Circadian oscillations in Trichoderma atroviride and the role of core clock components in secondary metabolism, development, and mycoparasitism against the phytopathogen Botrytis cinerea

Circadian clocks are important for an individual’s fitness, and recent studies have underlined their role in the outcome of biological interactions. However, the relevance of circadian clocks in fungal–fungal interactions remains largely unexplored. We sought to characterize a functional clock in th...

Full description

Bibliographic Details
Main Authors: Marlene Henríquez-Urrutia, Rebecca Spanner, Consuelo Olivares-Yánez, Aldo Seguel-Avello, Rodrigo Pérez-Lara, Hector Guillén-Alonso, Robert Winkler, Alfredo Herrera-Estrella, Paulo Canessa, Luis F Larrondo
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2022-08-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/71358
_version_ 1811205253562892288
author Marlene Henríquez-Urrutia
Rebecca Spanner
Consuelo Olivares-Yánez
Aldo Seguel-Avello
Rodrigo Pérez-Lara
Hector Guillén-Alonso
Robert Winkler
Alfredo Herrera-Estrella
Paulo Canessa
Luis F Larrondo
author_facet Marlene Henríquez-Urrutia
Rebecca Spanner
Consuelo Olivares-Yánez
Aldo Seguel-Avello
Rodrigo Pérez-Lara
Hector Guillén-Alonso
Robert Winkler
Alfredo Herrera-Estrella
Paulo Canessa
Luis F Larrondo
author_sort Marlene Henríquez-Urrutia
collection DOAJ
description Circadian clocks are important for an individual’s fitness, and recent studies have underlined their role in the outcome of biological interactions. However, the relevance of circadian clocks in fungal–fungal interactions remains largely unexplored. We sought to characterize a functional clock in the biocontrol agent Trichoderma atroviride to assess its importance in the mycoparasitic interaction against the phytopathogen Botrytis cinerea. Thus, we confirmed the existence of circadian rhythms in T. atroviride, which are temperature-compensated and modulated by environmental cues such as light and temperature. Nevertheless, the presence of such molecular rhythms appears to be highly dependent on the nutritional composition of the media. Complementation of a clock null (Δfrq) Neurospora crassa strain with the T. atroviride-negative clock component (tafrq) restored core clock function, with the same period observed in the latter fungus, confirming the role of tafrq as a bona fide core clock component. Confrontation assays between wild-type and clock mutant strains of T. atroviride and B. cinerea, in constant light or darkness, revealed an inhibitory effect of light on T. atroviride’s mycoparasitic capabilities. Interestingly, when confrontation assays were performed under light/dark cycles, T. atroviride’s overgrowth capacity was enhanced when inoculations were at dawn compared to dusk. Deleting the core clock-negative element FRQ in B. cinerea, but not in T. atroviride, was vital for the daily differential phenotype, suggesting that the B. cinerea clock has a more significant influence on the result of this interaction. Additionally, we observed that T. atroviride clock components largely modulate development and secondary metabolism in this fungus, including the rhythmic production of distinct volatile organic compounds (VOCs). Thus, this study provides evidence on how clock components impact diverse aspects of T. atroviride lifestyle and how daily changes modulate fungal interactions and dynamics.
first_indexed 2024-04-12T03:27:32Z
format Article
id doaj.art-bd0ea93ff23f49f5a7392fe920f0994c
institution Directory Open Access Journal
issn 2050-084X
language English
last_indexed 2024-04-12T03:27:32Z
publishDate 2022-08-01
publisher eLife Sciences Publications Ltd
record_format Article
series eLife
spelling doaj.art-bd0ea93ff23f49f5a7392fe920f0994c2022-12-22T03:49:38ZengeLife Sciences Publications LtdeLife2050-084X2022-08-011110.7554/eLife.71358Circadian oscillations in Trichoderma atroviride and the role of core clock components in secondary metabolism, development, and mycoparasitism against the phytopathogen Botrytis cinereaMarlene Henríquez-Urrutia0Rebecca Spanner1Consuelo Olivares-Yánez2Aldo Seguel-Avello3Rodrigo Pérez-Lara4Hector Guillén-Alonso5Robert Winkler6Alfredo Herrera-Estrella7Paulo Canessa8Luis F Larrondo9https://orcid.org/0000-0002-8832-7109ANID – Millennium Science Initiative Program - Millennium Institute for Integrative Biology (iBio), Santiago, Chile; Pontificia Universidad Católica de Chile, Biological Sciences Faculty, Molecular Genetics and Microbiology Department, Santiago, ChileANID – Millennium Science Initiative Program - Millennium Institute for Integrative Biology (iBio), Santiago, Chile; Pontificia Universidad Católica de Chile, Biological Sciences Faculty, Molecular Genetics and Microbiology Department, Santiago, ChileANID – Millennium Science Initiative Program - Millennium Institute for Integrative Biology (iBio), Santiago, Chile; Centro de Biotecnología Vegetal, Facultad de Ciencias de la Vida, Universidad Andrés, Santiago, ChileANID – Millennium Science Initiative Program - Millennium Institute for Integrative Biology (iBio), Santiago, Chile; Pontificia Universidad Católica de Chile, Biological Sciences Faculty, Molecular Genetics and Microbiology Department, Santiago, ChileANID – Millennium Science Initiative Program - Millennium Institute for Integrative Biology (iBio), Santiago, Chile; Pontificia Universidad Católica de Chile, Biological Sciences Faculty, Molecular Genetics and Microbiology Department, Santiago, ChileDepartment of Biotechnology and Biochemistry, Cinvestav Unidad Irapuato, Irapuato, MexicoDepartment of Biotechnology and Biochemistry, Cinvestav Unidad Irapuato, Irapuato, MexicoLaboratorio de expresión génica y desarrollo en hongos, Unidad de Genómica Avanzada-LANGEBIO, Irapuato, MexicoANID – Millennium Science Initiative Program - Millennium Institute for Integrative Biology (iBio), Santiago, Chile; Centro de Biotecnología Vegetal, Facultad de Ciencias de la Vida, Universidad Andrés, Santiago, ChileANID – Millennium Science Initiative Program - Millennium Institute for Integrative Biology (iBio), Santiago, Chile; Pontificia Universidad Católica de Chile, Biological Sciences Faculty, Molecular Genetics and Microbiology Department, Santiago, ChileCircadian clocks are important for an individual’s fitness, and recent studies have underlined their role in the outcome of biological interactions. However, the relevance of circadian clocks in fungal–fungal interactions remains largely unexplored. We sought to characterize a functional clock in the biocontrol agent Trichoderma atroviride to assess its importance in the mycoparasitic interaction against the phytopathogen Botrytis cinerea. Thus, we confirmed the existence of circadian rhythms in T. atroviride, which are temperature-compensated and modulated by environmental cues such as light and temperature. Nevertheless, the presence of such molecular rhythms appears to be highly dependent on the nutritional composition of the media. Complementation of a clock null (Δfrq) Neurospora crassa strain with the T. atroviride-negative clock component (tafrq) restored core clock function, with the same period observed in the latter fungus, confirming the role of tafrq as a bona fide core clock component. Confrontation assays between wild-type and clock mutant strains of T. atroviride and B. cinerea, in constant light or darkness, revealed an inhibitory effect of light on T. atroviride’s mycoparasitic capabilities. Interestingly, when confrontation assays were performed under light/dark cycles, T. atroviride’s overgrowth capacity was enhanced when inoculations were at dawn compared to dusk. Deleting the core clock-negative element FRQ in B. cinerea, but not in T. atroviride, was vital for the daily differential phenotype, suggesting that the B. cinerea clock has a more significant influence on the result of this interaction. Additionally, we observed that T. atroviride clock components largely modulate development and secondary metabolism in this fungus, including the rhythmic production of distinct volatile organic compounds (VOCs). Thus, this study provides evidence on how clock components impact diverse aspects of T. atroviride lifestyle and how daily changes modulate fungal interactions and dynamics.https://elifesciences.org/articles/71358Trichoderma atrovirideBotrytis cinereacircadian rhythmsorganismal interactionsphotobiology
spellingShingle Marlene Henríquez-Urrutia
Rebecca Spanner
Consuelo Olivares-Yánez
Aldo Seguel-Avello
Rodrigo Pérez-Lara
Hector Guillén-Alonso
Robert Winkler
Alfredo Herrera-Estrella
Paulo Canessa
Luis F Larrondo
Circadian oscillations in Trichoderma atroviride and the role of core clock components in secondary metabolism, development, and mycoparasitism against the phytopathogen Botrytis cinerea
eLife
Trichoderma atroviride
Botrytis cinerea
circadian rhythms
organismal interactions
photobiology
title Circadian oscillations in Trichoderma atroviride and the role of core clock components in secondary metabolism, development, and mycoparasitism against the phytopathogen Botrytis cinerea
title_full Circadian oscillations in Trichoderma atroviride and the role of core clock components in secondary metabolism, development, and mycoparasitism against the phytopathogen Botrytis cinerea
title_fullStr Circadian oscillations in Trichoderma atroviride and the role of core clock components in secondary metabolism, development, and mycoparasitism against the phytopathogen Botrytis cinerea
title_full_unstemmed Circadian oscillations in Trichoderma atroviride and the role of core clock components in secondary metabolism, development, and mycoparasitism against the phytopathogen Botrytis cinerea
title_short Circadian oscillations in Trichoderma atroviride and the role of core clock components in secondary metabolism, development, and mycoparasitism against the phytopathogen Botrytis cinerea
title_sort circadian oscillations in trichoderma atroviride and the role of core clock components in secondary metabolism development and mycoparasitism against the phytopathogen botrytis cinerea
topic Trichoderma atroviride
Botrytis cinerea
circadian rhythms
organismal interactions
photobiology
url https://elifesciences.org/articles/71358
work_keys_str_mv AT marlenehenriquezurrutia circadianoscillationsintrichodermaatrovirideandtheroleofcoreclockcomponentsinsecondarymetabolismdevelopmentandmycoparasitismagainstthephytopathogenbotrytiscinerea
AT rebeccaspanner circadianoscillationsintrichodermaatrovirideandtheroleofcoreclockcomponentsinsecondarymetabolismdevelopmentandmycoparasitismagainstthephytopathogenbotrytiscinerea
AT consueloolivaresyanez circadianoscillationsintrichodermaatrovirideandtheroleofcoreclockcomponentsinsecondarymetabolismdevelopmentandmycoparasitismagainstthephytopathogenbotrytiscinerea
AT aldoseguelavello circadianoscillationsintrichodermaatrovirideandtheroleofcoreclockcomponentsinsecondarymetabolismdevelopmentandmycoparasitismagainstthephytopathogenbotrytiscinerea
AT rodrigoperezlara circadianoscillationsintrichodermaatrovirideandtheroleofcoreclockcomponentsinsecondarymetabolismdevelopmentandmycoparasitismagainstthephytopathogenbotrytiscinerea
AT hectorguillenalonso circadianoscillationsintrichodermaatrovirideandtheroleofcoreclockcomponentsinsecondarymetabolismdevelopmentandmycoparasitismagainstthephytopathogenbotrytiscinerea
AT robertwinkler circadianoscillationsintrichodermaatrovirideandtheroleofcoreclockcomponentsinsecondarymetabolismdevelopmentandmycoparasitismagainstthephytopathogenbotrytiscinerea
AT alfredoherreraestrella circadianoscillationsintrichodermaatrovirideandtheroleofcoreclockcomponentsinsecondarymetabolismdevelopmentandmycoparasitismagainstthephytopathogenbotrytiscinerea
AT paulocanessa circadianoscillationsintrichodermaatrovirideandtheroleofcoreclockcomponentsinsecondarymetabolismdevelopmentandmycoparasitismagainstthephytopathogenbotrytiscinerea
AT luisflarrondo circadianoscillationsintrichodermaatrovirideandtheroleofcoreclockcomponentsinsecondarymetabolismdevelopmentandmycoparasitismagainstthephytopathogenbotrytiscinerea