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Redirection of the phenylpropanoid pathway to feruloyl malate in Arabidopsis mutants deficient for cinnamoyl-CoA reductase 1

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Abstract

Cinnamoyl-CoA reductase 1 (CCR1, gene At1g15950) is the main CCR isoform implied in the constitutive lignification of Arabidopsis thaliana. In this work, we have identified and characterized two new knockout mutants for CCR1. Both have a dwarf phenotype and a delayed senescence. At complete maturity, their inflorescence stems display a 25–35% decreased lignin level, some alterations in lignin structure with a higher frequency of resistant interunit bonds and a higher content in cell wall-bound ferulic esters. Ferulic acid-coniferyl alcohol ether dimers were found for the first time in dicot cell walls and in similar levels in wild-type and mutant plants. The expression of CCR2, a CCR gene usually involved in plant defense, was increased in the mutants and could account for the biosynthesis of lignins in the CCR1-knockout plants. Mutant plantlets have three to four-times less sinapoyl malate (SM) than controls and accumulate some feruloyl malate. The same compositional changes occurred in the rosette leaves of greenhouse-grown plants. By contrast and relative to the control, their stems accumulated unusually high levels of both SM and feruloyl malate as well as more kaempferol glycosides. These findings suggest that, in their hypolignified stems, the mutant plants would avoid the feruloyl-CoA accumulation by its redirection to cell wall-bound ferulate esters, to feruloyl malate and to SM. The formation of feruloyl malate to an extent far exceeding the levels reported so far indicates that ferulic acid is a potential substrate for the enzymes involved in SM biosynthesis and emphasizes the remarkable plasticity of Arabidopsis phenylpropanoid metabolism.

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Abbreviations

Col 0:

Columbia

CCR:

Cinnamoyl-CoA reductase

FeG:

Feruloyl glucose

FeM:

Feruloyl malate

FST:

Flanking sequence tag

F5H:

Ferulate -5-hydroxylase

GC-MS:

Gas chromatography-mass spectrometry

LC-MS:

Liquid chromatography-mass spectrometry

SE:

Standard error

SM:

Sinapoyl malate

TMS:

Trimethylsilylated

WS:

Wassilewskija

WT:

Wild-type

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Acknowledgments

We thank Fréderic Legée (AgroParisTech, UMR 206 Chimie Biologique) and Laurent Cézard (INRA, UMR 206 Chimie Biologique) for running the Klason lignin and the thioacidolysis analyses respectively and Christina Gofron (INRA Versailles) for Arabidopsis cultivation in the greenhouse.

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Authors and Affiliations

  1. Biologie Cellulaire, INRA, 78026, Versailles cedex, France

    Mohammad Mir Derikvand, Cao-Trung Do, Johanne Thévenin, Dominique Buffard & Lise Jouanin

  2. CERMAV-UPR5301, BP53, 38041, Grenoble, France

    Jimmy Berrio Sierra & Katia Ruel

  3. UMR 206 Chimie Biologique AgroParisTech-INRA, AgroParisTech Centre de Grignon, 78850, Thiverval-Grignon, France

    Jimmy Berrio Sierra, Brigitte Pollet & Catherine Lapierre

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  1. Mohammad Mir Derikvand
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  2. Jimmy Berrio Sierra
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Correspondence to Lise Jouanin.

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Mir Derikvand, M., Sierra, J.B., Ruel, K. et al. Redirection of the phenylpropanoid pathway to feruloyl malate in Arabidopsis mutants deficient for cinnamoyl-CoA reductase 1. Planta 227, 943–956 (2008). https://doi.org/10.1007/s00425-007-0669-x

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