Disruption of p-coumaroyl-CoA:monolignol transferases in rice drastically alters lignin composition

Author:

Lam Lydia Pui Ying12ORCID,Tobimatsu Yuki1ORCID,Suzuki Shiro13ORCID,Tanaka Takuto1ORCID,Yamamoto Senri1,Takeda-Kimura Yuri1ORCID,Osakabe Yuriko4ORCID,Osakabe Keishi5ORCID,Ralph John6ORCID,Bartley Laura E17ORCID,Umezawa Toshiaki1ORCID

Affiliation:

1. Research Institute for Sustainable Humanosphere, Kyoto University , Uji, Kyoto 611-0011 , Japan

2. Center for Crossover Education, Graduate School of Engineering Science, Akita University , Akita, Akita 010-0852 , Japan

3. Faculty of Applied Biological Sciences, Graduate School of Natural Science and Technology, and The United Graduate School of Agricultural Science, Gifu University , Gifu, Gifu 501-1193 Japan

4. School of Life Science and Technology, Tokyo Institute of Technology, Yokohama , Kanagawa 226-8502 Japan

5. Faculty of Bioscience and Bioindustry, Tokushima University , Tokushima, Tokushima 770-8503 Japan

6. Department of Biochemistry, and the U.S. Department of Energy Great Lakes Bioenergy Research Center, Wisconsin Energy Institute, University of Wisconsin , Madison, WI 53726 , USA

7. Institute of Biological Chemistry, Washington State University , Pullman, WA 99164 , USA

Abstract

Abstract Grasses are abundant feedstocks that can supply lignocellulosic biomass for production of cell-wall-derived chemicals. In grass cell walls, lignin is acylated with p-coumarate. These p-coumarate decorations arise from the incorporation of monolignol p-coumarate conjugates during lignification. A previous biochemical study identified a rice (Oryza sativa) BAHD acyltransferase (AT) with p-coumaroyl-CoA:monolignol transferase (PMT) activity in vitro. In this study, we determined that that enzyme, which we name OsPMT1 (also known as OsAT4), and the closely related OsPMT2 (OsAT3) harbor similar catalytic activity toward monolignols. We generated rice mutants deficient in either or both OsPMT1 and OsPMT2 by CRISPR/Cas9-mediated mutagenesis and subjected the mutants’ cell walls to analysis using chemical and nuclear magnetic resonance methods. Our results demonstrated that OsPMT1 and OsPMT2 both function in lignin p-coumaroylation in the major vegetative tissues of rice. Notably, lignin-bound p-coumarate units were undetectable in the ospmt1 ospmt2-2 double-knockout mutant. Further, in-depth structural analysis of purified lignins from the ospmt1 ospmt2-2 mutant compared with control lignins from wild-type rice revealed stark changes in polymer structures, including alterations in syringyl/guaiacyl aromatic unit ratios and inter-monomeric linkage patterns, and increased molecular weights. Our results provide insights into lignin polymerization in grasses that will be useful for the optimization of bioengineering approaches for the effective use of biomass in biorefineries.

Publisher

Oxford University Press (OUP)

Subject

Plant Science,Genetics,Physiology

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