Fungal Biofactories

Institution: Instituto de Agroquímica y Tecnología de Alimentos (IATA)

Members (researchers): Jose F. Marcos

Home page: https://www.iata.csic.es/en/research/fungal-biofactories
Contact email: jmarcos@csic.es

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Fungal biofactories; Filamentous fungi; Yeasts; Synthetic biology; Genome editing; Antifungals; Protein and enzyme bioproduction; Bioactive molecules; Metabolic engineering; Plant biomass valorization

Research topics:
Publications

Yélamos, A. M., Marcos, J. F., Manzanares, P., & Garrigues, S. (2025). Harnessing Filamentous Fungi for Enzyme Cocktail Production Through Rice Bran Bioprocessing. Journal of Fungi, 11(2), 106. https://doi.org/10.3390/jof11020106

Herranz, M. C., Navarro, J. A., Locascio, A., Peña, L., Manzanares, P., Marcos, J. F., & Pallás, V. (2024). Comparative metabolomic analysis of the phloem sap of nine citrus relatives with different degrees of susceptibility to Huanglongbing disease. European Journal of Plant Pathology, 170(3), 463–478. https://doi.org/10.1007/s10658-024-02910-4

Ropero-Pérez, C., Bolós, B., Giner-Llorca, M., Locascio, A., Garrigues, S., Gandía, M., Manzanares, P., & Marcos, J. F. (2023). Transcriptomic Profile of Penicillium digitatum Reveals Novel Aspects of the Mode of Action of the Antifungal Protein AfpB. Microbiology Spectrum, 11(3). https://doi.org/10.1128/spectrum.04846-22

Giner-Llorca, M., Locascio, A., del Real, J. A., Marcos, J. F., & Manzanares, P. (2023). Novel findings about the mode of action of the antifungal protein PeAfpA against Saccharomyces cerevisiae. Applied Microbiology and Biotechnology, 107(22), 6811–6829. https://doi.org/10.1007/s00253-023-12749-0

Gandía, M., Moreno‐Giménez, E., Giner‐Llorca, M., Garrigues, S., Ropero‐Pérez, C., Locascio, A., Martínez‐Culebras, P. V., Marcos, J. F., & Manzanares, P. (2022). Development of a FungalBraid Penicillium expansum‐based expression system for the production of antifungal proteins in fungal biofactories. Microbial Biotechnology, 15(2), 630–647. Portico. https://doi.org/10.1111/1751-7915.14006

Garrigues, S., Manzanares, P., & Marcos, J. F. (2022). Application of recyclable CRISPR/Cas9 tools for targeted genome editing in the postharvest pathogenic fungi Penicillium digitatum and Penicillium expansum. Current Genetics, 68(3–4), 515–529. https://doi.org/10.1007/s00294-022-01236-0

Gandía, M., Kakar, A., Giner-Llorca, M., Holzknecht, J., Martínez-Culebras, P., Galgóczy, L., Marx, F., Marcos, J. F., & Manzanares, P. (2021). Potential of Antifungal Proteins (AFPs) to Control Penicillium Postharvest Fruit Decay. Journal of Fungi, 7(6), 449. https://doi.org/10.3390/jof7060449

Martínez-Culebras, P. V., Gandía, M., Garrigues, S., Marcos, J. F., & Manzanares, P. (2021). Antifungal Peptides and Proteins to Control Toxigenic Fungi and Mycotoxin Biosynthesis. International Journal of Molecular Sciences, 22(24), 13261. https://doi.org/10.3390/ijms222413261

Bugeda, A., Garrigues, S., Gandía, M., Manzanares, P., Marcos, J. F., & Coca, M. (2020). The Antifungal Protein AfpB Induces Regulated Cell Death in Its Parental Fungus Penicillium digitatum. MSphere, 5(4). https://doi.org/10.1128/msphere.00595-20

Vazquez‐Vilar, M., Gandía, M., García‐Carpintero, V., Marqués, E., Sarrion‐Perdigones, A., Yenush, L., Polaina, J., Manzanares, P., Marcos, J. F., & Orzaez, D. (2020). Multigene Engineering by GoldenBraid Cloning: From Plants to Filamentous Fungi and Beyond. Current Protocols in Molecular Biology, 130(1). Portico. https://doi.org/10.1002/cpmb.116

Alexander, A. J. T., Muñoz, A., Marcos, J. F., & Read, N. D. (2020). Calcium homeostasis plays important roles in the internalization and activities of the small synthetic antifungal peptide PAF26. Molecular Microbiology, 114(4), 521–535. Portico. https://doi.org/10.1111/mmi.14532

Holzknecht, J., Kühbacher, A., Papp, C., Farkas, A., Váradi, G., Marcos, J. F., Manzanares, P., Tóth, G. K., Galgóczy, L., & Marx, F. (2020). The Penicillium chrysogenum Q176 Antimicrobial Protein PAFC Effectively Inhibits the Growth of the Opportunistic Human Pathogen Candida albicans. Journal of Fungi, 6(3), 141. https://doi.org/10.3390/jof6030141

Garrigues, S., Marcos, J. F., Manzanares, P., & Gandía, M. (2020). A Novel Secreted Cysteine-Rich Anionic (Sca) Protein from the Citrus Postharvest Pathogen Penicillium digitatum Enhances Virulence and Modulates the Activity of the Antifungal Protein B (AfpB). Journal of Fungi, 6(4), 203. https://doi.org/10.3390/jof6040203

Gandía, M., Garrigues, S., Bolós, B., Manzanares, P., & Marcos, J. F. (2019). The Myosin Motor Domain-Containing Chitin Synthases Are Involved in Cell Wall Integrity and Sensitivity to Antifungal Proteins in Penicillium digitatum. Frontiers in Microbiology, 10. https://doi.org/10.3389/fmicb.2019.02400

Bundó, M., Shi, X., Vernet, M., Marcos, J. F., López-García, B., & Coca, M. (2019). Rice Seeds as Biofactories of Rationally Designed and Cell-Penetrating Antifungal PAF Peptides. Frontiers in Plant Science, 10. https://doi.org/10.3389/fpls.2019.00731

Manzanares, P., Gandía, M., Garrigues, S., & Marcos, J. F. (2019). Improving Health-Promoting Effects of Food-Derived Bioactive Peptides through Rational Design and Oral Delivery Strategies. Nutrients, 11(10), 2545. https://doi.org/10.3390/nu11102545

Manzanares, P., Martínez, R., Garrigues, S., Genovés, S., Ramón, D., Marcos, J. F., & Martorell, P. (2018). Tryptophan-Containing Dual Neuroprotective Peptides: Prolyl Endopeptidase Inhibition and Caenorhabditis elegans Protection from β-Amyloid Peptide Toxicity. International Journal of Molecular Sciences, 19(5), 1491. https://doi.org/10.3390/ijms19051491

Garrigues, S., Gandía, M., Castillo, L., Coca, M., Marx, F., Marcos, J. F., & Manzanares, P. (2018). Three Antifungal Proteins From Penicillium expansum: Different Patterns of Production and Antifungal Activity. Frontiers in Microbiology, 9. https://doi.org/10.3389/fmicb.2018.02370

Heredero, M., Garrigues, S., Gandía, M., Marcos, J. F., & Manzanares, P. (2018). Rational Design and Biotechnological Production of Novel AfpB-PAF26 Chimeric Antifungal Proteins. Microorganisms, 6(4), 106. https://doi.org/10.3390/microorganisms6040106

Shi, X., Cordero, T., Garrigues, S., Marcos, J. F., Daròs, J., & Coca, M. (2018). Efficient production of antifungal proteins in plants using a new transient expression vector derived from tobacco mosaic virus. Plant Biotechnology Journal, 17(6), 1069–1080. Portico. https://doi.org/10.1111/pbi.13038

Garrigues, S., Gandía, M., Borics, A., Marx, F., Manzanares, P., & Marcos, J. F. (2017). Mapping and Identification of Antifungal Peptides in the Putative Antifungal Protein AfpB from the Filamentous Fungus Penicillium digitatum. Frontiers in Microbiology, 8. https://doi.org/10.3389/fmicb.2017.00592

Garrigues, S., Gandía, M., Popa, C., Borics, A., Marx, F., Coca, M., Marcos, J. F., & Manzanares, P. (2017). Efficient production and characterization of the novel and highly active antifungal protein AfpB from Penicillium digitatum. Scientific Reports, 7(1). https://doi.org/10.1038/s41598-017-15277-w

Ribera, J., Gandía, M., Marcos, J. F., Bas, M. del C., Fink, S., & Schwarze, F. W. M. R. (2017). Effect of Trichoderma-enriched organic charcoal in the integrated wood protection strategy. PLOS ONE, 12(8), e0183004. https://doi.org/10.1371/journal.pone.0183004

Cánovas, D., Marcos, J. F., Marcos, A. T., & Strauss, J. (2016). Nitric oxide in fungi: is there NO light at the end of the tunnel? Current Genetics, 62(3), 513–518. https://doi.org/10.1007/s00294-016-0574-6

Sonderegger, C., Galgóczy, L., Garrigues, S., Fizil, Á., Borics, A., Manzanares, P., Hegedüs, N., Huber, A., Marcos, J. F., Batta, G., & Marx, F. (2016). A Penicillium chrysogenum-based expression system for the production of small, cysteine-rich antifungal proteins for structural and functional analyses. Microbial Cell Factories, 15(1). https://doi.org/10.1186/s12934-016-0586-4

Harries, E., Gandía, M., Carmona, L., & Marcos, J. F. (2015). The <scp>P</scp>enicillium digitatum protein <scp>O</scp>‐mannosyltransferase <scp>P</scp>mt2 is required for cell wall integrity, conidiogenesis, virulence and sensitivity to the antifungal peptide <scp>PAF26</scp>. Molecular Plant Pathology, 16(7), 748–761. Portico. https://doi.org/10.1111/mpp.12232

López-García, B., Harries, E., Carmona, L., Campos-Soriano, L., López, J. J., Manzanares, P., Gandía, M., Coca, M., & Marcos, J. F. (2015). Concatemerization increases the inhibitory activity of short, cell-penetrating, cationic and tryptophan-rich antifungal peptides. Applied Microbiology and Biotechnology, 99(19), 8011–8021. https://doi.org/10.1007/s00253-015-6541-1

Garrigues, S., Gandía, M., & Marcos, J. F. (2015). Occurrence and function of fungal antifungal proteins: a case study of the citrus postharvest pathogen Penicillium digitatum. Applied Microbiology and Biotechnology, 100(5), 2243–2256. https://doi.org/10.1007/s00253-015-7110-3

Marcos, A. T., Ramos, M. S., Marcos, J. F., Carmona, L., Strauss, J., & Cánovas, D. (2015). Nitric oxide synthesis by nitrate reductase is regulated during development in <scp>A</scp>spergillus. Molecular Microbiology, 99(1), 15–33. Portico. https://doi.org/10.1111/mmi.13211

Muñoz, A., Harries, E., Contreras-Valenzuela, A., Carmona, L., Read, N. D., & Marcos, J. F. (2013). Two Functional Motifs Define the Interaction, Internalization and Toxicity of the Cell-Penetrating Antifungal Peptide PAF26 on Fungal Cells. PLoS ONE, 8(1), e54813. https://doi.org/10.1371/journal.pone.0054813

Bou Zeidan, M., Carmona, L., Zara, S., & Marcos, J. F. (2013). FLO11 Gene Is Involved in the Interaction of Flor Strains of Saccharomyces cerevisiae with a Biofilm-Promoting Synthetic Hexapeptide. Applied and Environmental Microbiology, 79(19), 6023–6032. https://doi.org/10.1128/aem.01647-13

Muñoz, A., Marcos, J. F., & Read, N. D. (2012). Concentration‐dependent mechanisms of cell penetration and killing by the de novo designed antifungal hexapeptide PAF26. Molecular Microbiology, 85(1), 89–106. Portico. https://doi.org/10.1111/j.1365-2958.2012.08091.x

Marcos, J. F., Gandía, M., Harries, E., Carmona, L., & Muñoz, A. (2012). Antifungal Peptides: Exploiting Non-Lytic Mechanisms and Cell Penetration Properties. Small Wonders: Peptides for Disease Control, 337–357. https://doi.org/10.1021/bk-2012-1095.ch016

Marcos, J. F., & Manzanares, P. (2011). Antimicrobial Peptides. Antimicrobial Polymers, 195–225. Portico. https://doi.org/10.1002/9781118150887.ch8

Enrique, M., Ibáñez, A., Marcos, J. F., Yuste, M., Martínez, M., Vallés, S., & Manzanares, P. (2010). β‐Glucanases as a Tool for the Control of Wine Spoilage Yeasts. Journal of Food Science, 75(1). Portico. https://doi.org/10.1111/j.1750-3841.2009.01448.x

Ruiz-Giménez, P., Ibáñez, A., Salom, J. B., Marcos, J. F., López-Díez, J. J., Vallés, S., Torregrosa, G., Alborch, E., & Manzanares, P. (2010). Antihypertensive Properties of Lactoferricin B-Derived Peptides. Journal of Agricultural and Food Chemistry, 58(11), 6721–6727. https://doi.org/10.1021/jf100899u

Gonzalez-Candelas, L., Alamar, S., Sanchez-Torres, P., Zacarias, L., & Marcos, J. F. (2010). A transcriptomic approach highlights induction of secondary metabolism in citrus fruit in response to Penicillium digitatum infection. BMC Plant Biology, 10(1), 194. https://doi.org/10.1186/1471-2229-10-194

López-García, B., Gandía, M., Muñoz, A., Carmona, L., & Marcos, J. F. (2010). A genomic approach highlights common and diverse effects and determinants of susceptibility on the yeast Saccharomyces cerevisiae exposed to distinct antimicrobial peptides. BMC Microbiology, 10(1). https://doi.org/10.1186/1471-2180-10-289

Marcos, J. F., & Gandía, M. (2009). Antimicrobial peptides: to membranes and beyond. Expert Opinion on Drug Discovery, 4(6), 659–671. https://doi.org/10.1517/17460440902992888

Marcos, J. F., Muñoz, A., Pérez-Payá, E., Misra, S., & López-García, B. (2008). Identification and Rational Design of Novel Antimicrobial Peptides for Plant Protection. Annual Review of Phytopathology, 46(1), 273–301. https://doi.org/10.1146/annurev.phyto.121307.094843

Marcos, J. F., Sánchez-Torres, P., Alamar, S., Zacarías, L., & González-Candelas, L. (2007). HIGH-THROUGHPUT APPROACHES TO THE IDENTIFICATION OF CITRUS GENES INVOLVED IN FRUIT RESPONSE TO PENICILLIUM DIGITATUM INFECTION. Acta Horticulturae, 738, 229–233. https://doi.org/10.17660/actahortic.2007.738.22

Muñoz, A., López-García, B., & Marcos, J. F. (2007). Comparative Study of Antimicrobial Peptides To Control Citrus Postharvest Decay Caused by Penicillium digitatum. Journal of Agricultural and Food Chemistry, 55(20), 8170–8176. https://doi.org/10.1021/jf0718143

Muñoz, A., López-García, B., & Marcos, J. F. (2006). Studies on the Mode of Action of the Antifungal Hexapeptide PAF26. Antimicrobial Agents and Chemotherapy, 50(11), 3847–3855. https://doi.org/10.1128/aac.00650-06

Centeno, J. M., Burguete, M. C., Castelló-Ruiz, M., Enrique, M., Vallés, S., Salom, J. B., Torregrosa, G., Marcos, J. F., Alborch, E., & Manzanares, P. (2006). Lactoferricin-Related Peptides with Inhibitory Effects on ACE-Dependent Vasoconstriction. Journal of Agricultural and Food Chemistry, 54(15), 5323–5329. https://doi.org/10.1021/jf060482j

Muñoz, A., & Marcos, J. F. (2006). Activity and mode of action against fungal phytopathogens of bovine lactoferricin-derived peptides. Journal of Applied Microbiology, 101(6), 1199–1207. https://doi.org/10.1111/j.1365-2672.2006.03089.x

Lafuente, M. T., Zacarias, L., Sala, J. M., Sánchez-Ballesta, M. T., Gosalbes, M. J., Marcos, J. F., González-Candelas, L., Lluch, Y., & Granell, A. (2005). UNDERSTANDING THE BASIS OF CHILLING INJURY IN CITRUS FRUIT. Acta Horticulturae, 682, 831–842. https://doi.org/10.17660/actahortic.2005.682.108

Vilar, M., Saurí, A., Marcos, J. F., Mingarro, I., & Pérez‐Payá, E. (2005). Transient Structural Ordering of the RNA‐Binding Domain of Carnation Mottle Virus p7 Movement Protein Modulates Nucleic Acid Binding. ChemBioChem, 6(8), 1391–1396. Portico. https://doi.org/10.1002/cbic.200400451

Marcos, J. F., González-Candelas, L., & Zacarías, L. (2005). Involvement of ethylene biosynthesis and perception in the susceptibility of citrus fruits to Penicillium digitatum infection and the accumulation of defence-related mRNAs. Journal of Experimental Botany, 56(418), 2183–2193. https://doi.org/10.1093/jxb/eri218

Rodrigo, M.-J., Marcos, J. F., & Zacarías, L. (2004). Biochemical and Molecular Analysis of Carotenoid Biosynthesis in Flavedo of Orange (Citrus sinensis L.) during Fruit Development and Maturation. Journal of Agricultural and Food Chemistry, 52(22), 6724–6731. https://doi.org/10.1021/jf049607f

Rodrigo, M.-J. (2003). Characterization of Pinalate, a novel Citrus sinensis mutant with a fruit-specific alteration that results in yellow pigmentation and decreased ABA content. Journal of Experimental Botany, 54(383), 727–738. https://doi.org/10.1093/jxb/erg083

López-García, B., Pérez-Payá, E., & Marcos, J. F. (2002). Identification of Novel Hexapeptides Bioactive against Phytopathogenic Fungi through Screening of a Synthetic Peptide Combinatorial Library. Applied and Environmental Microbiology, 68(5), 2453–2460. https://doi.org/10.1128/aem.68.5.2453-2460.2002

Schirra, M., Delogu, G., Cabras, P., Angioni, A., D’hallewin, G., Veyrat, A., Marcos, J. F., & Candelas, L. G. (2002). Complexation of Imazalil with β-Cyclodextrin, Residue Uptake, Persistence, and Activity against Penicillium Decay in Citrus Fruit Following Postharvest Dip Treatments. Journal of Agricultural and Food Chemistry, 50(23), 6790–6797. https://doi.org/10.1021/jf020542v

Cañizares, M. C., Marcos, J. F., & Pallás, V. (2001). Molecular variability of twenty-one geographically distinct isolates of Carnation mottle virus (CarMV) and phylogenetic relationships within the Tombusviridae family. Archives of Virology, 146(10), 2039–2051. https://doi.org/10.1007/s007050170051

López-García, B., González-Candelas, L., Marcos, J. F., & Pérez-Payá, E. (2001). IDENTIFICATION OF A PEPTIDE WITH SPECIFIC ACTIVITY AGAINST FUNGI THAT CAUSE POSTHARVEST DECAY IN FRUITS. Acta Horticulturae, 553, 447–448. https://doi.org/10.17660/actahortic.2001.553.105

López-García, B., González-Candelas, L., Pérez-Payá, E., & Marcos, J. F. (2000). Identification and Characterization of a Hexapeptide with Activity Against Phytopathogenic Fungi That Cause Postharvest Decay in Fruits. Molecular Plant-Microbe Interactions®, 13(8), 837–846. https://doi.org/10.1094/mpmi.2000.13.8.837

Cañizares, M. C., Marcos, J. F., & Pallás, V. (1999). Molecular Characterization of an Almond Isolate of Hop Stunt Viroid (HSVd) and Conditions for Eliminating Spurious Hybridization in its Diagnosis in Almond Samples. European Journal of Plant Pathology, 105(6), 553–558. https://doi.org/10.1023/a:1008794531725

Díez, J., Marcos, J. F., & Pallás, V. (1999). Characterization and in vitro translation analysis of pelargonium flower break virus. Archives of Virology, 144(8), 1627–1637. https://doi.org/10.1007/s007050050616

Cañizares, M. C., Marcos, J. F., & Pallás, V. (1998). STUDIES ON THE INCIDENCE OF HOP STUNT VIROID IN APRICOT TREES (PRUNUS ARMENIACA) BY USING AN EASY AND SHORT EXTRACTION METHOD TO ANALYZE A LARGE NUMBER OF SAMPLES. Acta Horticulturae, 472, 581–586. https://doi.org/10.17660/actahortic.1998.472.77

Ceriani, M. F., Marcos, J. F., Esteban Hopp, H., & Beachy, R. N. (1998). Simultaneous accumulation of multiple viral coat proteins from a TEV-NIa based expression vector. Plant Molecular Biology, 36(2), 239–248. https://doi.org/10.1023/a:1005952001774

Díez, J., Marcos, J. F., & Pallás, V. (1998). Carmovirus Isolation and RNA Extraction. Plant Virology Protocols, 211–217. https://doi.org/10.1385/0-89603-385-6:211

Marcos, J. F., & Beachy, R. N. (1997). Transgenic accumulation of two plant virus coat proteins on a single self-processing polypeptide. Journal of General Virology, 78(7), 1771–1778. https://doi.org/10.1099/0022-1317-78-7-1771

Kofalvi, S. A., Pall√°s, V., Marcos, J. F., Candresse, T., & Ca√±izares, M. C. (1997). Hop stunt viroid (HSVd) sequence variants from Prunus species: evidence for recombination between HSVd isolates. Journal of General Virology, 78(12), 3177–3186. https://doi.org/10.1099/0022-1317-78-12-3177

Aleman, M.-E., Marcos, J. F., Brugidou, C., Beachy, R. N., & Fauquet, C. (1996). The complete nucleotide sequence of yam mosaic virus (Ivory Coast isolate) genomic RNA. Archives of Virology, 141(7), 1259–1278. https://doi.org/10.1007/bf01718829

Astruc, N., Marcos, J. F., Macquaire, G., Candresse, T., & Pallás, V. (1996). Studies on the diagnosis of hop stunt viroid in fruit trees: Identification of new hosts and application of a nucleic acid extraction procedure based on non-organic solvents. European Journal of Plant Pathology, 102(9), 837–846. https://doi.org/10.1007/bf01877053

Marcos, J. F., Beachy, R. N., Houghten, R. A., Blondelle, S. E., & Pérez-Payá, E. (1995). Inhibition of a plant virus infection by analogs of melittin. Proceedings of the National Academy of Sciences, 92(26), 12466–12469. https://doi.org/10.1073/pnas.92.26.12466

Daròs, J. A., Marcos, J. F., Hernández, C., & Flores, R. (1994). Replication of avocado sunblotch viroid: evidence for a symmetric pathway with two rolling circles and hammerhead ribozyme processing. Proceedings of the National Academy of Sciences, 91(26), 12813–12817. https://doi.org/10.1073/pnas.91.26.12813

Marcos, J. F., & Beachy, R. N. (1994). In vitro characterization of a cassette to accumulate multiple proteins through synthesis of a self-processing polypeptide. Plant Molecular Biology, 24(3), 495–503. https://doi.org/10.1007/bf00024117

Marcos, J. F., & Flores, R. (1993). The 5’ end Generated in the in vitro Self-Cleavage Reaction of Avocado Sunblotch Viroid RNAs is Present in Naturally Occurring Linear Viroid Molecules. Journal of General Virology, 74(5), 907–910. https://doi.org/10.1099/0022-1317-74-5-907

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