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Title: Altering carbon allocation in hybrid poplar ( Populus alba × grandidentata ) impacts cell wall growth and development

Abstract

Galactinol synthase is a pivotal enzyme involved in the synthesis of the raffinose family of oligosaccharides (RFOs) that function as transport carbohydrates in the phloem, as storage compounds in sink tissues and as soluble metabolites that combat both abiotic and biotic stress in several plant species. For hybrid poplar (Populus alba 9 grandidentata) overexpressing the Arabidopsis thaliana GolS3 (AtGolS3) gene showed clear effects on development; the extreme overexpressing lines were stunted and had cell wall traits characteristic of tension wood, whereas lines with only moderate up-regulation grew normally and had moderately altered secondary cell wall composition and ultrastructure. Stem cross-sections of the developing xylem revealed a significant increase in the number of vessels, as well as the clear presence of a G-layer in the fibres. Furthermore, AtGolS3-OE lines possessed higher cellulose and lower lignin contents, an increase in cellulose crystallinity, and significantly altered hemicellulose-derived carbohydrates, notably manifested by their mannose and xylose contents. Additionally, the transgenic plants displayed elevated xylem starch content. Transcriptome interrogation of the transgenic plants showed a significant up-regulation of genes involved in the synthesis of myo-inositol, along with genes involved in sucrose degradation. Our results suggest that the over expression of GolS and its product galactinolmore » may serve as a molecular signal that initiates metabolic changes, culminating in a change in cell wall development and potentially the formation of tension wood.« less

Authors:
 [1];  [2];  [3];  [2];  [4]
  1. Univ. of British Columbia, Vancouver, BC (Canada). Dept. of Wood Science
  2. Univ. of Wisconsin, Madison, WI (United States). Dept. of Biochemistry; Wisconsin Energy Inst., Madison, WI (United States). Dept. of Energy Great Lakes Bioenergy Research Center
  3. Agricultural Research Council, Pretoria (South Africa). Biotechnology Platform
  4. Univ. of British Columbia, Vancouver, BC (Canada). Dept. of Wood Science; Wisconsin Energy Inst., Madison, WI (United States). Dept. of Energy Great Lakes Bioenergy Research Center
Publication Date:
Research Org.:
Univ. of Wisconsin, Madison, WI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1374538
Grant/Contract Number:
FC02-07ER64494
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Plant Biotechnology Journal
Additional Journal Information:
Journal Volume: 15; Journal Issue: 7; Journal ID: ISSN 1467-7644
Publisher:
Society for Experimental Biology; Association of Applied Biology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; galactinol synthase; RFOs; tension wood; cellulose; lignin; sugar signalling

Citation Formats

Unda, Faride, Kim, Hoon, Hefer, Charles, Ralph, John, and Mansfield, Shawn D. Altering carbon allocation in hybrid poplar ( Populus alba × grandidentata ) impacts cell wall growth and development. United States: N. p., 2017. Web. doi:10.1111/pbi.12682.
Unda, Faride, Kim, Hoon, Hefer, Charles, Ralph, John, & Mansfield, Shawn D. Altering carbon allocation in hybrid poplar ( Populus alba × grandidentata ) impacts cell wall growth and development. United States. doi:10.1111/pbi.12682.
Unda, Faride, Kim, Hoon, Hefer, Charles, Ralph, John, and Mansfield, Shawn D. Sat . "Altering carbon allocation in hybrid poplar ( Populus alba × grandidentata ) impacts cell wall growth and development". United States. doi:10.1111/pbi.12682. https://www.osti.gov/servlets/purl/1374538.
@article{osti_1374538,
title = {Altering carbon allocation in hybrid poplar ( Populus alba × grandidentata ) impacts cell wall growth and development},
author = {Unda, Faride and Kim, Hoon and Hefer, Charles and Ralph, John and Mansfield, Shawn D.},
abstractNote = {Galactinol synthase is a pivotal enzyme involved in the synthesis of the raffinose family of oligosaccharides (RFOs) that function as transport carbohydrates in the phloem, as storage compounds in sink tissues and as soluble metabolites that combat both abiotic and biotic stress in several plant species. For hybrid poplar (Populus alba 9 grandidentata) overexpressing the Arabidopsis thaliana GolS3 (AtGolS3) gene showed clear effects on development; the extreme overexpressing lines were stunted and had cell wall traits characteristic of tension wood, whereas lines with only moderate up-regulation grew normally and had moderately altered secondary cell wall composition and ultrastructure. Stem cross-sections of the developing xylem revealed a significant increase in the number of vessels, as well as the clear presence of a G-layer in the fibres. Furthermore, AtGolS3-OE lines possessed higher cellulose and lower lignin contents, an increase in cellulose crystallinity, and significantly altered hemicellulose-derived carbohydrates, notably manifested by their mannose and xylose contents. Additionally, the transgenic plants displayed elevated xylem starch content. Transcriptome interrogation of the transgenic plants showed a significant up-regulation of genes involved in the synthesis of myo-inositol, along with genes involved in sucrose degradation. Our results suggest that the over expression of GolS and its product galactinol may serve as a molecular signal that initiates metabolic changes, culminating in a change in cell wall development and potentially the formation of tension wood.},
doi = {10.1111/pbi.12682},
journal = {Plant Biotechnology Journal},
number = 7,
volume = 15,
place = {United States},
year = {Sat Mar 04 00:00:00 EST 2017},
month = {Sat Mar 04 00:00:00 EST 2017}
}

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  • No abstract prepared.
  • Here, a greater understanding of the genetic regulation of plant cell wall remodeling and the impact of modified cell walls on plant performance is important for the development of sustainable biofuel crops. Here, we studied the impact of down-regulating KORRIGAN-like cell wall biosynthesis genes, belonging to the endo-β-1,4-glucanase gene family, on Populus growth, metabolism and the ability to interact with symbiotic microbes. The reductions in cellulose content and lignin syringyl-to-guaiacyl unit ratio, and increase in cellulose crystallinity of cell walls of PdKOR RNAi plants corroborated the functional role of PdKOR in cell wall biosynthesis. Altered metabolism and reduced growth characteristicsmore » of RNAi plants revealed new implications on carbon allocation and partitioning. The distinctive metabolome phenotype comprised of a higher phenolic and salicylic acid content, and reduced lignin, shikimic acid and maleic acid content relative to control. Plant sustainability implications of modified cell walls on beneficial plant-microbe interactions were explored via co-culture with an ectomycorrhizal fungus, Laccaria bicolor. A significant increase in the mycorrhization rate was observed in transgenic plants, leading to measurable beneficial growth effects. These findings present new evidence for functional interconnectedness of cellulose biosynthesis pathway, metabolism and mycorrhizal association in plants, and further emphasize the consideration of the sustainability implications of plant trait improvement efforts.« less
  • A greater understanding of the genetic regulation of plant cell wall remodeling and the impact of modified cell walls on plant performance is important for the development of sustainable biofuel crops. Here, we studied the impact of down-regulating KORRIGAN-like cell wall biosynthesis genes, belonging to the endo-β-1,4-glucanase gene family, on Populus growth, metabolism and the ability to interact with symbiotic microbes. The reductions in cellulose content and lignin syringyl-to-guaiacyl unit ratio, and increase in cellulose crystallinity of cell walls of PdKOR RNAi plants corroborated the functional role of PdKOR in cell wall biosynthesis. Altered metabolism and reduced growth characteristics ofmore » RNAi plants revealed new implications on carbon allocation and partitioning. The distinctive metabolome phenotype comprised of a higher phenolic and salicylic acid content, and reduced lignin, shikimic acid and maleic acid content relative to control. Plant sustainability implications of modified cell walls on beneficial plant-microbe interactions were explored via co-culture with an ectomycorrhizal fungus, Laccaria bicolor. A significant increase in the mycorrhization rate was observed in transgenic plants, leading to measurable beneficial growth effects. Lastly, these findings present new evidence for functional interconnectedness of cellulose biosynthesis pathway, metabolism and mycorrhizal association in plants, and further emphasize the consideration of the sustainability implications of plant trait improvement efforts.« less