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

Published on Mar 7, 2017in Proceedings of the National Academy of Sciences of the United States of America9.58
· DOI :10.1073/pnas.1614864114
Wenfu Mao13
Estimated H-index: 13
(UIUC: University of Illinois at Urbana–Champaign),
Mary A. Schuler54
Estimated H-index: 54
(UIUC: University of Illinois at Urbana–Champaign),
May R. Berenbaum67
Estimated H-index: 67
(UIUC: University of Illinois at Urbana–Champaign)
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.
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References37
Newest
#1Jacob B. Campbell (ASU: Arizona State University)H-Index: 3
#2Rachna Nath (ASU: Arizona State University)H-Index: 2
Last.Jon F. Harrison (ASU: Arizona State University)H-Index: 40
view all 6 authors...
#1Alex J. Guseman (UMD: University of Maryland, College Park)H-Index: 1
#2Kaliah Miller (UMD: University of Maryland, College Park)H-Index: 1
Last.David J. Hawthorne (UMD: University of Maryland, College Park)H-Index: 18
view all 8 authors...
#1Dong Liu (CAS: Chinese Academy of Sciences)H-Index: 3
#2Y. Yuan (CAS: Chinese Academy of Sciences)H-Index: 3
Last.Xinghui Qiu (CAS: Chinese Academy of Sciences)H-Index: 15
view all 4 authors...
#1Wenfu Mao (UIUC: University of Illinois at Urbana–Champaign)H-Index: 13
#2Mary A. Schuler (UIUC: University of Illinois at Urbana–Champaign)H-Index: 54
Last.May R. Berenbaum (UIUC: University of Illinois at Urbana–Champaign)H-Index: 67
view all 3 authors...
#1May R. Berenbaum (UIUC: University of Illinois at Urbana–Champaign)H-Index: 67
#2Reed M. Johnson (OSU: Ohio State University)H-Index: 25
#1Vilma Kaškonienė (VMU: Vytautas Magnus University)H-Index: 10
#2Geralda Ruočkuvienė (VMU: Vytautas Magnus University)H-Index: 1
Last.Audrius Maruška (VMU: Vytautas Magnus University)H-Index: 17
view all 5 authors...
Cited By24
Newest
#1Rafaela Tadei (UFSCar: Federal University of São Carlos)
#2Caio E. C. Domingues (UNESP: Sao Paulo State University)
Last.Elaine C.M. Silva-Zacarin (UFSCar: Federal University of São Carlos)H-Index: 13
view all 6 authors...
#1May R. Berenbaum (UIUC: University of Illinois at Urbana–Champaign)H-Index: 67
#2Ling-Hsiu Liao (UIUC: University of Illinois at Urbana–Champaign)
#1Alberto Prado (INRA: Institut national de la recherche agronomique)H-Index: 1
#2Maryline Pioz (INRA: Institut national de la recherche agronomique)H-Index: 7
Last.Cédric Alaux (INRA: Institut national de la recherche agronomique)H-Index: 25
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