Abstract
The capability to respond to wounding is a process shared by organisms of different kingdoms that can result in the regeneration of whole-body parts or lost structures or organs. Filamentous fungi constitute a rich food source that ensures survival and reproduction of their predators and are therefore continuously exposed to mechanical damage. Nevertheless, our understanding of how fungi respond to wounding and predators is scarce. Fungi like plants and animals respond to injury recognizing Damage- and Microbe-Associated Molecular Patterns (DAMPs/MAMPs) that activate Ca2+ and Mitogen-Activated Protein Kinase dependent signaling for the activation of defense mechanisms. During herbivory, plants, in addition to activating pathways related to injury, activate specific responses to combat their predators. Using a transcriptional approach, we studied the capacity of the filamentous fungus Trichoderma atroviride to activate specific responses to injury and attack by different arthropods. Attack by Drosophila melanogaster inhibited the transcriptional activation of genes required for hyphal regeneration, and the fungal innate immune and chemical defense responses. We also provide mechanistic insight of this inhibition involving components of the D. melanogaster salivary glands that repress the expression of a set of genes and block hyphal regeneration.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
References
Künzler M. How fungi defend themselves against microbial competitors and animal predators. PLoS Pathog. 2018;14:1–10.
Jacobsen RM, Sverdrup-Thygeson A, Kauserud H, Birkemoe T. Revealing hidden insect-fungus interactions; moderately specialized, modular and anti-nested detritivore networks. Proc R Soc B Biol Sci. 2018;285:1–8.
Haney CH, Urbach JM, Ausubel FM. Differences and similarities: innate immunity in plants and animals. Biochem. 2014;36:40–44.
Choi HW, Klessig DF. DAMPs, MAMPs, and NAMPs in plant innate immunity. BMC Plant Biol. 2016;16:1–10.
Henry G, Thonart P. Ongena M. PAMPs, MAMPs, DAMPs and others: an update on the diversity of plant immunity elicitors. Biotechnol Agron Soc Env. 2012;16:257–68.
Amarante-Mendes GP, Adjemian S, Branco LM, Zanetti LC, Weinlich R, Bortoluci KR. Pattern recognition receptors and the host cell death molecular machinery. Front Immunol. 2018;9:1–19.
Walsh D, McCarthy J, O’Driscoll C, Melgar S. Pattern recognition receptors-Molecular orchestrators of inflammation in inflammatory bowel disease. Cytokine Growth Factor Rev. 2013;24:91–104.
Uehling J, Deveau A, Paoletti M. Do fungi have an innate immune response? An NLR-based comparison to plant and animal immune systems. PLoS Pathog. 2017;13:1–8.
Heller J, Clavé C, Gladieux P, Saupe SJ, Louise Glass N. NLR surveillance of essential SEC-9 SNARE proteins induces programmed cell death upon allorecognition in filamentous fungi. Proc Natl Acad Sci U S A. 2018;115:E2292–E2301.
Daskalov A, Heller J, Herzog S, Fleißner A, Glass NL. Molecular mechanisms regulating cell fusion and heterokaryon formation in filamentous fungi. Microbiol Spectr. 2017;5:1–15.
Glass NL, Kaneko I. Fatal attraction: nonself recognition and heterokaryon incompatibility in filamentous fungi. Eukaryot Cell. 2003;2:1–8.
Ipcho S, Sundelin T, Erbs G, Kistler HC, Newman MA, Olsson S. Fungal innate immunity induced by bacterial microbe-associated molecular patterns (MAMPs). G3 Genes Genomes Genet. 2016;6:1585–95.
Lamacchia M, Dyrka W, Breton A, Saupe SJ, Paoletti M. Overlapping Podospora anserina transcriptional responses to bacterial and fungal non-self indicate a multilayered innate immune response. Front Microbiol. 2016;7:1–18.
Medina-Castellanos E, Esquivel-Naranjo EU, Heil M, Herrera-Estrella A. Extracellular ATP activates MAPK and ROS signaling during injury response in the fungus Trichoderma atroviride. Front Plant Sci. 2014;5:1–11.
Medina-Castellanos E, Villalobos-Escobedo JM, Riquelme M, Read ND, Abreu-Goodger C, Herrera-Estrella A. Danger signals activate a putative innate immune system during regeneration in a filamentous fungus. PLoS Genet. 2018;14:1–21.
Paoletti M. Vegetative incompatibility in fungi: from recognition to cell death, whatever does the trick. Fungal Biol Rev. 2016;30:152–62.
Hernández-Oñate MA, Esquivel-Naranjo EU, Mendoza-Mendoza A, Stewart A, Herrera-Estrella AH. An injury-response mechanism conserved across kingdoms determines entry of the fungus Trichoderma atroviride into development. Proc Natl Acad Sci USA 2012;109:14918–23.
Spiteller P. Chemical defense strategies of higher fungi. Chem A Eur J 2008;14:9100–10.
Spiteller P. Chemical ecology of fungi. Nat Prod Rep. 2015;32:971–93.
Trienens M, Keller NP, Rohlfs M. Fruit, flies and filamentous fungi-experimental analysis of animal-microbe competition using Drosophila melanogaster and Aspergillus mould as a model system. Oikos 2010;119:1765–75.
Caballero-Ortiz S, Trienens M, Rohlfs M. Induced fungal resistance to insect grazing: reciprocal fitness consequences and fungal gene expression in the Drosophila-Aspergillus model system. PLoS One. 2013;8:1–10.
Trienens M, Rohlfs M. Insect-fungus interference competition - The potential role of global secondary metabolite regulation, pathway-specific mycotoxin expression and formation of oxylipins. Fungal Ecol. 2012;5:191–9.
Plaza DF, Schmieder SS, Lipzen A, Lindquist E, Künzler M. Identification of a novel nematotoxic protein by challenging the model mushroom Coprinopsis cinerea with a fungivorous nematode. G3 Genes Genomes Genet. 2016;6:87–98.
Bleuler-Martínez S, Butschi A, Garbani M, WÎlti MA, Wohlschlager T, Potthoff E, et al. A lectin-mediated resistance of higher fungi against predators and parasites. Mol Ecol. 2011;20:3056–70.
Atriztán-Hernández K, Moreno-Pedraza A, Winkler R, Markow T, Herrera-Estrella A. Trichoderma atroviride from predator to prey: role of the mitogen-activated protein kinase Tmk3 in fungal chemical defense against fungivory by Drosophila melanogaster larvae. Appl Environ Microbiol. 2019;85:1–15.
Andrews S. FastQC: A quality control tool for high throughput sequence data. 2010. Available online at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc.
Kim D, Langmead B, Salzberg SL. HISAT: a fast spliced aligner with low memory requirements. Nat Methods. 2016;12:357–60.
Anders S, Pyl PT, Huber W. HTSeq-A Python framework to work with high-throughput sequencing data. Bioinformatics 2015;31:166–9.
Robinson MD, McCarthy DJ, Smyth GK. edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2009;26:139–40.
Alexa A, Rahnenfuhrer J topGO: Enrichment analysis for gene ontology. R package version 2.40.0. 2020.
Supek F, Bošnjak M, Škunca N, Šmuc T. Revigo summarizes and visualizes long lists of gene ontology terms. PLoS One. 2011;6:e21800.
Korge G. Larval saliva in Drosophila melanogaster: Production, composition, and relationship to chromosome puffs. Dev Biol. 1977;58:339–55.
Jørgensen HB, Johansson T, Canbäck B, Hedlund K, Tunlid A. Selective foraging of fungi by collembolans in soil. Biol Lett. 2005;1:243–6.
Coolen S, Proietti S, Hickman R, Davila-Olivas NH, Huang PP, Van-Verk M. et al. Transcriptome dynamics of Arabidopsis during sequential biotic and abiotic stresses. Plant J. 2016;86:249–67.
Cohen SP, Leach JE. Abiotic and biotic stresses induce a core transcriptome response in rice. Sci Rep. 2019;9:1–11.
Yong HC, Chang HS, Gupta R, Wang X, Zhu T, Luan S. Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol. 2002;129:661–77.
Ben-Rejeb I, Pastor V, Mauch-Mani B. Plant responses to simultaneous biotic and abiotic stress: molecular mechanisms. Plants 2014;3:458–75.
Caballero-Ortiz S, Trienens M, Pfohl K, Karlovsky P, Holighaus G, Rohlfs M. Phenotypic responses to microbial volatiles render a mold fungus more susceptible to insect damage. Ecol Evol. 2018;8:4328–39.
Farkaš R, Sláma K. Respiratory metabolism of salivary glands during the late larval and prepupal development of Drosophila melanogaster. J Insect Physiol. 2015;81:109–17.
Beckendorf SK, Kafatos FC. Differentiation in the salivary glands of Drosophila melanogaster: characterization of the glue proteins and their developmental appearance. Cell 1976;9:365–73.
Plaza DF, Lin CW, Van Der Velden NSJ, Aebi M, Künzler M. Comparative transcriptomics of the model mushroom Coprinopsis cinerea reveals tissue-specific armories and a conserved circuitry for sexual development. BMC Genomics. 2014;15:1–17.
Lepenies B, Lang R. Lectins and their ligands in shaping immune responses. Front Immunol. 2019;10:1–3.
Van Holle S, Van, Damme JM. Signaling through plant lectins: modulation of plant immunity and beyond. Biochem Soc Trans. 2018;46:217–33.
Johannes L, Jacob R, Leffler H. Galectins at a glance. J Cell Sci. 2018;131:1–9.
Cui M, Wang Z, Chen K, Shah AM, Tan W, Duan L, et al. Dynamic transcriptional responses to injury of regenerative and non-regenerative cardiomyocytes revealed by single-nucleus RNA sequencing. Dev Cell. 2020;53:102–16.
Niethammer P. The early wound signals. Curr Opin Genet Dev. 2016;40:17–22.
Enyedi B, Niethammer P. Mechanisms of epithelial wound detection. Trends Cell Biol. 2015;25:398–407.
Rieger S, Sagasti A. Hydrogen peroxide promotes injury-induced peripheral sensory axon regeneration in the Zebrafish skin. PLoS Biol. 2011;9:1–12.
Love NR, Chen Y, Ishibashi S, Kritsiligkou P, Lea R, Koh Y, et al. Amputation-induced reactive oxygen species (ROS) are required for successful Xenopus tadpole tail regeneration. Nat Cell Biol. 2013;15:222–8.
Weavers H, Wood W, Martin P. Injury activates a dynamic cytoprotective network to confer stress resilience and drive repair. Curr Biol. 2019;29:3851–62.
Barghouti PG, Thiruvalluvan M, LeGro M, Oviedo NJ. DNA damage and tissue repair: what we can learn from planaria. Semin Cell Dev Biol. 2018;87:145–59.
Rohlfs M. Fungal secondary metabolism in the light of animal–fungus interactions: from mechanism to ecological function. In: Zeilinger S, Martín JF, García-Estrada C (eds). Biosynthesis and molecular genetics of fungal secondary metabolites, Fungal Biology. (Springer, New York, NY, 2015) Vol 2. pp 177–98.
Gaffoor I, Brown DW, Plattner R, Proctor RH, Qi W, Trail F. Functional analysis of the polyketide synthase genes in the filamentous fungus Gibberella zeae (Anamorph Fusarium graminearum). Eukaryot Cell. 2005;4:1926–33.
Oide S, Turgeon BG. Natural roles of non-ribosomal peptide metabolites in fungi. Mycoscience 2020;61:101–10.
Fujii I. Functional analysis of fungal polyketide biosynthesis genes. J Antibiot. 2010;63:207–18.
Buzgariu W, Wenger Y, Tcaciuc N, Catunda-Lemos AP, Galliot B. Impact of cycling cells and cell cycle regulation on Hydra regeneration. Dev Biol . 2018;433:240–25.
Heber-Katz E, Zhang Y, Bedelbaeva K, Song F, Chen X, Stocum DL. Cell cycle regulation and regeneration. In: Heber-Katz E, Stocum D (eds) New perspectives in regeneration. Current Topics in Microbiology and Immunology. (Springer, Berlin, Heidelberg, 2012) Vol 367. pp 253–76.
Katz ME, Braunberger K, Yi G, Cooper S, Nonhebelet HM, Gondro C. Ap53-like transcription factor similar to Ndt80 controls the response to nutrient stress in the filamentous fungus, Aspergillus nidulans. F1000 Res. 2013;2:72.
Katz ME, Cooper S. Extreme diversity in the regulation of Ndt80-like transcription factors in fungi. G3 Genes Genomes Genet. 2015;5:2783–92.
Hutchison EA, Glass NL. Meiotic regulators Ndt80 and Ime2 have different roles in Saccharomyces and Neurospora. Genetics 2010;185:1271–82.
Dementhon K, Iyer G, Glass NL. VIB-1 is required for expression of genes necessary for programmed cell death in Neurospora. Eukaryot Cell. 2006;5:2161–73.
Li N, Kunitake E, Endo Y, Aoyama M, Kanamaru K, Kimura M, et al. Involvement of an SRF-MADS protein McmA in regulation of extracellular enzyme production and asexual/sexual development in Aspergillus nidulans. Biosci Biotechnol Biochem. 2016;80:1820–8.
Szilagyi Z, Batta G, Enczi K, Sipiczki M. Characterization of two novel fork-head gene homologues of Schizosaccharomyces pombe: their involvement in cell cycle and sexual differentiation. Gene 2005;348:101–9.
Balázs A, Pócsi I, Hamari Z, Leiter E, Emri T, Miskei M, et al. AtfA bZIP-type transcription factor regulates oxidative and osmotic stress responses in Aspergillus nidulans. Mol Genet Genomics. 2010;283:289–303.
Acknowledgements
We thank Pedro Martínez-Hernández and Nestor Nazario-Yepiz for technical assistance. We also wish to thank Dr. Therese Markow for critical reading of the manuscript and providing D. melanogaster and, José Palacios-Vargas and Blanca Estela Mejia-Recamier for providing the collembollan used in this study. This work was support in full by Cinvestav institutional funds.
Author information
Authors and Affiliations
Contributions
KA-H carried out the experiments, analyzed data, and contributed to the experimental design. AH-E supervised K A-H, designed experiments, and obtained financial support. AH-E and KA-H wrote the manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Rights and permissions
About this article
Cite this article
Atriztán-Hernández, K., Herrera-Estrella, A. Drosophila attack inhibits hyphal regeneration and defense mechanisms activation for the fungus Trichoderma atroviride. ISME J 16, 149–158 (2022). https://doi.org/10.1038/s41396-021-01068-9
Received:
Revised:
Accepted:
Published:
Version of record:
Issue date:
DOI: https://doi.org/10.1038/s41396-021-01068-9


