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Disruption of a horizontally transferred phytoene desaturase abolishes carotenoid accumulation and diapause in Tetranychus urticae

Astrid Bryon UGent, Andre H Kurlovs, Wannes Dermauw UGent, Robert Greenhalgh, Maria Riga, Miodrag Grbić, Luc Tirry UGent, Masahiro Osakabe, John Vontas, Richard M Clark, et al. (2017) PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 114(29). p.E5871-E5880
abstract
Carotenoids underlie many of the vibrant yellow, orange, and red colors in animals, and are involved in processes ranging from vision to protection from stresses. Most animals acquire carotenoids from their diets because de novo synthesis of carotenoids is primarily limited to plants and some bacteria and fungi. Recently, sequencing projects in aphids and adelgids, spider mites, and gall midges identified genes with homology to fungal sequences encoding de novo carotenoid biosynthetic proteins like phytoene desaturase. The finding of horizontal gene transfers of carotenoid biosynthetic genes to three arthropod lineages was unprecedented; however, the relevance of the transfers for the arthropods that acquired them has remained largely speculative, which is especially true for spider mites that feed on plant cell contents, a known source of carotenoids. Pigmentation in spider mites results solely from carotenoids. Using a combination of genetic approaches, we show that mutations in a single horizontally transferred phytoene desaturase result in complete albinism in the two-spotted spider mite, Tetranychus urticae, as well as in the citrus red mite, Panonychus citri. Further, we show that phytoene desaturase activity is essential for photoperiodic induction of diapause in an overwintering strain of T. urticae, consistent with a role for this enzyme in provisioning provitamin A carotenoids required for light perception. Carotenoid biosynthetic genes of fungal origin have therefore enabled some mites to forgo dietary carotenoids, with endogenous synthesis underlying their intense pigmentation and ability to enter diapause, a key to the global distribution of major spider mite pests of agriculture.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
horizontal gene transfer, xanthophylls, beta-carotene, bulked segregant analysis, spider mites, 2-SPOTTED SPIDER-MITE, BETA-CAROTENE, FUSARIUM-FUJIKUROI, PHOTOPERIODIC INDUCTION, ACARI-TETRANYCHIDAE, GENE-TRANSFER, BIOSYNTHESIS, METABOLISM, EVOLUTION, KOCH
journal title
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
Proc. Natl. Acad. Sci. USA
volume
114
issue
29
pages
E5871 - E5880
Web of Science type
Article
Web of Science id
000405662300016
ISSN
0027-8424
DOI
10.1073/pnas.1706865114
language
English
UGent publication?
yes
classification
A1
copyright statement
I have retained and own the full copyright for this publication
id
8527517
handle
http://hdl.handle.net/1854/LU-8527517
date created
2017-07-24 13:28:49
date last changed
2017-10-12 07:36:17
@article{8527517,
  abstract     = {Carotenoids underlie many of the vibrant yellow, orange, and red colors in animals, and are involved in processes ranging from vision to protection from stresses. Most animals acquire carotenoids from their diets because de novo synthesis of carotenoids is primarily limited to plants and some bacteria and fungi. Recently, sequencing projects in aphids and adelgids, spider mites, and gall midges identified genes with homology to fungal sequences encoding de novo carotenoid biosynthetic proteins like phytoene desaturase. The finding of horizontal gene transfers of carotenoid biosynthetic genes to three arthropod lineages was unprecedented; however, the relevance of the transfers for the arthropods that acquired them has remained largely speculative, which is especially true for spider mites that feed on plant cell contents, a known source of carotenoids. Pigmentation in spider mites results solely from carotenoids. Using a combination of genetic approaches, we show that mutations in a single horizontally transferred phytoene desaturase result in complete albinism in the two-spotted spider mite, Tetranychus urticae, as well as in the citrus red mite, Panonychus citri. Further, we show that phytoene desaturase activity is essential for photoperiodic induction of diapause in an overwintering strain of T. urticae, consistent with a role for this enzyme in provisioning provitamin A carotenoids required for light perception. Carotenoid biosynthetic genes of fungal origin have therefore enabled some mites to forgo dietary carotenoids, with endogenous synthesis underlying their intense pigmentation and ability to enter diapause, a key to the global distribution of major spider mite pests of agriculture.},
  author       = {Bryon, Astrid and Kurlovs, Andre H and Dermauw, Wannes and Greenhalgh, Robert and Riga, Maria and Grbi\'{c}, Miodrag and Tirry, Luc and Osakabe, Masahiro and Vontas, John and Clark, Richard M and Van Leeuwen, Thomas},
  issn         = {0027-8424},
  journal      = {PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA},
  keyword      = {horizontal gene transfer,xanthophylls,beta-carotene,bulked segregant analysis,spider mites,2-SPOTTED SPIDER-MITE,BETA-CAROTENE,FUSARIUM-FUJIKUROI,PHOTOPERIODIC INDUCTION,ACARI-TETRANYCHIDAE,GENE-TRANSFER,BIOSYNTHESIS,METABOLISM,EVOLUTION,KOCH},
  language     = {eng},
  number       = {29},
  pages        = {E5871--E5880},
  title        = {Disruption of a horizontally transferred phytoene desaturase abolishes carotenoid accumulation and diapause in Tetranychus urticae},
  url          = {http://dx.doi.org/10.1073/pnas.1706865114},
  volume       = {114},
  year         = {2017},
}

Chicago
Bryon, Astrid, Andre H Kurlovs, Wannes Dermauw, Robert Greenhalgh, Maria Riga, Miodrag Grbić, Luc Tirry, et al. 2017. “Disruption of a Horizontally Transferred Phytoene Desaturase Abolishes Carotenoid Accumulation and Diapause in Tetranychus Urticae.” Proceedings of the National Academy of Sciences of the United States of America 114 (29): E5871–E5880.
APA
Bryon, A., Kurlovs, A. H., Dermauw, W., Greenhalgh, R., Riga, M., Grbić, M., Tirry, L., et al. (2017). Disruption of a horizontally transferred phytoene desaturase abolishes carotenoid accumulation and diapause in Tetranychus urticae. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 114(29), E5871–E5880.
Vancouver
1.
Bryon A, Kurlovs AH, Dermauw W, Greenhalgh R, Riga M, Grbić M, et al. Disruption of a horizontally transferred phytoene desaturase abolishes carotenoid accumulation and diapause in Tetranychus urticae. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 2017;114(29):E5871–E5880.
MLA
Bryon, Astrid, Andre H Kurlovs, Wannes Dermauw, et al. “Disruption of a Horizontally Transferred Phytoene Desaturase Abolishes Carotenoid Accumulation and Diapause in Tetranychus Urticae.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 114.29 (2017): E5871–E5880. Print.