Transcription factors in Cenococcum geophilum and their potential roles in ectomycorrhizal symbiosis with Populus tomentosa

Yuying Tang , Daisuke Tsugama , Eman Shalaby , Norihisa Matsushita , Chunlan Lian

Journal of Forestry Research ›› 2026, Vol. 37 ›› Issue (1) : 217

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Journal of Forestry Research ›› 2026, Vol. 37 ›› Issue (1) :217 DOI: 10.1007/s11676-026-02163-3
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Transcription factors in Cenococcum geophilum and their potential roles in ectomycorrhizal symbiosis with Populus tomentosa
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Abstract

Cenococcum geophilum is one of the most widespread ectomycorrhizal (ECM) fungi, yet the transcriptional regulatory mechanisms underlying its symbiosis remain poorly understood. Here, we characterized transcription factor (TF) repertoire across six geographically distinct C. geophilum strains and compared them with those of Laccaria bicolor and L. japonica. Genome-wide analyses revealed that C. geophilum harbors relatively high TF abundance, with expansions of fungal Zn(2)-Cys(6) binuclear cluster domain and fungal TF domain families and strain-specific differences likely reflecting both sequencing approaches and ecological adaptation. Transcriptome profiling of C. geophilum Jacg10 strain during colonization of Populus tomentosa revealed stage-specific expression of TFs, particularly those involved in nitrogen metabolism, aromatic compound processing, and cell cycle regulation. Quantitative reverse transcription-PCR confirmed dynamic expression patterns of six candidate TFs. Among these, CgRlm1 was strongly induced at mid-symbiotic stages, showed transcriptional activation activity in yeast, and provided preliminary evidence for association with promoters of genes linked to cell wall remodeling. These findings indicate that C. geophilum has an expanded and diverse TF repertoire and that specific TFs, especially CgRlm1, may play pivotal roles in regulating ECM development. Overall, this study highlights TFs as regulators of ECM symbiosis and provides a genomic and functional framework for investigating transcriptional regulation in non-model ECM fungi.

Keywords

Cenococcum geophilum / Ectomycorrhiza / TF repertoire / Rlm1 / Symbiosis

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Yuying Tang, Daisuke Tsugama, Eman Shalaby, Norihisa Matsushita, Chunlan Lian. Transcription factors in Cenococcum geophilum and their potential roles in ectomycorrhizal symbiosis with Populus tomentosa. Journal of Forestry Research, 2026, 37 (1) : 217 DOI:10.1007/s11676-026-02163-3

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References

[1]

Almagro Armenteros JJ, Tsirigos KD, Sønderby CK, Petersen TN, Winther O, Brunak S, von Heijne G, Nielsen H. SignalP 5.0 improves signal peptide predictions using deep neural networks. Nat Biotechnol, 2019, 374420423.

[2]

Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G. Gene ontology: tool for the unification of biology. Gene Ontol Consort Nat Genet, 2000, 2512529.

[3]

Balestrini R, Sillo F, Kohler A, Schneider G, Faccio A, Tisserant E, Martin F, Bonfante P. Genome-wide analysis of cell wall-related genes in Tuber melanosporum. Curr Genet, 2012, 583165177.

[4]

Berkey CD, Vyas VK, Carlson M. Nrg1 and Nrg2 transcriptional repressors are differently regulated in response to carbon source. Eukaryot Cell, 2004, 32311317.

[5]

Bonfante P (2001) At the interface between mycorrhizal fungi and plants: the structural organization of cell wall, plasma membrane and cytoskeleton. In: Fungal associations. Springer, pp 45–61. https://doi.org/10.1007/978-3-662-07334-6_4

[6]

Brundrett M, Tedersoo L. Evolutionary history of mycorrhiza symbioses and global host plant diversity. New Phytol, 2018, 220411081115.

[7]

Chen CJ, Wu Y, Li JW, Wang X, Zeng ZH, Xu J, Liu YL, Feng JT, Chen H, He YH, Xia R. TBtools-II: a “one for all, all for one” bioinformatics platform for biological big-data mining. Mol Plant, 2023, 161117331742.

[8]

Chen J, Geng XW, Zhang Q, Lin KQ, Li ZS, Wang BY, Xiao QC, Li XY. Effect of Claroideoglomus etunicatum on rhizosphere bacterial community of tobacco under low nutrient conditions. Adv Biotechnol, 2025, 3322.

[9]

Daguerre Y, Levati E, Ruytinx J, Tisserant E, Morin E, Kohler A, Montanini B, Ottonello S, Brun A, Veneault-Fourrey C, Martin F. Regulatory networks underlying mycorrhizal development delineated by genome-wide expression profiling and functional analysis of the transcription factor repertoire of the plant symbiotic fungus Laccaria bicolor. BMC Genom, 2017, 181737

[10]

de Freitas Pereira M, Veneault-Fourrey C, Vion P, Guinet F, Morin E, Barry KW, Lipzen A, Singan V, Pfister S, Na H, Kennedy M, Egli S, Grigoriev I, Martin F, Kohler A, Peter M. Secretome analysis from the ectomycorrhizal ascomycete Cenococcum geophilum. Front Microbiol, 2018, 9. 141

[11]

Duplessis S, Courty PE, Tagu D, Martin F. Transcript patterns associated with ectomycorrhiza development in Eucalyptus globulus and Pisolithus microcarpus. New Phytol, 2005, 1652599611.

[12]

Fan L, Zhang C, Li JF, Zhao ZT, Liu Y. Metabolomics revealed the tolerance and growth dynamics of arbuscular mycorrhizal fungi (AMF) to soil salinity in licorice. Plants, 2024, 13182652

[13]

Grant CE, Bailey TL, Noble WS. FIMO: scanning for occurrences of a given motif. Bioinformatics, 2011, 27710171018.

[14]

Gustavsson Ruus A (2022) Functional characterization of sterol regulatory element transcription factors in the biocontrol fungus Clonostachys rosea [dissertation]. Swedish University of Agricultural Sciences. https://stud.epsilon.slu.se/18209/3/ruus-gustavsson-a-20220831.pdf

[15]

Hallgren J, Tsirigos KD, Pedersen MD, Almagro Armenteros JJ, Marcatili P, Nielsen H, Krogh A, Winther O (2022) DeepTMHMM predicts alpha and beta transmembrane proteins using deep neural networks [preprint]. bioRxiv. 2022.04.08.487609. https://doi.org/10.1101/2022.04.08.487609

[16]

Hussein B, Huang H, Glory A, Osmani A, Kaminskyj S, Nantel A, Bachewich C. G1/S transcription factor orthologues Swi4p and Swi6p are important but not essential for cell proliferation and influence hyphal development in the fungal pathogen Candida albicans. Eukaryot Cell, 2011, 103384397.

[17]

Kolde R (2019) pheatmap: Pretty Heatmaps. R package version 1.0.12. https://CRAN.R-project.org/package=pheatmap

[18]

Lanfranco L, Bonfante P, Genre A. The mutualistic interaction between plants and arbuscular mycorrhizal fungi. Microbiol Spectr, 2016.

[19]

Lehto T, Zwiazek JJ. Ectomycorrhizas and water relations of trees: a review. Mycorrhiza, 2011, 2127190.

[20]

Levin DE. Regulation of cell wall biogenesis in Saccharomyces cerevisiae: the cell wall integrity signaling pathway. Genetics, 2011, 189411451175.

[21]

Li JL, Li CF, Tsuruta M, Matsushita N, Goto S, Shen ZG, Tsugama D, Zhang SJ, Lian CL. Physiological and transcriptional responses of the ectomycorrhizal fungus Cenococcum geophilum to salt stress. Mycorrhiza, 2022, 323–4327340.

[22]

Li MT, Yuan C, Zhang XH, Pang WB, Zhang PP, Xie RZ, Lian CL, Zhang TX. The transcriptional responses of ectomycorrhizal fungus, Cenococcum geophilum, to drought stress. J Fungi, 2023, 9115.

[23]

Lian C, Li C, Yuan C, Shi Y, Geng Q, Li J, Matsushita N, Zhang S, Ma J, Tsuruta M, Xia Y, Tao Y, Zhang T, Goto S, Obase K, Vaario LM, Siqinbilige S, Zhang H, Li J, Wu J, Kameyama N, Vélez JM, Jiao B, Zhang S, Schadt CW, Piapukiew J, Pachit P, Kosolwattana P, Xu J, Xing H, Wu S (2024) Genomes and population genomics of Cenococcum geophilum highlight the genetic diversity, evolution, and stress responses of ectomycorrhizal fungi [preprint]. Res Sq.https://doi.org/10.21203/rs.3.rs-4894562/v1

[24]

Liu JJ, An B, Luo HL, He CZ, Wang QN. The histone acetyltransferase FocGCN5 regulates growth, conidiation, and pathogenicity of the banana wilt disease causal agent Fusarium oxysporum f. sp. cubense tropical race 4. Res Microbiol, 2022, 1733103902

[25]

LoBuglio KF (1999) Cenococcum. In: Ectomycorrhizal fungi key Genera in profile. Springer, pp 287–309. https://doi.org/10.1007/978-3-662-06827-4_12

[26]

López-Pujol J, Zhang FM, Sun HQ, Ying TS, Ge S. Centres of plant endemism in China: places for survival or for speciation?. J Biogeogr, 2011, 38712671280.

[27]

Marchler-Bauer A, Bo Y, Han LY, He J, Lanczycki CJ, Lu SN, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Lu F, Marchler GH, Song JS, Thanki N, Wang ZX, Yamashita RA, Zhang DC, Zheng CJ, Geer LY, Bryant SH. CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res, 2017, 45D1D200D203.

[28]

Martin F, Aerts A, Ahrén D, Brun A, Danchin EGJ, Duchaussoy F, Gibon J, Kohler A, Lindquist E, Pereda V, Salamov A, Shapiro HJ, Wuyts J, Blaudez D, Buée M, Brokstein P, Canbäck B, Cohen D, Courty PE, Coutinho PM, Delaruelle C, Detter JC, Deveau A, DiFazio S, Duplessis S, Fraissinet-Tachet L, Lucic E, Frey-Klett P, Fourrey C, Feussner I, Gay G, Grimwood J, Hoegger PJ, Jain P, Kilaru S, Labbé J, Lin YC, Legué V, Le Tacon F, Marmeisse R, Melayah D, Montanini B, Muratet M, Nehls U, Niculita-Hirzel H, Oudot-Le Secq MP, Peter M, Quesneville H, Rajashekar B, Reich M, Rouhier N, Schmutz J, Yin T, Chalot M, Henrissat B, Kües U, Lucas S, Van de Peer Y, Podila GK, Polle A, Pukkila PJ, Richardson PM, Rouzé P, Sanders IR, Stajich JE, Tunlid A, Tuskan G, Grigoriev IV. The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature, 2008, 45271838892.

[29]

Martin F, Kohler A, Murat C, Veneault-Fourrey C, Hibbett DS. Unearthing the roots of ectomycorrhizal symbioses. Nat Rev Microbiol, 2016, 1412760773.

[30]

Montanini B, Levati E, Bolchi A, Kohler A, Morin E, Tisserant E, Martin F, Ottonello S. Genome-wide search and functional identification of transcription factors in the mycorrhizal fungus Tuber melanosporum. New Phytol, 2011, 1893736750.

[31]

Ouwerkerk PB, Meijer AH. Yeast one-hybrid screening for DNA-protein interactions. Curr Protoc Mol Biol, 2001, 12. 12.12

[32]

Paradis E, Claude J, Strimmer K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics, 2004, 202289290.

[33]

Peter M, Kohler A, Ohm RA, Kuo AL, Krützmann J, Morin E, Arend M, Barry KW, Binder M, Choi C, Clum A, Copeland A, Grisel N, Haridas S, Kipfer T, LaButti K, Lindquist E, Lipzen A, Maire R, Meier B, Mihaltcheva S, Molinier V, Murat C, Pöggeler S, Quandt CA, Sperisen C, Tritt A, Tisserant E, Crous PW, Henrissat B, Nehls U, Egli S, Spatafora JW, Grigoriev IV, Martin FM. Ectomycorrhizal ecology is imprinted in the genome of the dominant symbiotic fungus Cenococcum geophilum. Nat Commun, 2016, 7. 12662

[34]

Plett JM, Tisserant E, Brun A, Morin E, Grigoriev IV, Kuo AL, Martin F, Kohler A. The mutualist Laccaria bicolor expresses a core gene regulon during the colonization of diverse host plants and a variable regulon to counteract host-specific defenses. Mol Plant Microbe Interact, 2015, 283261273.

[35]

Raudaskoski M, Kothe E. Novel findings on the role of signal exchange in arbuscular and ectomycorrhizal symbioses. Mycorrhiza, 2015, 254243252.

[36]

Rauluseviciute I, Riudavets-Puig R, Blanc-Mathieu R, Castro-Mondragon JA, Ferenc K, Kumar V, Lemma RB, Lucas J, Chèneby J, Baranasic D, Khan A, Fornes O, Gundersen S, Johansen M, Hovig E, Lenhard B, Sandelin A, Wasserman WW, Parcy F, Mathelier A. JASPAR 2024: 20th anniversary of the open-access database of transcription factor binding profiles. Nucleic Acids Res, 2024, 52D1D174D182.

[37]

Rocha MC, Fabri JHTM, Franco de Godoy K, Alves de Castro P, Hori JI, Ferreira da Cunha A, Arentshorst M, Ram AFJ, van den Hondel CAMJJ, Goldman GH, Malavazi I. Aspergillus fumigatus MADS-box transcription factor rlmA is required for regulation of the cell wall integrity and virulence. G3 (Bethesda), 2016, 6929833002.

[38]

Shaw JA, Mol PC, Bowers B, Silverman SJ, Valdivieso MH, Durán A, Cabib E. The function of chitin synthases 2 and 3 in the Saccharomyces cerevisiae cell cycle. J Cell Biol, 1991, 1141111123.

[39]

Shelest E. Transcription factors in fungi. FEMS Microbiol Lett, 2008, 2862145151.

[40]

Shi Z, Zachara JM, Shi L, Wang ZM, Moore DA, Kennedy DW, Fredrickson JK. Redox reactions of reduced flavin mononucleotide (FMN), riboflavin (RBF), and anthraquinone-2, 6-disulfonate (AQDS) with ferrihydrite and lepidocrocite. Environ Sci Technol, 2012, 46211164411652.

[41]

Shi YY, Yan TY, Yuan C, Li CF, Rensing C, Chen YH, Xie RZ, Zhang TX, Lian CL. Comparative physiological and transcriptome analysis provide insights into the response of Cenococcum geophilum, an ectomycorrhizal fungus to cadmium stress. J Fungi, 2022, 87724.

[42]

Smith SE, Read DJ. Mycorrhizal symbiosis, 20083rd ednAcademic Press

[43]

Tagu D, Lapeyrie F, Martin F. The ectomycorrhizal symbiosis: genetics and development. Plant Soil, 2002, 244197105.

[44]

Tamura K, Stecher G, Kumar S. MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol, 2021, 38730223027.

[45]

Tarkka MT, Herrmann S, Wubet T, Feldhahn L, Recht S, Kurth F, Mailänder S, Bönn M, Neef M, Angay O, Bacht M, Graf M, Maboreke H, Fleischmann F, Grams TEE, Ruess L, Schädler M, Brandl R, Scheu S, Schrey SD, Grosse I, Buscot F. OakContigDF159.1, a reference library for studying differential gene expression in Quercus robur during controlled biotic interactions: use for quantitative transcriptomic profiling of oak roots in ectomycorrhizal symbiosis. New Phytol, 2013, 1992529540.

[46]

Todd RB, Zhou MM, Ohm RA, Leeggangers HACF, Visser L, de Vries RP. Prevalence of transcription factors in ascomycete and basidiomycete fungi. BMC Genomics, 2014, 15: 214.

[47]

Vyas VK, Berkey CD, Miyao T, Carlson M. Repressors Nrg1 and Nrg2 regulate a set of stress-responsive genes in Saccharomyces cerevisiae. Eukaryot Cell, 2005, 41118821891.

[48]

Wang HY, Guo SY, Huang MR, Thorsten LH, Wei JC. Ascomycota has a faster evolutionary rate and higher species diversity than Basidiomycota. Sci China Life Sci, 2010, 531011631169.

[49]

Wang Y, Yang ZS, Bao DP, Li B, Yin X, Wu YY, Chen HY, Tang GR, Li NY, Zou G. Improving hypoxia adaption causes distinct effects on growth and bioactive compounds synthesis in an entomopathogenic fungus Cordyceps militaris. Front Microbiol, 2021, 12. 698436

[50]

Wang JY, Chitsaz F, Derbyshire MK, Gonzales NR, Gwadz M, Lu SN, Marchler GH, Song JS, Thanki N, Yamashita RA, Yang MZ, Zhang DC, Zheng CJ, Lanczycki CJ, Marchler-Bauer A. The conserved domain database in 2023. Nucleic Acids Res, 2023, 51D1D384D388.

[51]

Wijnen H, Landman A, Futcher B. The G1 cyclin Cln3 promotes cell cycle entry via the transcription factor Swi6. Mol Cell Biol, 2002, 221244024418.

[52]

Xie DD, Tang C, Wang YY, Jin HJ, Wang YL. The transcription factor CcRlm1 regulates cell wall maintenance and poplar defense response by directly targeting CcChs6 and CcGna1 in Cytospora chrysosperma. Appl Environ Microbiol, 2023, 896e00661-23

[53]

Zhao L, Ding Q, Zeng J, Wang FR, Zhang J, Fan SJ, He XQ. An improved CTAB–ammonium acetate method for total RNA isolation from cotton. Phytochem Anal, 2012, 236647650.

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