Skip to main content
  • Submit
  • About
    • Editorial Board
    • PNAS Staff
    • FAQ
    • Accessibility Statement
    • Rights and Permissions
    • Site Map
  • Contact
  • Journal Club
  • Subscribe
    • Subscription Rates
    • Subscriptions FAQ
    • Open Access
    • Recommend PNAS to Your Librarian
  • Log in
  • My Cart

Main menu

  • Home
  • Articles
    • Current
    • Special Feature Articles - Most Recent
    • Special Features
    • Colloquia
    • Collected Articles
    • PNAS Classics
    • List of Issues
  • Front Matter
  • News
    • For the Press
    • This Week In PNAS
    • PNAS in the News
  • Podcasts
  • Authors
    • Information for Authors
    • Editorial and Journal Policies
    • Submission Procedures
    • Fees and Licenses
  • Submit
  • About
    • Editorial Board
    • PNAS Staff
    • FAQ
    • Accessibility Statement
    • Rights and Permissions
    • Site Map
  • Contact
  • Journal Club
  • Subscribe
    • Subscription Rates
    • Subscriptions FAQ
    • Open Access
    • Recommend PNAS to Your Librarian

User menu

  • Log in
  • My Cart

Search

  • Advanced search
Home
Home

Advanced Search

  • Home
  • Articles
    • Current
    • Special Feature Articles - Most Recent
    • Special Features
    • Colloquia
    • Collected Articles
    • PNAS Classics
    • List of Issues
  • Front Matter
  • News
    • For the Press
    • This Week In PNAS
    • PNAS in the News
  • Podcasts
  • Authors
    • Information for Authors
    • Editorial and Journal Policies
    • Submission Procedures
    • Fees and Licenses

New Research In

Physical Sciences

Featured Portals

  • Physics
  • Chemistry
  • Sustainability Science

Articles by Topic

  • Applied Mathematics
  • Applied Physical Sciences
  • Astronomy
  • Computer Sciences
  • Earth, Atmospheric, and Planetary Sciences
  • Engineering
  • Environmental Sciences
  • Mathematics
  • Statistics

Social Sciences

Featured Portals

  • Anthropology
  • Sustainability Science

Articles by Topic

  • Economic Sciences
  • Environmental Sciences
  • Political Sciences
  • Psychological and Cognitive Sciences
  • Social Sciences

Biological Sciences

Featured Portals

  • Sustainability Science

Articles by Topic

  • Agricultural Sciences
  • Anthropology
  • Applied Biological Sciences
  • Biochemistry
  • Biophysics and Computational Biology
  • Cell Biology
  • Developmental Biology
  • Ecology
  • Environmental Sciences
  • Evolution
  • Genetics
  • Immunology and Inflammation
  • Medical Sciences
  • Microbiology
  • Neuroscience
  • Pharmacology
  • Physiology
  • Plant Biology
  • Population Biology
  • Psychological and Cognitive Sciences
  • Sustainability Science
  • Systems Biology
Research Article

Disruption of quercetin metabolism by fungicide affects energy production in honey bees (Apis mellifera)

Wenfu Mao, Mary A. Schuler, and May R. Berenbaum
PNAS March 7, 2017 114 (10) 2538-2543; first published February 13, 2017; https://doi.org/10.1073/pnas.1614864114
Wenfu Mao
aDepartment of Entomology, University of Illinois at Urbana–Champaign, Urbana, IL 61801;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Mary A. Schuler
bDepartment of Cell and Developmental Biology, University of Illinois at Urbana–Champaign, Urbana, IL 61801
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
May R. Berenbaum
aDepartment of Entomology, University of Illinois at Urbana–Champaign, Urbana, IL 61801;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • For correspondence: maybe@illinois.edu
  1. Contributed by May R. Berenbaum, January 6, 2017 (sent for review September 7, 2016; reviewed by Zachary Y. Huang and Blair Siegfried)

This article has a Correction. Please see:

  • Correction to Supporting Information for Mao et al., Disruption of quercetin metabolism by fungicide affects energy production in honey bees (Apis mellifera) - June 26, 2017
  • Article
  • Figures & SI
  • Info & Metrics
  • PDF
Loading

Significance

The western honey bee, Apis mellifera, provides essential crop pollination services, but for 10 years, US beekeepers have experienced substantial colony losses. Although insecticides have been implicated in these losses, triazole fungicides affect bees by inhibiting cytochrome P450 monooxygenases that detoxify insecticides. These enzymes also detoxify phytochemicals, including the flavonol quercetin, in their nectar- and pollen-based diet. RNA-Seq analysis of bee larvae consuming quercetin revealed that it down-regulates multiple mitochondrion-related nuclear genes involved in energy production. Bees consuming quercetin together with the triazole myclobutanil produce less thoracic ATP and thus less energy for flight muscles. Therefore, agricultural use of triazole fungicides in combination with insecticides can potentially harm bees by compromising their capacity to extract sufficient energy from their natural diet.

Abstract

Cytochrome P450 monooxygenases (P450) in the honey bee, Apis mellifera, detoxify phytochemicals in honey and pollen. The flavonol quercetin is found ubiquitously and abundantly in pollen and frequently at lower concentrations in honey. Worker jelly consumed during the first 3 d of larval development typically contains flavonols at very low levels, however. RNA-Seq analysis of gene expression in neonates reared for three days on diets with and without quercetin revealed that, in addition to up-regulating multiple detoxifying P450 genes, quercetin is a negative transcriptional regulator of mitochondrion-related nuclear genes and genes encoding subunits of complexes I, III, IV, and V in the oxidative phosphorylation pathway. Thus, a consequence of inefficient metabolism of this phytochemical may be compromised energy production. Several P450s metabolize quercetin in adult workers. Docking in silico of 121 pesticide contaminants of American hives into the active pocket of CYP9Q1, a broadly substrate-specific P450 with high quercetin-metabolizing activity, identified six triazole fungicides, all fungal P450 inhibitors, that dock in the catalytic site. In adults fed combinations of quercetin and the triazole myclobutanil, the expression of five of six mitochondrion-related nuclear genes was down-regulated. Midgut metabolism assays verified that adult bees consuming quercetin with myclobutanil metabolized less quercetin and produced less thoracic ATP, the energy source for flight muscles. Although fungicides lack acute toxicity, they may influence bee health by interfering with quercetin detoxification, thereby compromising mitochondrial regeneration and ATP production. Thus, agricultural use of triazole fungicides may put bees at risk of being unable to extract sufficient energy from their natural food.

  • Apis mellifera
  • cytochrome P450
  • flavonol
  • mitochondria
  • myclobutanil

Footnotes

  • ↵1To whom correspondence should be addressed. Email: maybe{at}illinois.edu.
  • Author contributions: W.M., M.A.S., and M.R.B. designed research; W.M. performed research; W.M. and M.R.B. analyzed data; and W.M., M.A.S., and M.R.B. wrote the paper.

  • Reviewers: Z.Y.H., Michigan State University; and B.S., University of Florida–Gainesville.

  • The authors declare no conflict of interest.

  • Data deposition: The data reported in this paper have been deposited in the Gene Expression Omnibus (GEO) database, www.ncbi.nlm.nih.gov/geo (accession no. GSE83437).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1614864114/-/DCSupplemental.

View Full Text
PreviousNext
Back to top
Article Alerts
Email Article

Thank you for your interest in spreading the word on PNAS.

NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.

Enter multiple addresses on separate lines or separate them with commas.
Disruption of quercetin metabolism by fungicide affects energy production in honey bees (Apis mellifera)
(Your Name) has sent you a message from PNAS
(Your Name) thought you would like to see the PNAS web site.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Citation Tools
Flavonol–fungicide interactions in bees
Wenfu Mao, Mary A. Schuler, May R. Berenbaum
Proceedings of the National Academy of Sciences Mar 2017, 114 (10) 2538-2543; DOI: 10.1073/pnas.1614864114

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Request Permissions
Share
Flavonol–fungicide interactions in bees
Wenfu Mao, Mary A. Schuler, May R. Berenbaum
Proceedings of the National Academy of Sciences Mar 2017, 114 (10) 2538-2543; DOI: 10.1073/pnas.1614864114
Digg logo Reddit logo Twitter logo Facebook logo Google logo Mendeley logo
  • Tweet Widget
  • Facebook Like
  • Mendeley logo Mendeley
Proceedings of the National Academy of Sciences: 114 (10)
Table of Contents

Submit

Sign up for Article Alerts

Article Classifications

  • Biological Sciences
  • Agricultural Sciences

Jump to section

  • Article
    • Abstract
    • Results
    • Discussion
    • Materials and Methods
    • Acknowledgments
    • Footnotes
    • References
  • Figures & SI
  • Info & Metrics
  • PDF

You May Also be Interested in

Abstract depiction of a guitar and musical note
Science & Culture: At the nexus of music and medicine, some see disease treatments
Although the evidence is still limited, a growing body of research suggests music may have beneficial effects for diseases such as Parkinson’s.
Image credit: Shutterstock/agsandrew.
Large piece of gold
News Feature: Tracing gold's cosmic origins
Astronomers thought they’d finally figured out where gold and other heavy elements in the universe came from. In light of recent results, they’re not so sure.
Image credit: Science Source/Tom McHugh.
Dancers in red dresses
Journal Club: Friends appear to share patterns of brain activity
Researchers are still trying to understand what causes this strong correlation between neural and social networks.
Image credit: Shutterstock/Yeongsik Im.
Yellow emoticons
Learning the language of facial expressions
Aleix Martinez explains why facial expressions often are not accurate indicators of emotion.
Listen
Past PodcastsSubscribe
Goats standing in a pin
Transplantation of sperm-producing stem cells
CRISPR-Cas9 gene editing can improve the effectiveness of spermatogonial stem cell transplantation in mice and livestock, a study finds.
Image credit: Jon M. Oatley.

Similar Articles

Site Logo
Powered by HighWire
  • Submit Manuscript
  • Twitter
  • Facebook
  • RSS Feeds
  • Email Alerts

Articles

  • Current Issue
  • Special Feature Articles – Most Recent
  • List of Issues

PNAS Portals

  • Anthropology
  • Chemistry
  • Classics
  • Front Matter
  • Physics
  • Sustainability Science
  • Teaching Resources

Information

  • Authors
  • Editorial Board
  • Reviewers
  • Librarians
  • Press
  • Site Map
  • PNAS Updates

Feedback    Privacy/Legal

Copyright © 2021 National Academy of Sciences. Online ISSN 1091-6490