Integrated Transcriptomic and Proteomic Analyses Reveal Molecular Mechanism of Response to Heat Shock in

Overview

Journal J Fungi (Basel)

Date 2025 Jan 24

PMID 39852496

Authors

Jiexiong Zhang

Yanxia Li

Yifan Mao

Yesheng Zhang

Botong Zhou

Wei Liu

Wen Wang

Chen Zhang

Affiliations

Soon will be listed here.

Abstract

Morels ( spp.), as one of the rare macroascomycetes that can be cultivated artificially, possess significant economic and scientific values. Morel cultivation is highly sensitive to elevated temperatures; however, the mechanisms of their response to heat shock remain poorly understood. This study integrated transcriptomic and quantitative proteomic analyses of two strains with different thermotolerance (labeled as strains C and D) under normal (18 °C) and high temperature (28 °C) conditions. From over 9300 transcripts and 5000 proteins, both consistency and heterogeneity were found in response to heat shock between the two strains. Both strains displayed a capacity to maintain cellular homeostasis in response to heat shock through highly expressed cell wall integrity (CWI) pathways, heat shock proteins (HSPs), and antioxidant systems. However, strain D, which exhibited stronger thermotolerance, specifically upregulated the ubiquitin ligase , thereby further promoting the expression of HSPs, which may be a key factor influencing the thermotolerance difference among strains. A conceptual model of the heat shock adaptation regulatory network in was proposed for the first time; the results provide novel insights into the thermotolerance response mechanisms of macroascomycetes and valuable resources for the breeding enhancement of thermotolerant morel strains.

References

Anders S, Pyl P, Huber W . HTSeq--a Python framework to work with high-throughput sequencing data. Bioinformatics. 2014; 31(2):166-9. PMC: 4287950. DOI: 10.1093/bioinformatics/btu638. View

Liu Q, Ma H, Zhang Y, Dong C . Artificial cultivation of true morels: current state, issues and perspectives. Crit Rev Biotechnol. 2017; 38(2):259-271. DOI: 10.1080/07388551.2017.1333082. View

Rocha M, Minari K, Fabri J, Kerkaert J, Gava L, da Cunha A . Aspergillus fumigatus Hsp90 interacts with the main components of the cell wall integrity pathway and cooperates in heat shock and cell wall stress adaptation. Cell Microbiol. 2020; 23(2):e13273. PMC: 7855945. DOI: 10.1111/cmi.13273. View

Jiaojiao Z, Fen W, Kuanbo L, Qing L, Ying Y, Caihong D . Heat and light stresses affect metabolite production in the fruit body of the medicinal mushroom Cordyceps militaris. Appl Microbiol Biotechnol. 2018; 102(10):4523-4533. DOI: 10.1007/s00253-018-8899-3. View

Wang S, Li W, Hu L, Cheng J, Yang H, Liu Y . NAguideR: performing and prioritizing missing value imputations for consistent bottom-up proteomic analyses. Nucleic Acids Res. 2020; 48(14):e83. PMC: 7641313. DOI: 10.1093/nar/gkaa498. View

Ludwig C, Gillet L, Rosenberger G, Amon S, Collins B, Aebersold R . Data-independent acquisition-based SWATH-MS for quantitative proteomics: a tutorial. Mol Syst Biol. 2018; 14(8):e8126. PMC: 6088389. DOI: 10.15252/msb.20178126. View

Zhao Y, MacGurn J, Liu M, Emr S . The ART-Rsp5 ubiquitin ligase network comprises a plasma membrane quality control system that protects yeast cells from proteotoxic stress. Elife. 2013; 2:e00459. PMC: 3628405. DOI: 10.7554/eLife.00459. View

Anders S, Huber W . Differential expression analysis for sequence count data. Genome Biol. 2010; 11(10):R106. PMC: 3218662. DOI: 10.1186/gb-2010-11-10-r106. View

Rey O, Danchin E, Mirouze M, Loot C, Blanchet S . Adaptation to Global Change: A Transposable Element-Epigenetics Perspective. Trends Ecol Evol. 2016; 31(7):514-526. DOI: 10.1016/j.tree.2016.03.013. View

10.

Szklarczyk D, Gable A, Lyon D, Junge A, Wyder S, Huerta-Cepas J . STRING v11: protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 2018; 47(D1):D607-D613. PMC: 6323986. DOI: 10.1093/nar/gky1131. View

11.

Tiwari S, Thakur R, Shankar J . Role of Heat-Shock Proteins in Cellular Function and in the Biology of Fungi. Biotechnol Res Int. 2016; 2015:132635. PMC: 4736001. DOI: 10.1155/2015/132635. View

12.

Stanke M, Keller O, Gunduz I, Hayes A, Waack S, Morgenstern B . AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Res. 2006; 34(Web Server issue):W435-9. PMC: 1538822. DOI: 10.1093/nar/gkl200. View

13.

Yaakoub H, Mina S, Calenda A, Bouchara J, Papon N . Oxidative stress response pathways in fungi. Cell Mol Life Sci. 2022; 79(6):333. PMC: 11071803. DOI: 10.1007/s00018-022-04353-8. View

14.

Zhang C, Shi X, Zhang J, Zhang Y, Liu W, Wang W . Integration of Metabolomes and Transcriptomes Provides Insights into Morphogenesis and Maturation in . J Fungi (Basel). 2023; 9(12). PMC: 10744280. DOI: 10.3390/jof9121143. View

15.

Zhang X, Ren A, Li M, Cao P, Chen T, Zhang G . Heat Stress Modulates Mycelium Growth, Heat Shock Protein Expression, Ganoderic Acid Biosynthesis, and Hyphal Branching of Ganoderma lucidum via Cytosolic Ca2. Appl Environ Microbiol. 2016; 82(14):4112-4125. PMC: 4959220. DOI: 10.1128/AEM.01036-16. View

16.

Fuchs B, Mylonakis E . Our paths might cross: the role of the fungal cell wall integrity pathway in stress response and cross talk with other stress response pathways. Eukaryot Cell. 2009; 8(11):1616-25. PMC: 2772411. DOI: 10.1128/EC.00193-09. View

17.

Rodrigues-Pousada C, Devaux F, Caetano S, Pimentel C, Da Silva S, Cordeiro A . Yeast AP-1 like transcription factors (Yap) and stress response: a current overview. Microb Cell. 2019; 6(6):267-285. PMC: 6545440. DOI: 10.15698/mic2019.06.679. View

18.

Lei M, Wu X, Huang C, Qiu Z, Wang L, Zhang R . Trehalose induced by reactive oxygen species relieved the radial growth defects of Pleurotus ostreatus under heat stress. Appl Microbiol Biotechnol. 2019; 103(13):5379-5390. DOI: 10.1007/s00253-019-09834-8. View

19.

Zhang H, Shao S, Zeng Y, Wang X, Qin Y, Ren Q . Reversible phase separation of HSF1 is required for an acute transcriptional response during heat shock. Nat Cell Biol. 2022; 24(3):340-352. DOI: 10.1038/s41556-022-00846-7. View

20.

Shahsavarani H, Sugiyama M, Kaneko Y, Chuenchit B, Harashima S . Superior thermotolerance of Saccharomyces cerevisiae for efficient bioethanol fermentation can be achieved by overexpression of RSP5 ubiquitin ligase. Biotechnol Adv. 2011; 30(6):1289-300. DOI: 10.1016/j.biotechadv.2011.09.002. View