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Title: Amino Acid Change in an Orchid Desaturase Enables Mimicry of the Pollinator’s Sex Pheromone

Abstract

Here, we show that mimicry illustrates the power of selection to produce phenotypic convergence in biology. A striking example is the imitation of female insects by plants that are pollinated by sexual deception of males of the same insect species. This involves mimicry of visual, tactile, and chemical signals of females, especially their sex pheromones. The Mediterranean orchid Ophrys exaltata employs chemical mimicry of cuticular hydrocarbons, particularly the 7-alkenes, in an insect sex pheromone to attract and elicit mating behavior in its pollinators, males of the cellophane bee Colletes cunicularius. A difference in alkene double-bond positions is responsible for reproductive isolation between O. exaltata and closely related species, such as O. sphegodes. We show that these 7-alkenes are likely determined by the action of the stearoyl-acyl-carrier-protein desaturase (SAD) homolog SAD5. After gene duplication, changes in subcellular localization relative to the ancestral housekeeping desaturase may have allowed proto-SAD5’s reaction products to undergo further biosynthesis to both 7- and 9-alkenes. Such ancestral coproduction of two alkene classes may have led to pollinator-mediated deleterious pleiotropy. Despite possible evolutionary intermediates with reduced activity, amino acid changes at the bottom of the substrate-binding cavity have conferred enzyme specificity for 7-alkene biosynthesis by preventing the bindingmore » of longer-chained fatty acid (FA) precursors by the enzyme. In conclusion, this change in desaturase function enabled the orchid to perfect its chemical mimicry of pollinator sex pheromones by escape from deleterious pleiotropy, supporting a role of pleiotropy in determining the possible trajectories of adaptive evolution.« less

Authors:
; ; ; ; ;
Publication Date:
Research Org.:
Brookhaven National Lab. (BNL), Upton, NY (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1361703
Alternate Identifier(s):
OSTI ID: 1326867; OSTI ID: 1335436
Report Number(s):
BNL-112099-2016-JA
Journal ID: ISSN 0960-9822; S0960982216303402; PII: S0960982216303402
Grant/Contract Number:  
KC0304000; SC0012704; 31003A_130796; 31003A_141245
Resource Type:
Published Article
Journal Name:
Current Biology
Additional Journal Information:
Journal Name: Current Biology Journal Volume: 26 Journal Issue: 11; Journal ID: ISSN 0960-9822
Publisher:
Elsevier
Country of Publication:
United Kingdom
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Sedeek, Khalid E. M., Whittle, Edward, Guthörl, Daniela, Grossniklaus, Ueli, Shanklin, John, and Schlüter, Philipp M. Amino Acid Change in an Orchid Desaturase Enables Mimicry of the Pollinator’s Sex Pheromone. United Kingdom: N. p., 2016. Web. https://doi.org/10.1016/j.cub.2016.04.018.
Sedeek, Khalid E. M., Whittle, Edward, Guthörl, Daniela, Grossniklaus, Ueli, Shanklin, John, & Schlüter, Philipp M. Amino Acid Change in an Orchid Desaturase Enables Mimicry of the Pollinator’s Sex Pheromone. United Kingdom. https://doi.org/10.1016/j.cub.2016.04.018
Sedeek, Khalid E. M., Whittle, Edward, Guthörl, Daniela, Grossniklaus, Ueli, Shanklin, John, and Schlüter, Philipp M. Wed . "Amino Acid Change in an Orchid Desaturase Enables Mimicry of the Pollinator’s Sex Pheromone". United Kingdom. https://doi.org/10.1016/j.cub.2016.04.018.
@article{osti_1361703,
title = {Amino Acid Change in an Orchid Desaturase Enables Mimicry of the Pollinator’s Sex Pheromone},
author = {Sedeek, Khalid E. M. and Whittle, Edward and Guthörl, Daniela and Grossniklaus, Ueli and Shanklin, John and Schlüter, Philipp M.},
abstractNote = {Here, we show that mimicry illustrates the power of selection to produce phenotypic convergence in biology. A striking example is the imitation of female insects by plants that are pollinated by sexual deception of males of the same insect species. This involves mimicry of visual, tactile, and chemical signals of females, especially their sex pheromones. The Mediterranean orchid Ophrys exaltata employs chemical mimicry of cuticular hydrocarbons, particularly the 7-alkenes, in an insect sex pheromone to attract and elicit mating behavior in its pollinators, males of the cellophane bee Colletes cunicularius. A difference in alkene double-bond positions is responsible for reproductive isolation between O. exaltata and closely related species, such as O. sphegodes. We show that these 7-alkenes are likely determined by the action of the stearoyl-acyl-carrier-protein desaturase (SAD) homolog SAD5. After gene duplication, changes in subcellular localization relative to the ancestral housekeeping desaturase may have allowed proto-SAD5’s reaction products to undergo further biosynthesis to both 7- and 9-alkenes. Such ancestral coproduction of two alkene classes may have led to pollinator-mediated deleterious pleiotropy. Despite possible evolutionary intermediates with reduced activity, amino acid changes at the bottom of the substrate-binding cavity have conferred enzyme specificity for 7-alkene biosynthesis by preventing the binding of longer-chained fatty acid (FA) precursors by the enzyme. In conclusion, this change in desaturase function enabled the orchid to perfect its chemical mimicry of pollinator sex pheromones by escape from deleterious pleiotropy, supporting a role of pleiotropy in determining the possible trajectories of adaptive evolution.},
doi = {10.1016/j.cub.2016.04.018},
journal = {Current Biology},
number = 11,
volume = 26,
place = {United Kingdom},
year = {2016},
month = {6}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1016/j.cub.2016.04.018

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Cited by: 6 works
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Works referenced in this record:

    Works referencing / citing this record:

    Duplication and selection in β-ketoacyl-ACP synthase gene lineages in the sexually deceptive Chiloglottis (Orchidaceace)
    journal, February 2019

    • Wong, Darren C. J.; Amarasinghe, Ranamalie; Falara, Vasiliki
    • Annals of Botany, Vol. 123, Issue 6
    • DOI: 10.1093/aob/mcz013

    Duplication and selection in β-ketoacyl-ACP synthase gene lineages in the sexually deceptive Chiloglottis (Orchidaceace)
    journal, February 2019

    • Wong, Darren C. J.; Amarasinghe, Ranamalie; Falara, Vasiliki
    • Annals of Botany, Vol. 123, Issue 6
    • DOI: 10.1093/aob/mcz013

    Diversification in evolutionary arenas—Assessment and synthesis
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    • Nürk, Nicolai M.; Linder, H. Peter; Onstein, Renske E.
    • Ecology and Evolution
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    The magic of flowers or: speciation genes and where to find them
    journal, November 2018

    • Schlüter, Philipp M.
    • American Journal of Botany, Vol. 105, Issue 12
    • DOI: 10.1002/ajb2.1193

    Floral scent and species divergence in a pair of sexually deceptive orchids
    journal, June 2017

    • Gervasi, Daniel D. L.; Selosse, Marc-Andre; Sauve, Mathieu
    • Ecology and Evolution, Vol. 7, Issue 15
    • DOI: 10.1002/ece3.3147

    Molecular mechanisms of adaptation and speciation: why do we need an integrative approach?
    journal, May 2016

    • Byers, Kelsey J. R. P.; Xu, Shuqing; Schlüter, Philipp M.
    • Molecular Ecology, Vol. 26, Issue 1
    • DOI: 10.1111/mec.13678

    Identification of (Z)-8-Heptadecene and n-Pentadecane as Electrophysiologically Active Compounds in Ophrys insectifera and Its Argogorytes Pollinator
    journal, January 2020

    • Bohman, Björn; Weinstein, Alyssa M.; Mozuraitis, Raimondas
    • International Journal of Molecular Sciences, Vol. 21, Issue 2
    • DOI: 10.3390/ijms21020620