Structural Basis for Dual Functionality of Isoflavonoid O-Methyltransferases in the Evolution of Plant Defense Responses

Liu, C -J; Deavours, B E; Richard, S B; Ferrer, J -L; Blount, J W; Huhman, D; Dixon, R A; Noel, J

Title: Structural Basis for Dual Functionality of Isoflavonoid O-Methyltransferases in the Evolution of Plant Defense Responses

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Abstract

In leguminous plants such as pea (Pisum sativum), alfalfa (Medicago sativa), barrel medic (Medicago truncatula), and chickpea (Cicer arietinum), 4'-O-methylation of isoflavonoid natural products occurs early in the biosynthesis of defense chemicals known as phytoalexins. However, among these four species, only pea catalyzes 3-O-methylation that converts the pterocarpanoid isoflavonoid 6a-hydroxymaackiain to pisatin. In pea, pisatin is important for chemical resistance to the pathogenic fungus Nectria hematococca. While barrel medic does not biosynthesize 6a-hydroxymaackiain, when cell suspension cultures are fed 6a-hydroxymaackiain, they accumulate pisatin. In vitro, hydroxyisoflavanone 4'-O-methyltransferase (HI4'OMT) from barrel medic exhibits nearly identical steady state kinetic parameters for the 4'-O-methylation of the isoflavonoid intermediate 2,7,4'-trihydroxyisoflavanone and for the 3-O-methylation of the 6a-hydroxymaackiain isoflavonoid-derived pterocarpanoid intermediate found in pea. Protein x-ray crystal structures of HI4'OMT substrate complexes revealed identically bound conformations for the 2S,3R-stereoisomer of 2,7,4'-trihydroxyisoflavanone and the 6aR,11aR-stereoisomer of 6a-hydroxymaackiain. These results suggest how similar conformations intrinsic to seemingly distinct chemical substrates allowed leguminous plants to use homologous enzymes for two different biosynthetic reactions. The three-dimensional similarity of natural small molecules represents one explanation for how plants may rapidly recruit enzymes for new biosynthetic reactions in response to changing physiological and ecological pressures.

Authors:: Liu, C -J; Deavours, B E; Richard, S B; Ferrer, J -L; Blount, J W; Huhman, D; Dixon, R A; Noel, J

Publication Date:: Tue Jul 10 00:00:00 EDT 2007

Research Org.:: SLAC National Accelerator Lab., Menlo Park, CA (United States)

Sponsoring Org.:: USDOE

OSTI Identifier:: 909777

Report Number(s):: SLAC-REPRINT-2007-118
TRN: US200723%%177

DOE Contract Number:: AC02-76SF00515

Resource Type:: Journal Article

Journal Name:: Submitted to Plant Cell

Additional Journal Information:: Journal Name: Submitted to Plant Cell

Country of Publication:: United States

Language:: English

Subject:: 36 MATERIALS SCIENCE; ALFALFA; BIOSYNTHESIS; CRYSTAL STRUCTURE; ENZYMES; IN VITRO; KINETICS; PEAS; PISUM; PROTEINS; SUBSTRATES; PLANTS; Other,OTHER

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                    Liu, C -J, Deavours, B E, Richard, S B, Ferrer, J -L, Blount, J W, Huhman, D, Dixon, R A, and Noel, J. Structural Basis for Dual Functionality of Isoflavonoid O-Methyltransferases in the Evolution of Plant Defense Responses.  United States: N. p., 2007. 
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                    Liu, C -J, Deavours, B E, Richard, S B, Ferrer, J -L, Blount, J W, Huhman, D, Dixon, R A, & Noel, J. Structural Basis for Dual Functionality of Isoflavonoid O-Methyltransferases in the Evolution of Plant Defense Responses.  United States.

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                    Liu, C -J, Deavours, B E, Richard, S B, Ferrer, J -L, Blount, J W, Huhman, D, Dixon, R A, and Noel, J. 2007.  
        "Structural Basis for Dual Functionality of Isoflavonoid O-Methyltransferases in the Evolution of Plant Defense Responses".  United States.

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@article{osti_909777,

  title        = {Structural Basis for Dual Functionality of Isoflavonoid O-Methyltransferases in the Evolution of Plant Defense Responses},

  author       = {Liu, C -J and Deavours, B E and Richard, S B and Ferrer, J -L and Blount, J W and Huhman, D and Dixon, R A and Noel, J},

  abstractNote = {In leguminous plants such as pea (Pisum sativum), alfalfa (Medicago sativa), barrel medic (Medicago truncatula), and chickpea (Cicer arietinum), 4'-O-methylation of isoflavonoid natural products occurs early in the biosynthesis of defense chemicals known as phytoalexins. However, among these four species, only pea catalyzes 3-O-methylation that converts the pterocarpanoid isoflavonoid 6a-hydroxymaackiain to pisatin. In pea, pisatin is important for chemical resistance to the pathogenic fungus Nectria hematococca. While barrel medic does not biosynthesize 6a-hydroxymaackiain, when cell suspension cultures are fed 6a-hydroxymaackiain, they accumulate pisatin. In vitro, hydroxyisoflavanone 4'-O-methyltransferase (HI4'OMT) from barrel medic exhibits nearly identical steady state kinetic parameters for the 4'-O-methylation of the isoflavonoid intermediate 2,7,4'-trihydroxyisoflavanone and for the 3-O-methylation of the 6a-hydroxymaackiain isoflavonoid-derived pterocarpanoid intermediate found in pea. Protein x-ray crystal structures of HI4'OMT substrate complexes revealed identically bound conformations for the 2S,3R-stereoisomer of 2,7,4'-trihydroxyisoflavanone and the 6aR,11aR-stereoisomer of 6a-hydroxymaackiain. These results suggest how similar conformations intrinsic to seemingly distinct chemical substrates allowed leguminous plants to use homologous enzymes for two different biosynthetic reactions. The three-dimensional similarity of natural small molecules represents one explanation for how plants may rapidly recruit enzymes for new biosynthetic reactions in response to changing physiological and ecological pressures.},

  doi          = {},

  url          = {https://www.osti.gov/biblio/909777},
  journal      = {Submitted to Plant Cell},
number       = ,

  volume       = ,

  place        = {United States},

  year         = {Tue Jul 10 00:00:00 EDT 2007},

  month        = {Tue Jul 10 00:00:00 EDT 2007}

}

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Structural Basis for Dual Functionality of Isoflavonoid O-Methyltransferases in the Evolution of Plant Defense Responses

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