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Iron incorporation both intra- and extra-cellularly improves the yield and saccharification of switchgrass (Panicum virgatum L.) biomass

Lin, Chien-Yuan and Donohoe, Bryon S. and Bomble, Yannick J. and Yang, Haibing and Yunes, Manal and Sarai, Nicholas S. and Shollenberger, Todd and Decker, Stephen R. and Chen, Xiaowen and McCann, Maureen C. and Tucker, Melvin P. and Wei, Hui and Himmel, Michael E. (2021) Iron incorporation both intra- and extra-cellularly improves the yield and saccharification of switchgrass (Panicum virgatum L.) biomass. Biotechnology for Biofuels, 14 (1). Art. No. 55. ISSN 1754-6834. PMCID PMC7931346. https://resolver.caltech.edu/CaltechAUTHORS:20210305-113751556

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Abstract

Background: Pretreatments are commonly used to facilitate the deconstruction of lignocellulosic biomass to its component sugars and aromatics. Previously, we showed that iron ions can be used as co-catalysts to reduce the severity of dilute acid pretreatment of biomass. Transgenic iron-accumulating Arabidopsis and rice plants exhibited higher iron content in grains, increased biomass yield, and importantly, enhanced sugar release from the biomass. Results: In this study, we used intracellular ferritin (FerIN) alone and in combination with an improved version of cell wall-bound carbohydrate-binding module fused iron-binding peptide (IBPex) specifically targeting switchgrass, a bioenergy crop species. The FerIN switchgrass improved by 15% in height and 65% in yield, whereas the FerIN/IBPex transgenics showed enhancement up to 30% in height and 115% in yield. The FerIN and FerIN/IBPex switchgrass had 27% and 51% higher in planta iron accumulation than the empty vector (EV) control, respectively, under normal growth conditions. Improved pretreatability was observed in FerIN switchgrass (~ 14% more glucose release than the EV), and the FerIN/IBPex plants showed further enhancement in glucose release up to 24%. Conclusions: We conclude that this iron-accumulating strategy can be transferred from model plants and applied to bioenergy crops, such as switchgrass. The intra- and extra-cellular iron incorporation approach improves biomass pretreatability and digestibility, providing upgraded feedstocks for the production of biofuels and bioproducts.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1186/s13068-021-01891-4DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7931346PubMed CentralArticle
ORCID:
AuthorORCID
Lin, Chien-Yuan0000-0001-5081-3550
Donohoe, Bryon S.0000-0002-2272-5059
Bomble, Yannick J.0000-0001-7624-8000
Sarai, Nicholas S.0000-0002-4655-0038
Additional Information:© The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Received 20 June 2020; Accepted 27 January 2021; Published 04 March 2021. We thank Crissa Doeppke and Erica Gjersing for their help with the grinding of biomass samples. This work was authored in part by Alliance for Sustainable Energy, LLC, the manager and operator of the National Renewable Energy Laboratory for the U.S. Department of Energy (DOE) under Contract No. DE-AC36-08GO28308. Funding for MEH, BSD, and CYL was provided by Center for Direct Catalytic Conversion of Biomass to Biofuels (C3Bio), an Energy Frontier Research Center funded by the U.S. Department of Energy, Office of Science, Office of Basic Energy Sciences, Award Number DE-SC0000997. XC, HW, and MPT were supported by the BioEnergy Technologies Office (BETO) program in the U.S. DOE Office of Energy Efficiency and Renewable Energy (EERE). NSS and YJB were supported by the U.S. Department of Energy Center for Bioenergy Innovation (CBI). The Center for Bioenergy Innovation is a U.S. Department of Energy Bioenergy Research Center supported by the Office of Biological and Environmental Research in the U.S. Department of Energy Office of Science. The views expressed in the article do not necessarily represent the views of the DOE or the U.S. Government. The U.S. Government retains and the publisher, by accepting the article for publication, acknowledges that the U.S. Government retains a nonexclusive, paid-up, irrevocable, worldwide license to publish or reproduce the published form of this work, or allow others to do so, for U.S. Government purposes. The funding sources were not involved in the design of the study, data interpretation, report writing or decision in submitting the article for publication. Availability of data and materials: The data supporting the conclusions of this article are included within the article. Author Contributions: CYL, BSD, MPT, HW, and MEH designed and coordinated the study. NSS and YJB performed protein purification and characterization. CYL and HW conducted the molecular plant biology work. HBY and MCM contributed to the design of IBP constructs. MY processed the switchgrass biomass. TS, SRD, XC, and MPT performed hot-water pretreatment (HWP) and co-saccharification analysis. CYL, BSD, and HW wrote the manuscript with contributions from all authors. All authors read and approved the final manuscript. Ethics approval and consent to participate: Not applicable. Consent for publication: All authors consent to the manuscript for publication in Biotechnology for Biofuels. The authors declare that they have no competing interests.
Funders:
Funding AgencyGrant Number
Department of Energy (DOE)DE-AC36-08GO28308
Department of Energy (DOE)DE-SC0000997
Subject Keywords:Ferritin; Iron co-catalyst; Transgenic switchgrass; High-throughput hot-water pretreatment; Saccharification; Sugar release; Perls’ Prussian blue staining
Issue or Number:1
PubMed Central ID:PMC7931346
Record Number:CaltechAUTHORS:20210305-113751556
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20210305-113751556
Official Citation:Lin, CY., Donohoe, B.S., Bomble, Y.J. et al. Iron incorporation both intra- and extra-cellularly improves the yield and saccharification of switchgrass (Panicum virgatum L.) biomass. Biotechnol Biofuels 14, 55 (2021). https://doi.org/10.1186/s13068-021-01891-4
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:108332
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:08 Mar 2021 20:07
Last Modified:08 Mar 2021 20:46

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