CoChat
Sign Up
Cited by 0Fungal and yeast genetics researchBiofuel production and bioconversionEnzyme Production and Characterization

The DOI matches its Crossref record; 1 of the 1 references it cites were found in a registry or an index.

Multi-omics analysis reveals Protein Kinase A-associated regulatory remodeling during adaptation of Trichoderma reesei to lignocellulosic substrate

Open access
Zenaide-Neto, Hermano, Pedersoli, Wellington Ramos, Maués, David Batista, Pereira, Lucas Matheus Soares, Taveira, Iasmin Cartaxo, Simon, Thiago de Andrade, Steindorff, Andrei S., Faça, Vitor Marcel, de Paula, Renato Graciano, Silva, Roberto N.·2026·World Journal of Microbiology and Biotechnology
DOI 10.1007/s11274-026-05252-xPMC PMC13550043

Published version of a preprint

Open this paper in CoChat — free accountOpen PDF

Abstract

The filamentous fungus Trichoderma reesei is a major industrial source of holocellulolytic enzymes, and its response to complex carbon sources is regulated by nutrient-sensing mechanisms, including the cyclic adenosine monophosphate (cAMP)–protein kinase A (PKA) signaling pathway. Here, we integrated transcriptomics, quantitative proteomics, and phosphoproteomics to analyze PKAc1-associated responses in the parental strain QM9414 and a Δ pkac1 strain cultivated under glucose or sugarcane bagasse conditions. Deletion of pkac1 was associated with altered growth-related phenotypes and reduced extracellular activities of selected biomass-depolymerizing enzymes. Multi-omics profiling revealed condition-dependent changes affecting subsets of carbohydrate-active enzymes (CAZymes) genes and proteins, nutrient transporters, stress-associated proteins, and regulatory factors. Phosphoproteomics identified phosphorylation-state changes associated with pkac1 deletion, including reduced phosphorylation at sites enriched for the PKA consensus motif. In silico peptide docking was used to prioritize candidate PKAc1-associated substrates for future validation, including a Sec 7-derived peptide with favorable docking behavior relative to the control peptide. Together, these data support a working model in which PKAc1 contributes to regulatory and phosphorylation-state remodeling during adaptation to sugarcane bagasse, with effects on the magnitude and/or timing of selected CAZyme-related outputs in T. reesei .

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1007/s11274-026-05252-x

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Flagged first, then by citations

Show all 1 references

Research works printed but not linked: 39

  1. Antoniêto ACC, de Paula RG, Castro LS, Silva-Rocha R, Persinoti GF, Silva RN (2016) Trichoderma reesei CRE1-mediated carbon catabolite repression in response to sophorose through RNA sequencing analysis. Curr Genomics 17(2):119–131 · DOI
  2. Baker SE (2018) Protein hyperproduction in fungi by design. Appl Microbiol Biotechnol 102:8621–8628. https://doi.org/10.1007/s00253-018-9265-1 · DOI
  3. Banno S, Ochiai N, Noguchi R et al (2005) A catalytic subunit of cyclic AMP-dependent protein kinase, Pkac-1, regulates asexual differentiation in Neurospora crassa. Genes Genet Syst 80(1):25–34 · DOI
  4. Bischof RH, Ramoni J, Seiboth B (2016) Cellulases and beyond: the first 70 years of the enzyme producer Trichoderma reesei. Microb Cell Fact 15:106 · DOI
  5. Budovskaya YV, Stephan JS, Deminoff SJ, Herman PK (2005) An evolutionary proteomics approach identifies substrates of the cAMP-dependent protein kinase. Proc Natl Acad Sci U S A 102(39):13933–13938 · DOI
  6. Chen Y, Sun J, Yang Y, Zhang J, Zheng F, Liu W (2021) cAMP activates calcium signalling via phospholipase C to regulate cellulase production in the filamentous fungus Trichoderma reesei. Biotechnol Biofuels 14:62 · DOI
  7. de Paula RG, Antoniêto ACC, Carraro CB, Lopes DCB, Persinoti GF, Peres NTA, Martinez-Rossi NM, Silva-Rocha R, Silva RN (2018) The duality of the MAPK signaling pathway in the control of metabolic processes and cellulase production in Trichoderma reesei. Sci Rep 8:14931 · DOI
  8. de Souza WR, de Gouvêa PF, Savoldi M, Malavazi I, de Souza Bernardes LA, Goldman MHS, de Vries RP, de Castro Oliveira JV, Goldman GH (2011) Transcriptome analysis of Aspergillus niger grown on sugarcane bagasse. Biotechnol Biofuels 4:40 · DOI
  9. Dos Santos Castro L, Pedersoli WR, Antoniêto ACC, Steindorff AS, Silva-Rocha R, Martinez-Rossi NM, Rossi A, Brown NA, Goldman GH, Faça VM, Persinoti GF, Silva RN (2014a) Comparative metabolism of cellulose, sophorose and glucose in Trichoderma reesei using high-throughput genomic and proteomic analyses. Biotechnol Biofuels 7:41 · DOI
  10. Dos Santos Castro L, Antoniêto ACC, Pedersoli WR, Silva-Rocha R, Persinoti GF, Silva RN (2014b) Expression pattern of cellulolytic and xylanolytic genes regulated by transcriptional factors Xyr1 and Cre1 are affected by carbon source in Trichoderma reesei. Gene Expr Patterns 14(2):88–95 · DOI
  11. Dos Santos Castro L, de Paula RG, Antoniêto ACC, Persinoti GF, Silva-Rocha R, Silva RN (2016) Understanding the role of the master regulator XYR1 in Trichoderma reesei by global transcriptional analysis. Front Microbiol 7:175 · DOI
  12. Druzhinina IS, Kubicek CP (2017) Genetic engineering of Trichoderma reesei cellulases and their production. Microb Biotechnol 10(6):1485–1499 · DOI
  13. Garcia Lopez A, Pem V, Jacobsen ID, Ebel F, Dandekar T, Müller T (2024) FungiFun3: systemic gene set enrichment analysis for fungal species. Bioinformatics 40:11 · DOI
  14. Grosse C, Heinekamp T, Kniemeyer O, Gehrke A, Brakhage AA (2008) Protein kinase A regulates growth, sporulation, and pigment formation in Aspergillus fumigatus. Appl Environ Microbiol 74(15):4923–4933 · DOI
  15. Himmel ME, Ding SY, Johnson DK, Adney WS, Nimlos MR, Brady JW, Foust TD (2007) Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science 315(5813):804–807 · DOI
  16. Hinterdobler W, Schalamun M, Udvardi V, Dubey M, Molnar AP, Sulyok M, Schmoll M (2019) The role of Pkac1 in gene regulation and trichodimerol production in Trichoderma reesei. Fungal Biol Biotechnol 6:12 · DOI
  17. Howard SC, Chang YW, Budovskaya YV, Herman PK (2001) The Ras/PKA signaling pathway of Saccharomyces cerevisiae exhibits a functional interaction with the Sin4p complex of the RNA polymerase II holoenzyme. Genetics 159(1):77–89 · DOI
  18. Huang ZX, Wang H, Wang YM, Wang Y (2014) Novel mechanism coupling cyclic AMP-protein kinase A signaling and Golgi trafficking via Gyp1 phosphorylation in polarized growth. Eukaryot Cell 13(12):1548–1556 · DOI
  19. International Energy Agency (IEA) (2025) Renewables 2025: Analysis and forecasts to 2030. IEA, Paris
  20. Ivanova C, Bædker M, Seiboth B (2017) Genome sequencing and transcriptome analysis of Trichoderma reesei QM9978 strain reveals a distal chromosome translocation to be responsible for loss of vib1 expression and loss of cellulase induction. Biotechnol Biofuels 10:209 · DOI
  21. Kerkaert JD, Huberman LB (2023) Regulation of nutrient utilization in filamentous fungi. Appl Microbiol Biotechnol 107(19):5873–5898 · DOI
  22. Kim D, Paggi JM, Park C, Bennett C, Salzberg SL (2019) Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat Biotechnol 37(8):907–915 · DOI · Paper page
  23. Li N, Zhang K, Shi P, Yang K, Wang Y, Luo H, Yao B, Huang H (2022) Roles of Pkac1 and Cre1 in cellulose degradation, conidiation, and yellow pigment synthesis in Trichoderma reesei QM6a. Biotechnol Lett 44(12):1465–1475 · DOI
  24. Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15(12):550 · DOI · Paper page
  25. Miller G (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428 · DOI · Paper page
  26. Nogueira KM, Costa MN, de Paula RG, Mendonça-Natividade FC, Ricci-Azevedo R, Silva RN (2015) Evidence of cAMP involvement in cellobiohydrolase expression and secretion by Trichoderma reesei in presence of the inducer sophorose. BMC Microbiol 15:195 · DOI
  27. Olsen JV, Blagoev B, Gnad F, Macek B, Kumar C, Mortensen P, Mann M (2006) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127(3):635–648 · DOI
  28. Oshiquiri LH, Pereira LMS, Maués DB, Milani ER, Silva AC, Jesus LFMC, Silva-Neto JA, Veras FP, de Paula RG, Silva RN (2024) Regulatory role of vacuolar calcium transport proteins in growth, calcium signaling, and cellulase production in Trichoderma reesei. J Fungi (Basel) 10(12):853 · DOI
  29. Pedersoli WR, de Paula RG, Antoniêto ACC, Carraro CB, Taveira IC, Maués DB, Martins MP, Ribeiro LFC, Damasio ARL, Silva-Rocha R, Rossi Filho A, Silva RN (2021) Analysis of the phosphorylome of Trichoderma reesei cultivated on sugarcane bagasse suggests post-translational regulation of the secreted glycosyl hydrolase Cel7A. Biotechnol Rep (Amst) 31:e00652 · DOI
  30. Richardson BC, McDonold CM, Fromme JC (2012) The Sec 7 Arf-GEF is recruited to the trans-Golgi network by positive feedback. Dev Cell 22(4):799–810 · DOI
  31. Schalamun M, Kiesenhofer DP, Castanheira S, Malzl D, Mach RL, Zeilinger S, Schmoll M (2023) MAPkinases regulate secondary metabolism, sexual development and light dependent cellulase regulation in Trichoderma reesei. Sci Rep 13:1912 · DOI
  32. Schmoll M (2018) Regulation of plant cell wall degradation by light in Trichoderma. Fungal Biol Biotechnol 5:10 · DOI
  33. Schuster A, Bruno KS, Collett JR, Baker SE, Seiboth B, Kubicek CP, Schmoll M (2012) Roles of protein kinase A and adenylate cyclase in light-modulated cellulase regulation in Trichoderma reesei. Appl Environ Microbiol 78(7):2168–2178 · DOI
  34. Tyanova S, Temu T, Cox J (2015) Visualization of LC–MS/MS proteomics data in MaxQuant. Proteomics 15(8):1453–1456 · DOI
  35. Tyanova S, Temu T, Sinitcyn P et al (2016) The Perseus computational platform for comprehensive analysis of (prote)omics data. Nat Methods 13(9):731–740 · DOI · Paper page
  36. Wang Z, An X, Liu L, Liu G, Qu Y (2019) CLP1, a novel plant homeo domain protein, participates in regulating cellulase gene expression in the filamentous fungus Trichoderma reesei. Front Microbiol 10:1700 · DOI
  37. Xiao Z, Storms R, Tsang A (2005) Microplate-based carboxymethylcellulose assay for endoglucanase activity. Anal Biochem 342(1):176–178 · DOI
  38. Yan S, Xu Y, Yu XW (2021) From induction to secretion: a complicated route for cellulase production in Trichoderma reesei. Bioresour Bioprocess 8:107. https://doi.org/10.1186/s40643-021-00461-8 · DOI
  39. Zhou P, Jin B, Li H, Huang SY (2018) HPEPDOCK: a web server for blind peptide–protein docking based on a hierarchical algorithm. Nucleic Acids Res 46(W1):W443–W450 · DOI

Metadata

Authors
Zenaide-Neto, H., Pedersoli, W. R., Maués, D. B., Pereira, L. M. S., Taveira, I. C., Simon, T. D. A., Steindorff, A. S., Faça, V. M., de Paula, R. G., & Silva, R. N.
Affiliations
  • Universidade de São Paulo (BR)
  • Universidade Federal do Espírito Santo (BR)
  • Joint Genome Institute (US)
Corresponding author
Silva, Roberto N.
ORCID
Venue
World Journal of Microbiology and Biotechnology
Publisher
Springer Science and Business Media LLC
Published
2026-09-08
Volume
42
Issue
9
ISSN
  • 0959-3993 (ISSN-L)
  • 1573-0972
DOI
10.1007/s11274-026-05252-x
PMC
PMC13550043
OpenAlex
W7211891226
Cited by
0
References
1
FWCI
0.00
Type
journal article
Language
en
Open access
Licence
Locations
  • World Journal of Microbiology and Biotechnology (publishedVersion, cc-by)
  • Research Square (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
Universidade De São Paulo
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
  • Physical Sciences › Engineering › Biomedical Engineering › Biofuel production and bioconversion
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Enzyme Production and Characterization
Keywords
Trichoderma reesei, protein kinase A, cAMP signaling, sugarcane bagasse, carbohydrate-active enzymes, phosphoproteomics, nutrient sensing, protein-peptide docking, nutrient transporters, stress-related proteins
MeSH terms
Multiomics, Adaptation, Physiological, Cellulose, Fungal Proteins, Glucose, Hypocreales, Lignin, Phosphorylation, Trichoderma, Signal Transduction, Gene Expression Regulation, Fungal, Cyclic AMP-Dependent Protein Kinases, Gene Expression Profiling, Saccharum, Proteomics

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review