Homolog identification of heat shock proteins in eight fungi belonging to Pezizomycetes and copy number comparisons

Authors

  • Elisa Zampieri Istituto per la Protezione Sostenibile delle Piante - CNR, Strada delle Cacce 73, 10135 Torino, Italy
  • Antonietta Mello Istituto per la Protezione Sostenibile delle Piante - CNR, Viale P.A. Mattioli 25, 10125 - Torino, Italy

DOI:

https://doi.org/10.60923/issn.2531-7342/23502

Keywords:

Pezizomycetes, comparative genomics, blastp, heat shock proteins, chaperones, stress

Abstract

Heat shock proteins are ubiquitous, highly conserved and play a role in the fungal adaptation to the environment. In the present study of comparative genomics, we used gene models, identified as the stress-response related gene families in the genome of Tuber melanosporum, to find the homologs in the genome of seven other Pezizomycetes having different lifestyles and in the new genome assembly of T. melanosporum. The produced list of homologs was also used to search for a correlation: 1) between heat shock protein copy number and lifestyle (saprotrophic and symbiotic) and 2) heat shock protein copy number and genome size. No significant correlation was found between copies and size, as well as between copies and lifestyle within the limited set of considered fungal species. The utility of a list of genes homologs in Pezizomycetes coding for heat shock proteins or other chaperones is discussed.

References

Andreeva L, Heads R, Green CJ (1999) Cyclophilins and their possible role in the stress response. International Journal of Experimental Pathology 80(6):305‒315. https://doi.org/10.1046/j.1365-2613.1999.00128.x

Chang D, Duda TF Jr (2012) Extensive and continuous duplication facilitates rapid evolution and diversification of gene families. Molecular Biology and Evolution 29(8):2019‒2029. https://doi.org/10.1093/molbev/mss068

Chen B, Feder ME, Kang L (2018) Evolution of heat-shock protein expression underlying adaptive responses to environmental stress. Molecular Ecology 27(15):3040‒3054. https://doi.org/10.1111/mec.14769

Cruz-Laufer AJ, Vanhove MPM, Bachmann L, Barson M, Bassirou H, Bitja Nyom AR, Geraerts M, Hahn C, Huyse T, Kasembele GK, Njom S, Resl P, Smeets K, Kmentová N (2025) Adaptive evolution of stress response genes in parasites aligns with host niche diversity. BMC Biology 23(1):10. https://doi.org/10.1186/s12915-024-02091-w

Felts SJ, Toft DO (2003) p23, a simple protein with complex activities. Cell Stress & Chaperones 8(2):108‒113. https://doi.org/10.1379/1466-1268(2003)008<0108:paspwc>2.0.co;2

Gabella S, Abbà S, Duplessis S, Montanini B, Martin F, Bonfante P (2005) Transcript profiling reveals novel marker genes involved in fruiting body formation in Tuber borchii. Eukaryotic Cell 4(9):1599‒1602. https://doi.org/10.1128/EC.4.9.1599-1602.2005

Hartl FU, Bracher A, Hayer-Hartl M (2011) Molecular chaperones in protein folding and proteostasis. Nature 475(7356):324‒332. https://doi.org/10.1038/nature10317

Kurahashi A, Sato M, Nishibori K, Fujimori F (2014) Heat shock protein 9 mRNA expression increases during fruiting body differentiation in Grifola frondosa and other edible mushrooms. Mycoscience 55(2):98‒102. https://doi.org/10.1016/j.myc.2013.06.001

Lebreton A, Zeng Q, Miyauchi S, Kohler A, Dai YC, Martin FM (2021) Evolution of the mode of nutrition in symbiotic and saprotrophic fungi in forest ecosystems. Annual Review Ecology, Evolution, and Systematics 52:385‒404. https://doi.org/10.1146/annurev-ecolsys-012021-114902

Leonardi P, Iotti M, Donati Zeppa S, Lancellotti E, Amicucci A, Zambonelli A (2017) Morphological and functional changes in mycelium and mycorrhizas of Tuber borchii due to heat stress. Fungal Ecology 29:20‒29. https://doi.org/10.1016/j.funeco.2017.05.003

Lindquist S (1986) The heat-shock response. Annual Review of Biochemistry 55:1151‒1191. https://doi.org/10.1146/annurev.bi.55.070186.005443

Liu D, Qin Z, Wei M, Kong D, Zheng Q, Bai S, Lin S, Zhang Z, Ma Y (2022) Genome-wide analyses of heat shock protein superfamily provide new insights on adaptation to sulfide-rich environments in Urechis unicinctus (Annelida, Echiura). International Journal of Molecular Sciences 23(5):2715. https://doi.org/10.3390/ijms23052715

Martelossi J, Vujovic J, Huang Y, Tatti A, Xu K, Puliga F, Chen X, Stabelli OR, Ghiselli F, Zhang X, Zambonelli A (2025) The high quality Chinese white truffle genome and novel fossil-calibrated estimate of Pezizomycetes divergence reveal the tempo and mode of true truffles genome evolution. Genome Research 35:2601‒2616. https://doi.org/10.1101/gr.280368.124

Martin F, Kohler A, Murat C, Balestrini R, Coutinho PM, Jaillon O, Montanini B, Morin E, Noel B, Percudani R, Porcel B, Rubini A, Amicucci A, Amselem J, Anthouard V, Arcioni S, Artiguenave F, Aury JM, Ballario P, Bolchi A, Brenna A, Brun A, Buée M, Cantarel B, Chevalier G, Couloux A, Da Silva C, Denoeud F, Duplessis S, Ghignone S, Hilselberger B, Iotti M, Marçais B, Mello A, Miranda M, Pacioni G, Quesneville H, Riccioni C, Ruotolo R, Splivallo R, Stocchi V, Tisserant E, Viscomi AR, Zambonelli A, Zampieri E, Henrissat B, Lebrun MH, Paolocci F, Bonfante P, Ottonello S, Wincker P (2010) Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464(7291):1033‒1038. https://doi.org/10.1038/nature08867

Muggia L, Ametrano CG, Sterflinger K, Tesei D (2020) An overview of genomics, phylogenomics and proteomics approaches in Ascomycota. Life 10(12):356. https://doi.org/10.3390/life10120356

Murat C, Payen T, Noel B, Kuo A, Morin E, Chen J, Kohler A, Krizsán K, Balestrini R, Da Silva C, Montanini B, Hainaut M, Levati E, Barry KW, Belfiori B, Cichocki N, Clum A, Dockter RB, Fauchery L, Guy J, Iotti M, Le Tacon F, Lindquist EA, Lipzen A, Malagnac F, Mello A, Molinier V, Miyauchi S, Poulain J, Riccioni C, Rubini A, Sitrit Y, Splivallo R, Traeger S, Wang M, Žifčáková L, Wipf D, Zambonelli A, Paolocci F, Nowrousian M, Ottonello S, Baldrian P, Spatafora JW, Henrissat B, Nagy LG, Aury JM, Wincker P, Grigoriev IV, Bonfante P, Martin FM (2018) Pezizomycetes genomes reveal the molecular basis of ectomycorrhizal truffle lifestyle. Nature Ecology & Evolution 2(18):1956‒1965. https://doi.org/10.1038/s41559-018-0710-4

Pantzartzi CN, Drosopoulou E, Scouras ZG (2013) Assessment and reconstruction of novel HSP90 genes: duplications, gains and losses in fungal and animal lineages. PLoS One 8(9):e73217. https://doi.org/10.1371/journal.pone.0073217

Powell AJ, Conant GC, Brown DE, Carbone I, Dean RA (2008) Altered patterns of gene duplication and differential gene gain and loss in fungal pathogens. BMC Genomics 9:147. https://doi.org/10.1186/1471-2164-9-147

Sagini JPN, Ligabue-Braun R (2024) Fungal heat shock proteins: molecular phylogenetic insights into the host takeover. The Science of Nature 111(2):16. https://doi.org/10.1007/s00114-024-01903-x

Seaver FT (1909) Studies in pyrophilous fungi: I. The occurrence and cultivation of Pyronema. Mycologia 1(4):131–139. https://doi.org/10.1080/00275514.1909.12020584

Takayama S, Xie Z, Reed JC (1999) An evolutionarily conserved family of Hsp70/Hsc70 molecular chaperone regulators. Journal of Biological Chemistry 274(2):781‒786. https://doi.org/10.1074/jbc.274.2.781

Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30(12):2725‒2729. https://doi.org/10.1093/molbev/mst197

Tercero AD, Place SP (2020) Characterizing gene copy number of heat shock protein gene families in the emerald rockcod, Trematomus bernacchii. Genes 11(8):867. https://doi.org/10.3390/genes11080867

Tiwari S, Thakur R, Shankar J (2015) Role of heat-shock proteins in cellular function and in the biology of fungi. Biotechnology Research International 2015:132635. https://doi.org/10.1155/2015/132635

Touchman J (2010) Comparative genomics. Nature Education Knowledge 3(10):13.

Traeger S, Altegoer F, Freitag M, Gabaldon T, Kempken F, Kumar A, Marcet-Houben M, Pöggeler S, Stajich JE, Nowrousian M (2013) The genome and development-dependent transcriptomes of Pyronema confluens: a window into fungal evolution. PLoS Genetics 9(9):e1003820. https://doi.org/10.1371/journal.pgen.1003820

Turan M (2023) Genome-wide analysis and characterization of HSP gene families (HSP20, HSP40, HSP60, HSP70, HSP90) in the yellow fever mosquito (Aedes aegypti) (Diptera: Culicidae). Journal of Insect Science 23(6):27. https://doi.org/10.1093/jisesa/iead114

Wilson AM, Wingfield MJ, Duong TA, Wingfield BD (2025) Thermotolerance and post-fire growth in Rhizina undulata is associated with the expansion of heat stress-related protein families. BMC Genomics 26:1041. https://doi.org/10.1186/s12864-025-11902-5

Wu J, Wang M, Zhou L, Yu D (2016) Small heat shock proteins, phylogeny in filamentous fungi and expression analyses in Aspergillus nidulans. Gene 575(2, Part 3):675‒679. https://doi.org/10.1016/j.gene.2015.09.044

Zampieri E, Balestrini R, Kohler A, Abbà S, Martin F, Bonfante P (2011) The Perigord black truffle responds to cold temperature with an extensive reprogramming of its transcriptional activity. Fungal Genetics and Biology 48(6):585‒591. https://doi.org/10.1016/j.fgb.2010.09.007

Zampieri E, Guzzo F, Commisso M, Mello A, Bonfante P, Balestrini R (2014) Gene expression and metabolite changes during Tuber magnatum fruiting body storage. Current Genetics 60(4):285‒294. https://doi.org/10.1007/s00294-014-0434-1

Zhao X, Yin K, Feng R, Miao R, Lin J, Cao L, Ni Y, Li W, Zhang Q (2023) Genome-wide identification and analysis of the heat-shock protein gene in L. edodes and expression pattern analysis under heat shock. Current Issues in Molecular Biology 45(1):614‒627. https://doi.org/10.3390/cimb45010041

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Published

2026-03-31

How to Cite

Zampieri, E., & Mello, A. (2026). Homolog identification of heat shock proteins in eight fungi belonging to Pezizomycetes and copy number comparisons. Italian Journal of Mycology, 55(1), 24–33. https://doi.org/10.60923/issn.2531-7342/23502

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