Pinoresinol rescues developmental phenotypes of Arabidopsis phenylpropanoid mutants overexpressing FERULATE 5-HYDROXYLASE

Journal Article · Mon Jul 24 00:00:00 EDT 2023 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.2216543120· OSTI ID:1992157

Muro-Villanueva, Fabiola ^[1]; Pysh, Leonard D. ^[2]; Kim, Hoon  ^[3]; Bouse, Tyler ^[4]; Ralph, John  ^[5]; Luo, Zhiwei ^[1]; Cooper, Bruce R. ^[6]; Jannasch, Amber S. ^[6]; Zhang, Zeyu ^[7]; Gu, Chong ^[7]; Chapple, Clint  ^[1]

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1. Department of Biochemistry, Purdue University, West Lafayette, IN 47907, Center for Plant Biology, Purdue University, West Lafayette, IN 47907
2. Department of Biology, Roanoke College, Salem, VA 24153
3. US Department of Energy’s Great Lakes Bioenergy Research Center, Wisconsin Energy Institute, Madison, WI 53726
4. Department of Biochemistry, Purdue University, West Lafayette, IN 47907
5. US Department of Energy’s Great Lakes Bioenergy Research Center, Wisconsin Energy Institute, Madison, WI 53726, Department of Biochemistry, University of Wisconsin-Madison, Madison, WI 53706
6. Bindley Bioscience Center, Purdue University, West Lafayette, IN 47907
7. Department of Statistics, Purdue University, West Lafayette, IN 47907

Most phenylpropanoid pathway flux is directed toward the production of monolignols, but this pathway also generates multiple bioactive metabolites. The monolignols coniferyl and sinapyl alcohol polymerize to form guaiacyl (G) and syringyl (S) units in lignin, components that are characteristic of plant secondary cell walls. Lignin negatively impacts the saccharification potential of lignocellulosic biomass. Although manipulation of its content and composition through genetic engineering has reduced biomass recalcitrance, in some cases, these genetic manipulations lead to impaired growth. The reduced-growth phenotype is often attributed to poor water transport due to xylem collapse in low-lignin mutants, but alternative models suggest that it could be caused by the hyper- or hypoaccumulation of phenylpropanoid intermediates. In Arabidopsis thaliana , overexpression of FERULATE 5-HYDROXYLASE ( F5H ) shifts the normal G/S lignin ratio to nearly pure S lignin and does not result in substantial changes to plant growth. In contrast, when we overexpressed F5H in the low-lignin mutants cinnamyl dehydrogenase c and d ( cadc cadd ), cinnamoyl-CoA reductase 1 , and reduced epidermal fluorescence 3 , plant growth was severely compromised. In addition, cadc cadd plants overexpressing F5H exhibited defects in lateral root development. Exogenous coniferyl alcohol (CA) and its dimeric coupling product, pinoresinol, rescue these phenotypes. These data suggest that mutations in the phenylpropanoid pathway limit the biosynthesis of pinoresinol, and this effect is exacerbated by overexpression of F5H , which further draws down cellular pools of its precursor, CA. Overall, these genetic manipulations appear to restrict the synthesis of pinoresinol or a downstream metabolite that is necessary for plant growth.

• Sponsoring Organization: USDOE
• Grant/Contract Number: SC0000997; SC0020368; SC0018409
• OSTI ID: 1992157
• Journal Information: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Vol. 120 Journal Issue: 31; ISSN 0027-8424
• Publisher: Proceedings of the National Academy of Sciences
• Country of Publication: United States
• Language: English