Secondary metabolites of Hülle cells mediate protection of fungal reproductive and overwintering structures against fungivorous animals

Publikation: Beitrag in Fachzeitschrift › Artikel › Forschung › Peer-Review

Autoren

  • Li Liu
  • Christoph Sasse
  • Benedict Dirnberger
  • Oliver Valerius
  • Eniko Fekete-Szuecs
  • Rebekka Harting
  • Daniela E. Nordzieke
  • Stefanie Poeggeler
  • Petr Karlovsky
  • Jennifer Gerke
  • Gerhard H. Braus

Externe Organisationen

  • Georg-August-Universität Göttingen
Forschungs-netzwerk anzeigen

Details

OriginalspracheEnglisch
Aufsatznummere68058
FachzeitschriftELIFE
Jahrgang10
PublikationsstatusVeröffentlicht - 12 Okt. 2021
Extern publiziertJa

Abstract

Fungal Hülle cells with nuclear storage and developmental backup functions are reminiscent of multipotent stem cells. In the soil, Hülle cells nurse the overwintering fruiting bodies of Aspergillus nidulans. The genome of A. nidulans harbors genes for the biosynthesis of xanthones. We show that enzymes and metabolites of this biosynthetic pathway accumulate in Hülle cells under the control of the regulatory velvet complex, which coordinates development and secondary metabolism. Deletion strains blocked in the conversion of anthraquinones to xanthones accumulate emodins and are delayed in maturation and growth of fruiting bodies. Emodin represses fruiting body and resting structure formation in other fungi. Xanthones are not required for sexual development but exert antifeedant effects on fungivorous animals such as springtails and woodlice. Our findings reveal a novel role of Hülle cells in establishing secure niches for A. nidulans by accumulating metabolites with antifeedant activity that protect reproductive structures from animal predators.

ASJC Scopus Sachgebiete

Zitieren

Secondary metabolites of Hülle cells mediate protection of fungal reproductive and overwintering structures against fungivorous animals. / Liu, Li; Sasse, Christoph; Dirnberger, Benedict et al.
in: ELIFE, Jahrgang 10, e68058, 12.10.2021.

Publikation: Beitrag in Fachzeitschrift › Artikel › Forschung › Peer-Review

Liu, L, Sasse, C, Dirnberger, B, Valerius, O, Fekete-Szuecs, E, Harting, R, Nordzieke, DE, Poeggeler, S, Karlovsky, P, Gerke, J & Braus, GH 2021, 'Secondary metabolites of Hülle cells mediate protection of fungal reproductive and overwintering structures against fungivorous animals', ELIFE, Jg. 10, e68058. https://doi.org/10.7554/eLife.68058
Liu, L., Sasse, C., Dirnberger, B., Valerius, O., Fekete-Szuecs, E., Harting, R., Nordzieke, D. E., Poeggeler, S., Karlovsky, P., Gerke, J., & Braus, G. H. (2021). Secondary metabolites of Hülle cells mediate protection of fungal reproductive and overwintering structures against fungivorous animals. ELIFE, 10, Artikel e68058. https://doi.org/10.7554/eLife.68058
Liu L, Sasse C, Dirnberger B, Valerius O, Fekete-Szuecs E, Harting R et al. Secondary metabolites of Hülle cells mediate protection of fungal reproductive and overwintering structures against fungivorous animals. ELIFE. 2021 Okt 12;10:e68058. doi: 10.7554/eLife.68058
Download
@article{2f66dbbccbaf473480f1c2544abe1ca5,
title = "Secondary metabolites of H{\"u}lle cells mediate protection of fungal reproductive and overwintering structures against fungivorous animals",
abstract = "Fungal H{\"u}lle cells with nuclear storage and developmental backup functions are reminiscent of multipotent stem cells. In the soil, H{\"u}lle cells nurse the overwintering fruiting bodies of Aspergillus nidulans. The genome of A. nidulans harbors genes for the biosynthesis of xanthones. We show that enzymes and metabolites of this biosynthetic pathway accumulate in H{\"u}lle cells under the control of the regulatory velvet complex, which coordinates development and secondary metabolism. Deletion strains blocked in the conversion of anthraquinones to xanthones accumulate emodins and are delayed in maturation and growth of fruiting bodies. Emodin represses fruiting body and resting structure formation in other fungi. Xanthones are not required for sexual development but exert antifeedant effects on fungivorous animals such as springtails and woodlice. Our findings reveal a novel role of H{\"u}lle cells in establishing secure niches for A. nidulans by accumulating metabolites with antifeedant activity that protect reproductive structures from animal predators.",
keywords = "Hulle cells, sexual development, secondary metabolites, xanthones, emodin, Aspergillus nidulans, Verticillium, Sordaria macrospora, Folsomia candida, Trichorhina tomentosa, Tenebrio molitor",
author = "Li Liu and Christoph Sasse and Benedict Dirnberger and Oliver Valerius and Eniko Fekete-Szuecs and Rebekka Harting and Nordzieke, {Daniela E.} and Stefanie Poeggeler and Petr Karlovsky and Jennifer Gerke and Braus, {Gerhard H.}",
note = "Funding information: We thank Verena Gro{\ss}e, Nicole Scheiter, Gertrud Stahlhut, and Ruth Pilot for technical assistance, Kerstin Schmitt and Miriam Kolog Gulko for preparing protein digestion solutions and proteome data discussions. We acknowledge support by the doctoral programs of G{\"o}ttinger Graduiertenzentrum f{\"u}r Neurowissenschaften, Biophysik und Molekulare Biowissenschaften (GGNB) (University of G{\"o}ttingen), the China Scholarship Council (CSC), and the European Union{\textquoteright}s Seventh Framework Programme FP7/2007-2013 (grant agreement 607332). Funding was provided by the German Research Council to GHB (DFG grant BR 1502/19–1).",
year = "2021",
month = oct,
day = "12",
doi = "10.7554/eLife.68058",
language = "English",
volume = "10",
journal = "ELIFE",
issn = "2050-084X",
publisher = "eLife Sciences Publications",

}

Download

TY - JOUR

T1 - Secondary metabolites of Hülle cells mediate protection of fungal reproductive and overwintering structures against fungivorous animals

AU - Liu, Li

AU - Sasse, Christoph

AU - Dirnberger, Benedict

AU - Valerius, Oliver

AU - Fekete-Szuecs, Eniko

AU - Harting, Rebekka

AU - Nordzieke, Daniela E.

AU - Poeggeler, Stefanie

AU - Karlovsky, Petr

AU - Gerke, Jennifer

AU - Braus, Gerhard H.

N1 - Funding information: We thank Verena Große, Nicole Scheiter, Gertrud Stahlhut, and Ruth Pilot for technical assistance, Kerstin Schmitt and Miriam Kolog Gulko for preparing protein digestion solutions and proteome data discussions. We acknowledge support by the doctoral programs of Göttinger Graduiertenzentrum für Neurowissenschaften, Biophysik und Molekulare Biowissenschaften (GGNB) (University of Göttingen), the China Scholarship Council (CSC), and the European Union’s Seventh Framework Programme FP7/2007-2013 (grant agreement 607332). Funding was provided by the German Research Council to GHB (DFG grant BR 1502/19–1).

PY - 2021/10/12

Y1 - 2021/10/12

N2 - Fungal Hülle cells with nuclear storage and developmental backup functions are reminiscent of multipotent stem cells. In the soil, Hülle cells nurse the overwintering fruiting bodies of Aspergillus nidulans. The genome of A. nidulans harbors genes for the biosynthesis of xanthones. We show that enzymes and metabolites of this biosynthetic pathway accumulate in Hülle cells under the control of the regulatory velvet complex, which coordinates development and secondary metabolism. Deletion strains blocked in the conversion of anthraquinones to xanthones accumulate emodins and are delayed in maturation and growth of fruiting bodies. Emodin represses fruiting body and resting structure formation in other fungi. Xanthones are not required for sexual development but exert antifeedant effects on fungivorous animals such as springtails and woodlice. Our findings reveal a novel role of Hülle cells in establishing secure niches for A. nidulans by accumulating metabolites with antifeedant activity that protect reproductive structures from animal predators.

AB - Fungal Hülle cells with nuclear storage and developmental backup functions are reminiscent of multipotent stem cells. In the soil, Hülle cells nurse the overwintering fruiting bodies of Aspergillus nidulans. The genome of A. nidulans harbors genes for the biosynthesis of xanthones. We show that enzymes and metabolites of this biosynthetic pathway accumulate in Hülle cells under the control of the regulatory velvet complex, which coordinates development and secondary metabolism. Deletion strains blocked in the conversion of anthraquinones to xanthones accumulate emodins and are delayed in maturation and growth of fruiting bodies. Emodin represses fruiting body and resting structure formation in other fungi. Xanthones are not required for sexual development but exert antifeedant effects on fungivorous animals such as springtails and woodlice. Our findings reveal a novel role of Hülle cells in establishing secure niches for A. nidulans by accumulating metabolites with antifeedant activity that protect reproductive structures from animal predators.

KW - Hulle cells

KW - sexual development

KW - secondary metabolites

KW - xanthones

KW - emodin

KW - Aspergillus nidulans

KW - Verticillium

KW - Sordaria macrospora

KW - Folsomia candida

KW - Trichorhina tomentosa

KW - Tenebrio molitor

UR - http://www.scopus.com/inward/record.url?scp=85118210515&partnerID=8YFLogxK

U2 - 10.7554/eLife.68058

DO - 10.7554/eLife.68058

M3 - Article

VL - 10

JO - ELIFE

JF - ELIFE

SN - 2050-084X

M1 - e68058

ER -