Molecular basis for enantioselective herbicide degradation imparted by aryloxyalkanoate dioxygenases in transgenic plants

Jonathan R. Chekan, Chayanid Ongpipattanakul, Terry R. Wright, Bo Zhang, J. Martin Bollinger, Lauren J. Rajakovich, Carsten Krebs, Robert M. Cicchillo, Satish K Nair

Research output: Contribution to journalArticle

Abstract

The synthetic auxin 2,4-dichlorophenoxyacetic acid (2,4-D) is an active ingredient of thousands of commercial herbicides. Multiple species of bacteria degrade 2,4-D via a pathway initiated by the Fe(II) and α-ketoglutarate (Fe/αKG)-dependent aryloxyalkanoate dioxygenases (AADs). Recently, genes encoding 2 AADs have been deployed commercially in herbicide-tolerant crops. Some AADs can also inactivate chiral phenoxypropionate and aryloxyphenoxypropionate (AOPP) herbicides, albeit with varying substrate enantio-selectivities. Certain AAD enzymes, such as AAD-1, have expanded utility in weed control systems by enabling the use of diverse modes of action with a single trait. Here, we report 1) the use of a genomic context-based approach to identify 59 additional members of the AAD class, 2) the biochemical characterization of AAD-2 from Bradyrhizobium diazoefficiens USDA 110 as a catalyst to degrade (S)-stereoisomers of chiral synthetic auxins and AOPP herbicides, 3) spectroscopic data that demonstrate the canonical ferryl complex in the AAD-1 reaction, and 4) crystal structures of representatives of the AAD class. Structures of AAD-1, an (R)-enantiomer substrate-specific enzyme, in complexes with a phenoxypropionate synthetic auxin or with AOPP herbicides and of AAD-2, which has the opposite (S)-enantiomeric substrate specificity, reveal the structural basis for stereoselectivity and provide insights into a common catalytic mechanism.

Original languageEnglish (US)
Pages (from-to)13299-13304
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume116
Issue number27
DOIs
StatePublished - Jan 1 2019

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Dioxygenases
Genetically Modified Plants
Herbicides
2,4-Dichlorophenoxyacetic Acid
Indoleacetic Acids
Weed Control
Bradyrhizobium
United States Department of Agriculture
Stereoisomerism
Enzymes
Substrate Specificity

Keywords

  • Auxin
  • Enzyme
  • Herbicide
  • Mechanism
  • Resistance

ASJC Scopus subject areas

  • General

Cite this

Molecular basis for enantioselective herbicide degradation imparted by aryloxyalkanoate dioxygenases in transgenic plants. / Chekan, Jonathan R.; Ongpipattanakul, Chayanid; Wright, Terry R.; Zhang, Bo; Martin Bollinger, J.; Rajakovich, Lauren J.; Krebs, Carsten; Cicchillo, Robert M.; Nair, Satish K.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 116, No. 27, 01.01.2019, p. 13299-13304.

Research output: Contribution to journalArticle

Chekan, Jonathan R. ; Ongpipattanakul, Chayanid ; Wright, Terry R. ; Zhang, Bo ; Martin Bollinger, J. ; Rajakovich, Lauren J. ; Krebs, Carsten ; Cicchillo, Robert M. ; Nair, Satish K. / Molecular basis for enantioselective herbicide degradation imparted by aryloxyalkanoate dioxygenases in transgenic plants. In: Proceedings of the National Academy of Sciences of the United States of America. 2019 ; Vol. 116, No. 27. pp. 13299-13304.
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AU - Martin Bollinger, J.

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AB - The synthetic auxin 2,4-dichlorophenoxyacetic acid (2,4-D) is an active ingredient of thousands of commercial herbicides. Multiple species of bacteria degrade 2,4-D via a pathway initiated by the Fe(II) and α-ketoglutarate (Fe/αKG)-dependent aryloxyalkanoate dioxygenases (AADs). Recently, genes encoding 2 AADs have been deployed commercially in herbicide-tolerant crops. Some AADs can also inactivate chiral phenoxypropionate and aryloxyphenoxypropionate (AOPP) herbicides, albeit with varying substrate enantio-selectivities. Certain AAD enzymes, such as AAD-1, have expanded utility in weed control systems by enabling the use of diverse modes of action with a single trait. Here, we report 1) the use of a genomic context-based approach to identify 59 additional members of the AAD class, 2) the biochemical characterization of AAD-2 from Bradyrhizobium diazoefficiens USDA 110 as a catalyst to degrade (S)-stereoisomers of chiral synthetic auxins and AOPP herbicides, 3) spectroscopic data that demonstrate the canonical ferryl complex in the AAD-1 reaction, and 4) crystal structures of representatives of the AAD class. Structures of AAD-1, an (R)-enantiomer substrate-specific enzyme, in complexes with a phenoxypropionate synthetic auxin or with AOPP herbicides and of AAD-2, which has the opposite (S)-enantiomeric substrate specificity, reveal the structural basis for stereoselectivity and provide insights into a common catalytic mechanism.

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