Skip to main content
Log in

Comparative transcriptomic analysis identified differentially expressed genes and pathways involved in the interaction between Tremella fuciformis and Annulohypoxylon stygium

  • Original Paper
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

Tremella fuciformis is an edible and medicinal white jelly mushroom. It has a life cycle that interacts with its companion fungus Annulohypoxylon stygium, both in natural conditions and artificial cultivation. RNA sequencing (RNA-Seq) was used to study the interaction between T. fuciformis and A. stygium by constructing 5 libraries, including the individual T. fuciformis mycelium (1), the T. fuciformis mycelium after interaction with A. stygium (2), the dual mycelia after interaction (3), the A. stygium mycelium after interaction with T. fuciformis (4), and the individual A. stygium mycelium (5). 33.4 G data and 46,871 Unigenes were generated from de novo splicing. For identification of differentially expressed genes (DEGs) related to interaction, we analyzed the expression data of DEGs1-vs-2 ∩ DEGs1-vs-3, and DEGs5-vs-4 ∩ DEGs5-vs-3. DEGs1-vs-2 ∩ DEGs1-vs-3, and DEGs5-vs-4 ∩ DEGs5-vs-3 data showed 614 DEGs and 1537 DEGs, respectively. The 614 DEGs for T. fuciformis and 1537 DEGs for A. stygium were analyzed by GO annotation and were assigned to biology process, cell composition, and molecular functions. The DEGs were used to match the KEGG database. In T. fuciformis, the pathways are primarily enriched various amino acids metabolism, pentose and glucuronate interconversions. In A. stygium, the pathways are primarily enriched in the biosynthesis of secondary metabolites, biosynthesis of antibiotics, starch and sucrose metabolism. The expression patterns of DEGs determined by qRT-PCR were consistent with those obtained by RNA-Seq, thus validating the reliability of our RNA-Seq data. Future studies of the functions of these interesting genes will be helpful to understand the mechanisms by which T. fuciformis interacts with A. stygium. This will also provide a reference for other research on interacting microorganisms.

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

Access this article

Price includes VAT (France)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  • Bach E, Costa S, Oliveira H, Junior J, Silva K, Marco R, Hi EMB, Wadt NSY (2015) Use of polysaccharide extracted from Tremella fuciformis Berk for control diabetes induced in rats. Emir J Food Agric 27:585–591

    Article  Google Scholar 

  • Balestrasse KB, Benavides MP, Gallego SM, Tomaro ML (2003) Effect of cadmium stress on nitrogen metabolism in nodules and roots of soybean plants. Funct Plant Biol 30:57–64

    Article  CAS  Google Scholar 

  • Becker Y, Eaton CJ, Brasell E, May KJ, Becker M, Hassing B, Cartwright GM, Reinhold L, Scott B (2015) The fungal cell-wall integrity MAPK cascade is crucial for hyphal network formation and maintenance of restrictive growth of Epichloë festucae in symbiosis with Lolium perenne. Mol Plant Microbe Interact 28:69–85

    Article  Google Scholar 

  • Brauc S, De Vooght E, Claeys M, Höfte M, Angenon G (2011) Influence of over-expression of cytosolic aspartate aminotransferase on amino acid metabolism and defence responses against Botrytis cinerea infection in Arabidopsis thaliana. J Plant Physiol 168:1813–1819

    Article  CAS  Google Scholar 

  • Chang HY (1998) Mycelial properties of Tremella fuciformis and Hypoxylon sp. Kor J Mycol 26:321–326

    Google Scholar 

  • Chen CJ (1998) Morphological and molecular studies in the genus Tremella. Bibl Mycol 174:1–225

    Google Scholar 

  • Chen AW, Huang NL (2002) Mixed-culture cultivation of edible and medicinal mushroom Tremella fuciformis Berk. (Phragmobasidiomycetes) on synthetic logs. Int J Med Mushrooms 4:349–354

    Google Scholar 

  • Chen Y, Zhao L, Liu B, Zuo S (2012) Application of response surface methodology to optimize microwave-assisted extraction of polysaccharide from Tremella. Phys Procedia 24:429–433

    Article  CAS  Google Scholar 

  • Deng Y, van Peer AF, Lan FS, Wang QF, Jiang Y, Lian LD, Lu DM, Xie B (2016) Morphological and molecular analysis identifies the associated fungus (“Xianghui”) of the medicinal white jelly mushroom, Tremella fuciformis, as Annulohypoxylon stygium. Int J Med Mushrooms 18:253–260

    Article  Google Scholar 

  • Deng Y, Hsiang T, Li S, Lin L, Wang Q, Chen Q, Xie B, Ming R (2018) Comparison of the mitochondrial genome sequences of six Annulohypoxylon stygium isolates suggests short fragment insertions as a potential factor leading to larger genomic size. Front Microbiol 9:2079

    Article  Google Scholar 

  • Deveau A, Kohler A, Frey-Klett P, Martin F (2008) The major pathways of carbohydrate metabolism in the ectomycorrhizal basidiomycete Laccaria bicolor S238N. New Phytol 180:379–390

    Article  CAS  Google Scholar 

  • Eisenman HC, Casadevall A (2012) Synthesis and assembly of fungal melanin. Appl Microbiol Biotechnol 93:931–940

    Article  CAS  Google Scholar 

  • Freihorst D, Brunsch M, Wirth S, Krause K, Kniemeyer O, Linde J, Kunert M, Boland W, Kothe E (2018) Smelling the difference: transcriptome, proteome and volatilome changes after mating. Fungal Genet Biol 112:2–11

    Article  CAS  Google Scholar 

  • Gehrmann T, Pelkmans JF, Ohm RA, Vos AM, Sonnenberg ASM, Baars JJP, Wösten HAB, Reinders MJT, Abeel T (2018) Nucleus-specific expression in the multinuclear mushroom-forming fungus Agaricus bisporus reveals different nuclear regulatory programs. Proc Natl Acad Sci U S A 115:4429–4434

    Article  CAS  Google Scholar 

  • Hsieh HM, Ju YM, Rogers JD (2005) Molecular phylogeny of Hypoxylon and closely related genera. Mycologia 97:844–865

    Article  CAS  Google Scholar 

  • Igbaria A, Lev S, Rose MS, Lee BN, Hadar R, Degani O, Horwitz BA (2008) Distinct and combined roles of the MAP kinases of Cochliobolus heterostrophus in virulence and stress responses. Mol Plant Microbe Interact 21:769–780

    Article  CAS  Google Scholar 

  • Lam HM, Coschigano K, Schultz C, Melo-Oliveira R, Tjaden G, Oliveira I, Ngai N, Hsieh MH, Coruzzi G (1995) Use of arabidopsis mutants and genes to study amide amino acid biosynthesis. Plant Cell 7:887–898

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li HT, Zhou H, Duan RT, Li HY, Tang LH, Yang XQ, Yang YB, Ding ZT (2019) Inducing secondary metabolite production by co-culture of the endophytic fungus Phoma sp. and the symbiotic fungus Armillaria sp. J Nat Prod 82:1009–1013

    Article  CAS  Google Scholar 

  • Li W, Sun YN, Lee C, Bang SH, Kim S, Ma JY, Kim YH, Shim SH (2017) Annulohpoxylotol A and B, new sesquiterpenoids from the endophytic fungus Annulohypoxylon truncatum, are natural NF-jB inhibitors. Arch Pharm Res 40:152–158

    Article  CAS  Google Scholar 

  • Maciel OMC, Tavares RSN, Caluz DRE, Gaspar LR, Debonsi HM (2018) Photoprotective potential of metabolites isolated from algae-associated fungi Annulohypoxylon stygium. J Photochem Photobiol B 178:316–322

    Article  CAS  Google Scholar 

  • Maddi A, Dettman A, Fu C, Seiler S, Free SJ (2012) WSC-1 and HAM-7 are MAK-1 MAP kinase pathway sensors required for cell wall integrity and hyphal fusion in Neurospora crassa. PLoS ONE 7:e42374

    Article  CAS  Google Scholar 

  • Menezes RC, Kai M, Krause K, Matthäus C, Svatoš A, Popp J, Kothe E (2015) Monitoring metabolites from Schizophyllum commune interacting with Hypholoma fasciculare combining LESA–HR mass spectrometry and Raman microscopy. Anal Bioanal 407:2273–2282

    Article  CAS  Google Scholar 

  • Nagalakshmi U, Wang Z, Waern K, Shou C, Raha D, Gerstein M, Snyder M (2008) The transcriptional landscape of the yeast genome defined by RNA sequencing. Science 320:1344–1349

    Article  CAS  Google Scholar 

  • Patyshakuliyeva A, Post H, Zhou M, Jurak E, Heck AJ, Hildén KS, Kabel MA, Mäkelä MR, Altelaar MA, de Vries RP (2015) Uncovering the abilities of Agaricus bisporus to degrade plant biomass throughout its life cycle. Environ Microbiol 17:3098–31109

    Article  CAS  Google Scholar 

  • Pelkmans JF, Vos AM, Scholtmeijer K, Hendrix E, Baars JJ, Gehrmann T, Reinders MJ, Lugones LG, Wösten HA (2016) The transcriptional regulator c2h2 accelerates mushroom formation in Agaricus bisporus. Appl Microbiol Biotechnol 100:7151–7159

    Article  CAS  Google Scholar 

  • Pelkmans JF, Patil MB, Gehrmann T, Reinders MJ, Wösten HA, Lugones LG (2017) Transcription factors of Schizophyllum commune involved in mushroom formation and modulation of vegetative growth. Sci Rep 7:310

    Article  Google Scholar 

  • Rosenthal AZ, Matson EG, Eldar A, Leadbetter JR (2011) RNA-seq reveals cooperative metabolic interactions between two termite-gut spirochete species in co-culture. ISME J 5:1133–1142

    Article  CAS  Google Scholar 

  • Surup F, Mohr KI, Jansen R, Stadler M (2013) Cohaerins G-K, azaphilone pigments from Annulohypoxylon cohaerens and absolute stereochemistry of cohaerins C-K. Phytochemistry 95:252–258

    Article  CAS  Google Scholar 

  • Surup F, Wiebach V, Kuhnert E, Stadler M (2016) Truncaquinones A and B, asterriquinones from Annulohypoxylon truncatum. Tetrahedron Lett 57:2813–2815

    Article  Google Scholar 

  • Ujor VC, Monti M, Peiris DG, Clements MO, Hedger JN (2012) The mycelial response of the white-rot fungus, Schizophyllum commune to the biocontrol agent, Trichoderma viride. Fungal Biol 116:332–341

    Article  Google Scholar 

  • Westermann AJ, Gorski SA, Vogel J (2012) Dual RNA-seq of pathogen and host. Nat Rev Microbiol 10:618–630

    Article  CAS  Google Scholar 

  • Wilhelm BT, Marguerat S, Watt S, Schubert F, Wood V, Goodhead I, Penkett CJ, Rogers J, Bähler J (2008) Dynamic repertoire of a eukaryotic transcriptome surveyed at single-nucleotide resolution. Nature 453:1239–1243

    Article  CAS  Google Scholar 

  • Wingfield BD, Bills GF, Dong Y, Huang W, Nel WJ, Swalarsk-Parry BS, Vaghefi N, Wilken PM, An Z et al (2018) Draft genome sequence of Annulohypoxylon stygium, Aspergillus mulundensis, Berkeleyomyces basicola (syn. Thielaviopsis basicola), Ceratocystis smalleyi, two Cercospora beticola strains, Coleophoma cylindrospora, Fusarium fracticaudum, Phialophora cf. hyalina, and Morchella septimelata. IMA Fungus 9:199–223

    Article  Google Scholar 

  • Wu G (2009) Amino acids: metabolism, functions, and nutrition. Amino Acids 37:1–17

    Article  Google Scholar 

  • Wu Y, Shan L, Yang S, Ma A (2008) Identification and antioxidant activity of melanin isolated from Hypoxylon archeri, a companion fungus of Tremella fuciformis. J Basic Microbiol 48:217–221

    Article  CAS  Google Scholar 

  • Wu YJ, Wei ZX, Zhang FM, Linhardt RJ, Sun PL, Zhang AQ (2019) Structure, bioactivities and applications of the polysaccharides from Tremella fuciformis mushroom: a review. Int J Biol Macromol 121:1005–1010

    Article  CAS  Google Scholar 

  • Yang XM (1954) Tremella fuciformis of China. Bull Biol 12:15–17 (In Chinese)

    Google Scholar 

  • Zhang L, Wang M (2016) Polyethylene glycol-based ultrasound-assisted extraction and ultrafiltration separation of polysaccharides from Tremella fuciformis (snow fungus). Food Bioprod Process 100:464–468

    Article  CAS  Google Scholar 

  • Zhang JX, Chen Q, Huang CY, Gao W, Qu JB (2015) History, current situation and trend of edible mushroom industry development. Mycosystema 34:524–540 (in Chinese with an English abstract)

    CAS  Google Scholar 

  • Zou Y, Hou X (2017) Extraction optimization, composition analysis, and antioxidation evaluation of polysaccharides from white jelly mushroom, Tremella fuciformis (Tremellomycetes). Int J Med Mushrooms 19:1113–1121

    Article  Google Scholar 

Download references

Acknowledgements

This research was supported by a grant from the National Natural Science Foundation of China (NSFC) (No. 31572182) to Aimin Ma.

Author information

Authors and Affiliations

Authors

Contributions

DL and AM designed the experiments. DL and DP performed the experiments. YW and ZZ analyzed the data. DL wrote the manuscript. LZ, LC, and AM critically reviewed the manuscript.

Corresponding author

Correspondence to Aimin Ma.

Ethics declarations

Conflict of interest

The authors declare that there are no conflicts of interest.

Ethical approval

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

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, D., Pujiana, D., Wang, Y. et al. Comparative transcriptomic analysis identified differentially expressed genes and pathways involved in the interaction between Tremella fuciformis and Annulohypoxylon stygium. Antonie van Leeuwenhoek 112, 1675–1689 (2019). https://doi.org/10.1007/s10482-019-01294-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-019-01294-4

Keywords

Navigation