Metabolic profiling reveals altered sugar and secondary metabolism in response to UGPase overexpression in Populus

Raja S. Payyavula; Timothy J. Tschaplinski; Sara S. Jawdy; Robert W. Sykes; Gerald A. Tuskan; Udaya C. Kalluri

doi:10.1186/s12870-014-0265-8

Metabolic profiling reveals altered sugar and secondary metabolism in response to UGPase overexpression in Populus

Raja S. Payyavula
, Timothy J. Tschaplinski
, Sara S. Jawdy
, Robert W. Sykes
, Gerald A. Tuskan
, Udaya C. Kalluri

Research output: Contribution to journal › Article › peer-review

54 Scopus citations

Abstract

Background: UDP-glucose pyrophosphorylase (UGPase) is a sugar-metabolizing enzyme (E.C. 2.7.7.9) that catalyzes a reversible reaction of UDP-glucose and pyrophosphate from glucose-1-phosphate and UTP. UDP-glucose is a key intermediate sugar that is channeled to multiple metabolic pathways. The functional role of UGPase in perennial woody plants is poorly understood.Results: We characterized the functional role of a UGPase gene in Populus deltoides, PdUGPase2. Overexpression of the native gene resulted in increased leaf area and leaf-to-shoot biomass ratio but decreased shoot and root growth. Metabolomic analyses showed that manipulation of PdUGPase2 results in perturbations in primary, as well as secondary metabolism, resulting in reduced sugar and starch levels and increased phenolics, such as caffeoyl and feruloyl conjugates. While cellulose and lignin levels in the cell walls were not significantly altered, the syringyl-to-guaiacyl ratio was significantly reduced.Conclusions: These results demonstrate that PdUGPase2 plays a key role in the tightly coupled primary and secondary metabolic pathways and perturbation in its function results in pronounced effects on growth and metabolism beyond cell wall biosynthesis of Populus.

Original language	English
Article number	265
Journal	BMC Plant Biology
Volume	14
Issue number	1
DOIs	https://doi.org/10.1186/s12870-014-0265-8
State	Published - Oct 7 2014

Funding

We thank Zackary Moore, Lee Gunter and Brock Carter for propagation and maintenance of plants in ORNL greenhouses; Xiaohan Yang, Will Rottmann, Kim Winkler and ArborGen LLC for binary construct development and plant transformation; Kelsey Yee and Mark Davis for HPLC runs of cell wall digests and MBMS analyses, respectively. We also thank Nancy Engle, Sara Allen and Madhavi Martin for assistance with metabolite analyses. This research was funded by the U.S. Department of Energy (DOE) BioEnergy Science Center project. The BioEnergy Science Center is a Bioenergy Research Center supported by the Office of Biological and Environmental Research in the DOE Office of Science. ORNL is managed by UT-Battelle, LLC for the U.S. Department of Energy under Contract Number DE–AC05–00OR22725.

Keywords

Cell wall
Metabolic profiling
Populus
Primary and secondary metabolism
UGPase

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title = "Metabolic profiling reveals altered sugar and secondary metabolism in response to UGPase overexpression in Populus",

abstract = "Background: UDP-glucose pyrophosphorylase (UGPase) is a sugar-metabolizing enzyme (E.C. 2.7.7.9) that catalyzes a reversible reaction of UDP-glucose and pyrophosphate from glucose-1-phosphate and UTP. UDP-glucose is a key intermediate sugar that is channeled to multiple metabolic pathways. The functional role of UGPase in perennial woody plants is poorly understood.Results: We characterized the functional role of a UGPase gene in Populus deltoides, PdUGPase2. Overexpression of the native gene resulted in increased leaf area and leaf-to-shoot biomass ratio but decreased shoot and root growth. Metabolomic analyses showed that manipulation of PdUGPase2 results in perturbations in primary, as well as secondary metabolism, resulting in reduced sugar and starch levels and increased phenolics, such as caffeoyl and feruloyl conjugates. While cellulose and lignin levels in the cell walls were not significantly altered, the syringyl-to-guaiacyl ratio was significantly reduced.Conclusions: These results demonstrate that PdUGPase2 plays a key role in the tightly coupled primary and secondary metabolic pathways and perturbation in its function results in pronounced effects on growth and metabolism beyond cell wall biosynthesis of Populus.",

keywords = "Cell wall, Metabolic profiling, Populus, Primary and secondary metabolism, UGPase",

author = "Payyavula, \{Raja S.\} and Tschaplinski, \{Timothy J.\} and Jawdy, \{Sara S.\} and Sykes, \{Robert W.\} and Tuskan, \{Gerald A.\} and Kalluri, \{Udaya C.\}",

note = "Publisher Copyright: {\textcopyright} 2014 Payyavula et al.; licensee BioMed Central Ltd.",

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doi = "10.1186/s12870-014-0265-8",

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T1 - Metabolic profiling reveals altered sugar and secondary metabolism in response to UGPase overexpression in Populus

AU - Payyavula, Raja S.

AU - Tschaplinski, Timothy J.

AU - Jawdy, Sara S.

AU - Sykes, Robert W.

AU - Tuskan, Gerald A.

AU - Kalluri, Udaya C.

PY - 2014/10/7

Y1 - 2014/10/7

N2 - Background: UDP-glucose pyrophosphorylase (UGPase) is a sugar-metabolizing enzyme (E.C. 2.7.7.9) that catalyzes a reversible reaction of UDP-glucose and pyrophosphate from glucose-1-phosphate and UTP. UDP-glucose is a key intermediate sugar that is channeled to multiple metabolic pathways. The functional role of UGPase in perennial woody plants is poorly understood.Results: We characterized the functional role of a UGPase gene in Populus deltoides, PdUGPase2. Overexpression of the native gene resulted in increased leaf area and leaf-to-shoot biomass ratio but decreased shoot and root growth. Metabolomic analyses showed that manipulation of PdUGPase2 results in perturbations in primary, as well as secondary metabolism, resulting in reduced sugar and starch levels and increased phenolics, such as caffeoyl and feruloyl conjugates. While cellulose and lignin levels in the cell walls were not significantly altered, the syringyl-to-guaiacyl ratio was significantly reduced.Conclusions: These results demonstrate that PdUGPase2 plays a key role in the tightly coupled primary and secondary metabolic pathways and perturbation in its function results in pronounced effects on growth and metabolism beyond cell wall biosynthesis of Populus.

AB - Background: UDP-glucose pyrophosphorylase (UGPase) is a sugar-metabolizing enzyme (E.C. 2.7.7.9) that catalyzes a reversible reaction of UDP-glucose and pyrophosphate from glucose-1-phosphate and UTP. UDP-glucose is a key intermediate sugar that is channeled to multiple metabolic pathways. The functional role of UGPase in perennial woody plants is poorly understood.Results: We characterized the functional role of a UGPase gene in Populus deltoides, PdUGPase2. Overexpression of the native gene resulted in increased leaf area and leaf-to-shoot biomass ratio but decreased shoot and root growth. Metabolomic analyses showed that manipulation of PdUGPase2 results in perturbations in primary, as well as secondary metabolism, resulting in reduced sugar and starch levels and increased phenolics, such as caffeoyl and feruloyl conjugates. While cellulose and lignin levels in the cell walls were not significantly altered, the syringyl-to-guaiacyl ratio was significantly reduced.Conclusions: These results demonstrate that PdUGPase2 plays a key role in the tightly coupled primary and secondary metabolic pathways and perturbation in its function results in pronounced effects on growth and metabolism beyond cell wall biosynthesis of Populus.

KW - Cell wall

KW - Metabolic profiling

KW - Populus

KW - Primary and secondary metabolism

KW - UGPase

UR - https://www.scopus.com/pages/publications/84907957103

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DO - 10.1186/s12870-014-0265-8

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C2 - 25287590

AN - SCOPUS:84907957103

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JO - BMC Plant Biology

JF - BMC Plant Biology

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ER -

Metabolic profiling reveals altered sugar and secondary metabolism in response to UGPase overexpression in Populus

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