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Title: Cell wall targeted in planta iron accumulation enhances biomass conversion and seed iron concentration in Arabidopsis and rice

Abstract

Conversion of nongrain biomass into liquid fuel is a sustainable approach to energy demands as global population increases. Previously, we showed that iron can act as a catalyst to enhance the degradation of lignocellulosic biomass for biofuel production. However, direct addition of iron catalysts to biomass pretreatment is diffusion-limited, would increase the cost and complexity of biorefinery unit operations and may have deleterious environmental impacts. Here, we show a new strategy for in planta accumulation of iron throughout the volume of the cell wall where iron acts as a catalyst in the deconstruction of lignocellulosic biomass. We engineered CBM-IBP fusion polypeptides composed of a carbohydrate-binding module family 11 (CBM11) and an iron-binding peptide (IBP) for secretion into Arabidopsis and rice cell walls. CBM-IBP transformed Arabidopsis and rice plants show significant increases in iron accumulation and biomass conversion compared to respective controls. Further, CBM-IBP rice shows a 35% increase in seed iron concentration and a 40% increase in seed yield in greenhouse experiments. CBM-IBP rice potentially could be used to address iron deficiency, the most common and widespread nutritional disorder according to the World Health Organization.

Authors:
 [1];  [2];  [3];  [4];  [5];  [3];  [6];  [3];  [7];  [5];  [8];  [9];  [2];  [5];  [4];  [10];  [11]
  1. Center for Direct Catalytic Conversion Of Biomass to Biofuels (C3Bio), Purdue University, West Lafayette IN USA; Department of Horticulture, Purdue University, West Lafayette IN USA; Department of Biological Sciences, Purdue University, West Lafayette IN USA
  2. Biosciences Center, National Renewable Energy Laboratory, Golden CO USA
  3. Center for Direct Catalytic Conversion Of Biomass to Biofuels (C3Bio), Purdue University, West Lafayette IN USA; Department of Horticulture, Purdue University, West Lafayette IN USA
  4. Center for Direct Catalytic Conversion Of Biomass to Biofuels (C3Bio), Purdue University, West Lafayette IN USA; Department of Biological Sciences, Purdue University, West Lafayette IN USA
  5. X-ray Science Division, Advanced Photon Source, Argonne National Laboratory, Argonne IL USA
  6. Department of Horticulture, Purdue University, West Lafayette IN USA
  7. National Bioenergy Center, National Renewable Energy Laboratory, Golden CO USA
  8. Department of Biological Sciences, Purdue University, West Lafayette IN USA; Department of Botany and Plant Pathology, Purdue University, West Lafayette IN USA
  9. Department of Bioengineering, Northeastern University, Boston MA USA; Department of Chemistry and Chemical Biology, Northeastern University, Boston MA USA
  10. Center for Direct Catalytic Conversion Of Biomass to Biofuels (C3Bio), Purdue University, West Lafayette IN USA; Department of Horticulture, Purdue University, West Lafayette IN USA; Department of Plant Science and Landscape Architecture, University of Maryland, College Park MD USA
  11. Center for Direct Catalytic Conversion Of Biomass to Biofuels (C3Bio), Purdue University, West Lafayette IN USA; Department of Horticulture, Purdue University, West Lafayette IN USA; Department of Plant Science and Landscape Architecture, University of Maryland, College Park MD USA; Department of Environmental Science and Technology, University of Maryland, College Park MD USA
Publication Date:
Research Org.:
Energy Frontier Research Centers (EFRC) (United States). Center for Direct Catalytic Conversion of Biomass to Biofuels (C3Bio); Argonne National Laboratory (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1373944
DOE Contract Number:  
AC02-06CH11357
Resource Type:
Journal Article
Journal Name:
Plant Biotechnology Journal
Additional Journal Information:
Journal Volume: 14; Journal Issue: 10; Journal ID: ISSN 1467-7644
Publisher:
Society for Experimental Biology; Association of Applied Biology
Country of Publication:
United States
Language:
English
Subject:
Biofuel; carbohydrate-binding module; cell wall; iron concentration; iron-binding peptide; secretion

Citation Formats

Yang, Haibing, Wei, Hui, Ma, Guojie, Antunes, Mauricio S., Vogt, Stefan, Cox, Joseph, Zhang, Xiao, Liu, Xiping, Bu, Lintao, Gleber, S. Charlotte, Carpita, Nicholas C., Makowski, Lee, Himmel, Michael E., Tucker, Melvin P., McCann, Maureen C., Murphy, Angus S., and Peer, Wendy A. Cell wall targeted in planta iron accumulation enhances biomass conversion and seed iron concentration in Arabidopsis and rice. United States: N. p., 2016. Web. doi:10.1111/pbi.12557.
Yang, Haibing, Wei, Hui, Ma, Guojie, Antunes, Mauricio S., Vogt, Stefan, Cox, Joseph, Zhang, Xiao, Liu, Xiping, Bu, Lintao, Gleber, S. Charlotte, Carpita, Nicholas C., Makowski, Lee, Himmel, Michael E., Tucker, Melvin P., McCann, Maureen C., Murphy, Angus S., & Peer, Wendy A. Cell wall targeted in planta iron accumulation enhances biomass conversion and seed iron concentration in Arabidopsis and rice. United States. https://doi.org/10.1111/pbi.12557
Yang, Haibing, Wei, Hui, Ma, Guojie, Antunes, Mauricio S., Vogt, Stefan, Cox, Joseph, Zhang, Xiao, Liu, Xiping, Bu, Lintao, Gleber, S. Charlotte, Carpita, Nicholas C., Makowski, Lee, Himmel, Michael E., Tucker, Melvin P., McCann, Maureen C., Murphy, Angus S., and Peer, Wendy A. 2016. "Cell wall targeted in planta iron accumulation enhances biomass conversion and seed iron concentration in Arabidopsis and rice". United States. https://doi.org/10.1111/pbi.12557.
@article{osti_1373944,
title = {Cell wall targeted in planta iron accumulation enhances biomass conversion and seed iron concentration in Arabidopsis and rice},
author = {Yang, Haibing and Wei, Hui and Ma, Guojie and Antunes, Mauricio S. and Vogt, Stefan and Cox, Joseph and Zhang, Xiao and Liu, Xiping and Bu, Lintao and Gleber, S. Charlotte and Carpita, Nicholas C. and Makowski, Lee and Himmel, Michael E. and Tucker, Melvin P. and McCann, Maureen C. and Murphy, Angus S. and Peer, Wendy A.},
abstractNote = {Conversion of nongrain biomass into liquid fuel is a sustainable approach to energy demands as global population increases. Previously, we showed that iron can act as a catalyst to enhance the degradation of lignocellulosic biomass for biofuel production. However, direct addition of iron catalysts to biomass pretreatment is diffusion-limited, would increase the cost and complexity of biorefinery unit operations and may have deleterious environmental impacts. Here, we show a new strategy for in planta accumulation of iron throughout the volume of the cell wall where iron acts as a catalyst in the deconstruction of lignocellulosic biomass. We engineered CBM-IBP fusion polypeptides composed of a carbohydrate-binding module family 11 (CBM11) and an iron-binding peptide (IBP) for secretion into Arabidopsis and rice cell walls. CBM-IBP transformed Arabidopsis and rice plants show significant increases in iron accumulation and biomass conversion compared to respective controls. Further, CBM-IBP rice shows a 35% increase in seed iron concentration and a 40% increase in seed yield in greenhouse experiments. CBM-IBP rice potentially could be used to address iron deficiency, the most common and widespread nutritional disorder according to the World Health Organization.},
doi = {10.1111/pbi.12557},
url = {https://www.osti.gov/biblio/1373944}, journal = {Plant Biotechnology Journal},
issn = {1467-7644},
number = 10,
volume = 14,
place = {United States},
year = {Thu Apr 07 00:00:00 EDT 2016},
month = {Thu Apr 07 00:00:00 EDT 2016}
}

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Purification of an iron-binding nona-peptide from hydrolysates of porcine blood plasma protein
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A protocol for Agrobacterium-mediated transformation in rice
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Rice endosperm iron biofortification by targeted and synergistic action of nicotianamine synthase and ferritin
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Altered expression of expansin modulates leaf growth and pedicel abscission in Arabidopsis thaliana
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High-Throughput Screening Techniques for Biomass Conversion
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Environmental, economic, and energetic costs and benefits of biodiesel and ethanol biofuels
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PIN2 Turnover in Arabidopsis Root Epidermal Cells Explored by the Photoconvertible Protein Dendra2
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Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana
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Multiscale deconstruction of molecular architecture in corn stover
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Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation
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CHARMM Additive All-Atom Force Field for Glycosidic Linkages between Hexopyranoses
journal, August 2009


Colorimetric Method for Determination of Sugars and Related Substances
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Recent structural studies of carbohydrate-binding modules
journal, November 2006


Decrystallization of Oligosaccharides from the Cellulose Iβ Surface with Molecular Simulation
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Iron fortification of rice seed by the soybean ferritin gene
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Engineered endophytic bacteria improve phytoremediation of water-soluble, volatile, organic pollutants
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Semimicro determination of cellulose inbiological materials
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Engineering of a high-throughput screening system to identify cellulosic biomass, pretreatments, and enzyme formulations that enhance sugar release
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Genotypic variation in element concentrations in brown rice from Yunnan landraces in China
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Facing the challenges of Cu, Fe and Zn homeostasis in plants
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Role of the Extensin Superfamily in Primary Cell Wall Architecture
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Mechanism of pore opening in the calcium-activated chloride channel TMEM16A
journal, February 2021


Lignin content in natural Populus variants affects sugar release
text, January 2011


CHARMM: the biomolecular simulation program
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Engineering of a high-throughput screening system to identify cellulosic biomass, pretreatments, and enzyme formulations that enhance sugar release
journal, February 2010


CHARMM: The biomolecular simulation program
journal, July 2009


Recent structural studies of carbohydrate-binding modules
journal, November 2006


Iron accumulation does not parallel the high expression level of ferritin in transgenic rice seeds
journal, April 2005


Genotypic variation in element concentrations in brown rice from Yunnan landraces in China
journal, June 2009


A semi-empirical method for prediction of antigenic determinants on protein antigens
journal, December 1990


Corn stover pretreatment by inorganic salts and its effects on hemicellulose and cellulose degradation
journal, December 2009


Harnessing glycosylation to improve cellulase activity
journal, June 2012


Iron content and bioavailability in rice
journal, June 2005


CHARMM Additive All-Atom Force Field for Glycosidic Linkages between Hexopyranoses
journal, August 2009


All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins
journal, April 1998


Plant ferritin and human iron deficiency
journal, July 1999


Solving the structure of human H ferritin by genetically engineering intermolecular crystal contacts
journal, February 1991


Engineered endophytic bacteria improve phytoremediation of water-soluble, volatile, organic pollutants
journal, April 2004


A guide to choosing fluorescent proteins
journal, November 2005


A protocol for Agrobacterium-mediated transformation in rice
journal, December 2006


Multiscale deconstruction of molecular architecture in corn stover
journal, January 2014


Solution structure, dynamics and binding studies of a family 11 carbohydrate-binding module from Clostridium thermocellum (CtCBM11)
journal, March 2013


Altered expression of expansin modulates leaf growth and pedicel abscission in Arabidopsis thaliana
journal, August 2000


Iron Acquisition from Fe-Pyoverdine by Arabidopsis thaliana
journal, April 2007


The Arabidopsis AtOPT3 Protein Functions in Metal Homeostasis and Movement of Iron to Developing Seeds
journal, December 2007


Role of the Extensin Superfamily in Primary Cell Wall Architecture
journal, March 2011


SmartGrain : High-Throughput Phenotyping Software for Measuring Seed Shape through Image Analysis
journal, October 2012


Regulation of Expansin Gene Expression Affects Growth and Development in Transgenic Rice Plants
journal, May 2003


Rice endosperm iron biofortification by targeted and synergistic action of nicotianamine synthase and ferritin
journal, September 2009


Biomass Recalcitrance: Engineering Plants and Enzymes for Biofuels Production
journal, February 2007


The Path from  -Carotene to Carlactone, a Strigolactone-Like Plant Hormone
journal, March 2012


Carbohydrate Binding Modules: Biochemical Properties and Novel Applications
journal, June 2006


Elucidating the role of ferrous ion cocatalyst in enhancing dilute acid pretreatment of lignocellulosic biomass
journal, January 2011


Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation
journal, July 2007


Works referencing / citing this record:

Biotechnological Strategies to Improve Plant Biomass Quality for Bioethanol Production
journal, January 2017


Directed plant cell-wall accumulation of iron: embedding co-catalyst for efficient biomass conversion
journal, October 2016


Directed plant cell-wall accumulation of iron: embedding co-catalyst for efficient biomass conversion
journal, October 2016


Iron incorporation both intra- and extra-cellularly improves the yield and saccharification of switchgrass (Panicum virgatum L.) biomass
journal, March 2021