierman WC, Denning DW, Caddick M, Hynes M, Paoletti M, Fischer R, Miller B, Dyer P, Sachs MS, Osmani SA, Birren BW (2005) Sequencing of Aspergillus nidulans. and comparative analysis with A. fumigatus and A. oryzae. Nature 438:1105–1115CrossRefGoogle Scholar
  13. Gietz RD, Schiestl RH (2007) Quick and easy yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat Protoc 2:35–37CrossRefGoogle Scholar
  14. Hagiwara D, Suzuki S, Kamei K, Gonoi T, Kawamoto S (2014) The role of AtfA and HOG MAPK pathway in stress tolerance in conidia of Aspergillus fumigatus. Fungal Genet Biol 73:138–149CrossRefGoogle Scholar
  15. Hagiwara D, Sakamoto K, Abe K, Gomi K (2016) Signaling pathways for stress responses and adaptation in Aspergillus species: stress biology in the post-genomic era. Biosci Biotechnol Biochem 80:1–14CrossRefGoogle Scholar
  16. Han F, Pei H, Hu W, Zhang S, Han L, Ma G (2016) The feasibility of ultrasonic stimulation on microalgae for efficient lipid accumulation at the end of the logarithmic phase. Algal Res 16:189–194CrossRefGoogle Scholar
  17. He B, Gu YH, Tao X, Cheng XJ, Wei CH, Fu J, Cheng ZQ, Zhang YZ (2015) De novo transcriptome sequencing of Oryza officinalis Wall ex Watt to identify disease-resistance genes. Int J Mol Sci 16:29482–29495CrossRefGoogle Scholar
  18. He B, Ma L, Hu Z, Li H, Ai M, Long C, Zeng B (2017) Deep sequencing analysis of transcriptomes in Aspergillus oryzae in response to salinity stress. Appl Microbiol Biotechnol 1–2:1–10Google Scholar
  19. Hohmann S, Krantz M, Nordlander B (2007) Yeast osmoregulation. Method Enzymol 428:29CrossRefGoogle Scholar
  20. Ivashchenko AT, Tauasarova MI, Atambayeva SA (2009) Exon-intron structure of genes in complete fungal genomes. Mol Bio 43:24–31CrossRefGoogle Scholar
  21. Ji Y, Yang F, Ma D, Zhang J, Wan Z, Liu W, Li R (2012) HOG-MAPK signaling regulates the adaptive responses of Aspergillus fumigatus to thermal stress and other related stress. Mycopathologia 174:273–282CrossRefGoogle Scholar
  22. Kitamoto K (2015) Cell biology of the Koji mold Aspergillus oryzae. Biosci Biotechnol Biochem 79:1–7CrossRefGoogle Scholar
  23. Lee YH, Tominaga M, Hayashi R, Sakamoto K, Yamada O, Akita O (2006) Aspergillus oryzae strains with a large deletion of the aflatoxin biosynthetic homologous gene cluster differentiated by chromosomal breakage. Appl Microbiol Biotechnol 72:339–345CrossRefGoogle Scholar
  24. Lee YM, Kim E, An J, Lee Y, Choi E, Choi W, Moon E, Kim W (2016) Dissection of the HOG pathway activated by hydrogen peroxide in Saccharomyces cerevisiae. Environ Microbiol 19:584–597CrossRefGoogle Scholar
  25. Lenassi M, Vaupotic T, Gundecimerman N, Plemenitas A (2007) The MAP kinase HwHog1 from the halophilic black yeast Hortaea werneckii: coping with stresses in solar salterns. Aquat Biosyst 3:1–11Google Scholar
  26. Liu B (2013) Characterizing the contributions of individual components to the dynamic properties of the HOG pathway in S. cerevisiae. Princeton: Princeton UniversityGoogle Scholar
  27. Liu Q, Xue Q (2007) Computational identification and phylogenetic analysis of the MAPK gene family in Oryza sativa. Plant Physiol Biochem 45:6CrossRefGoogle Scholar
  28. Loftus BJ et al (2005) The genome of the Basidiomycetous Yeast and Human Pathogen. Cryptococcus Neoformans Sci 307:1321Google Scholar
  29. Machida M et al (2005) Genome sequencing and analysis of Aspergillus oryzae. Nature 438:1157–1161CrossRefGoogle Scholar
  30. Machida M, Yamada O, Gomi K (2008) Genomics of Aspergillus oryzae: learning from the history of Koji Mold and exploration of its future. DNA Res 15:173CrossRefGoogle Scholar
  31. Maeda H, Sano M, Maruyama Y, Tanno T, Akao T, Totsuka Y, Endo M, Sakurada R, Yamagata Y, Machida M, Akita O, Hasegawa F, Abe K, Gomi K, Nakajima T, Iguchi Y (2004) Transcriptional analysis of genes for energy catabolism and hydrolytic enzymes in the filamentous fungus Aspergillus oryzae using cDNA microarrays and expressed sequence tags. Appl Microbiol Biotechnol 65:74–83CrossRefGoogle Scholar
  32. Mcguire AM, Pearson MD, Neafsey DE, Galagan JE (2008) Cross-kingdom patterns of alternative splicing and splice recognition. Genome Biol 9:R50CrossRefGoogle Scholar
  33. Nakazawa J, Terada S, Yamada M, Hikichi S (2013) The HOG signal transduction pathway in the halophilic fungus Wallemia ichthyophaga: identification and characterisation of MAP kinases WiHog1A and WiHog1B Extremophiles. Life Under Extreme Conditions 17:623–636CrossRefGoogle Scholar
  34. Payne GA et al (2009) Whole genome comparison of Aspergillus flavus. and A. oryzae. Med Mycol 44:S9–S11CrossRefGoogle Scholar
  35. Posas F, WurglerMurphy SM, Maeda T, Witten EA, Thai TC, Saito H (1996) Yeast HOG1 MAP kinase cascade is regulated by a multistep phosphorelay mechanism in the SLN1-YPD1-SSK1 “two-component” osmosensor. Cell 86:865–875CrossRefGoogle Scholar
  36. Solé C, Nadalribelles M, Kraft C, Peter M, Posas F, Nadal ED (2011) Control of Ubp3 ubiquitin protease activity by the Hog1 SAPK modulates transcription upon osmostress. Embo J 30:3274–3284CrossRefGoogle Scholar
  37. Wang D, Zheng ZY, Feng J, Zhan XB, Zhang LM, Wu JR, Lin CC (2013) A high salt tolerant neutral protease from Aspergillus oryzae: purification, characterization and kinetic properties. Appl Biochem Microbiol 49:378–385CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  • Bin He
    • 1
  • Yayi Tu
    • 1
  • Zhihong Hu
    • 1
  • Long Ma
    • 1
  • Jing Dai
    • 1
  • Xiaojie Cheng
    • 2
  • Haoran Li
    • 1
  • Lanlan Liu
    • 1
  • Bin Zeng
    • 1
  1. 1.Jiangxi Key Laboratory of Bioprocess Engineering and Co-Innovation Center for In-Vitro Diagnostic Reagents and Devices of Jiangxi Province, College of Life SciencesJiangxi Science & Technology Normal UniversityNanchangChina
  2. 2.Key Laboratory of Bio-resources and Eco-environment, Ministry of Education, Sichuan Key Laboratory of Molecular Biology and Biotechnology, College of Life SciencesSichuan UniversityChengduChina

Personalised recommendations