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Title: A Cytosolic Bypass and G6P Shunt in Plants Lacking Peroxisomal Hydroxypyruvate Reductase

Abstract

The oxygenation of ribulose 1,5-bisphosphate by Rubisco is the first step in photorespiration and reduces the efficiency of photosynthesis in C 3 plants. Our recent data indicate that mutants in photorespiration have increased rates of photosynthetic cyclic electron flow around photosystem I. We investigated mutant lines lacking peroxisomal hydroxypyruvate reductase to determine if there are connections between 2-phosphoglycolate accumulation and cyclic electron flow in Arabidopsis (Arabidopsis thaliana). We found that 2-phosphoglycolate is a competitive inhibitor of triose phosphate isomerase, an enzyme in the Calvin-Benson cycle that converts glyceraldehyde 3-phosphate to dihydroxyacetone phosphate. This block in metabolism could be overcome if glyceraldehyde 3-phosphate is exported to the cytosol, where cytosolic triose phosphate isomerase could convert it to dihydroxyacetone phosphate. We found evidence that carbon is reimported as glucose-6-phosphate, forming a cytosolic bypass around the block of stromal triose phosphate isomerase. However, this also stimulates a glucose-6-phosphate shunt, which consumes ATP, which can be compensated by higher rates of cyclic electron flow.

Authors:
ORCiD logo [1]; ORCiD logo [1];  [1]; ORCiD logo [1];  [2];  [1];  [2];  [2]; ORCiD logo [3]; ORCiD logo [4]
  1. Michigan State University-Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, Michigan 48824
  2. Michigan State University-Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, Michigan 48824, Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824
  3. Michigan State University-Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, Michigan 48824, Department of Plant Biology, Michigan State University, East Lansing, Michigan 48824
  4. Michigan State University-Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, Michigan 48824, Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824, Plant Resilience Institute, Michigan State University, East Lansing, Michigan 48824
Publication Date:
Research Org.:
Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1524250
Alternate Identifier(s):
OSTI ID: 1607882
Grant/Contract Number:  
FG02-91ER2002; FG02-91ER20021
Resource Type:
Journal Article: Published Article
Journal Name:
Plant Physiology (Bethesda)
Additional Journal Information:
Journal Name: Plant Physiology (Bethesda) Journal Volume: 180 Journal Issue: 2; Journal ID: ISSN 0032-0889
Publisher:
American Society of Plant Biologists
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Li, Jiying, Weraduwage, Sarathi M., Preiser, Alyssa L., Tietz, Stefanie, Weise, Sean E., Strand, Deserah D., Froehlich, John E., Kramer, David M., Hu, Jianping, and Sharkey, Thomas D. A Cytosolic Bypass and G6P Shunt in Plants Lacking Peroxisomal Hydroxypyruvate Reductase. United States: N. p., 2019. Web. doi:10.1104/pp.19.00256.
Li, Jiying, Weraduwage, Sarathi M., Preiser, Alyssa L., Tietz, Stefanie, Weise, Sean E., Strand, Deserah D., Froehlich, John E., Kramer, David M., Hu, Jianping, & Sharkey, Thomas D. A Cytosolic Bypass and G6P Shunt in Plants Lacking Peroxisomal Hydroxypyruvate Reductase. United States. https://doi.org/10.1104/pp.19.00256
Li, Jiying, Weraduwage, Sarathi M., Preiser, Alyssa L., Tietz, Stefanie, Weise, Sean E., Strand, Deserah D., Froehlich, John E., Kramer, David M., Hu, Jianping, and Sharkey, Thomas D. Mon . "A Cytosolic Bypass and G6P Shunt in Plants Lacking Peroxisomal Hydroxypyruvate Reductase". United States. https://doi.org/10.1104/pp.19.00256.
@article{osti_1524250,
title = {A Cytosolic Bypass and G6P Shunt in Plants Lacking Peroxisomal Hydroxypyruvate Reductase},
author = {Li, Jiying and Weraduwage, Sarathi M. and Preiser, Alyssa L. and Tietz, Stefanie and Weise, Sean E. and Strand, Deserah D. and Froehlich, John E. and Kramer, David M. and Hu, Jianping and Sharkey, Thomas D.},
abstractNote = {The oxygenation of ribulose 1,5-bisphosphate by Rubisco is the first step in photorespiration and reduces the efficiency of photosynthesis in C3 plants. Our recent data indicate that mutants in photorespiration have increased rates of photosynthetic cyclic electron flow around photosystem I. We investigated mutant lines lacking peroxisomal hydroxypyruvate reductase to determine if there are connections between 2-phosphoglycolate accumulation and cyclic electron flow in Arabidopsis (Arabidopsis thaliana). We found that 2-phosphoglycolate is a competitive inhibitor of triose phosphate isomerase, an enzyme in the Calvin-Benson cycle that converts glyceraldehyde 3-phosphate to dihydroxyacetone phosphate. This block in metabolism could be overcome if glyceraldehyde 3-phosphate is exported to the cytosol, where cytosolic triose phosphate isomerase could convert it to dihydroxyacetone phosphate. We found evidence that carbon is reimported as glucose-6-phosphate, forming a cytosolic bypass around the block of stromal triose phosphate isomerase. However, this also stimulates a glucose-6-phosphate shunt, which consumes ATP, which can be compensated by higher rates of cyclic electron flow.},
doi = {10.1104/pp.19.00256},
url = {https://www.osti.gov/biblio/1524250}, journal = {Plant Physiology (Bethesda)},
issn = {0032-0889},
number = 2,
volume = 180,
place = {United States},
year = {2019},
month = {3}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record at https://doi.org/10.1104/pp.19.00256

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Cited by: 10 works
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Works referencing / citing this record:

Does the stromal concentration of P i control chloroplast ATP synthase protein amount in contrasting growth environments?
journal, October 2019


Peroxisomes: versatile organelles with diverse roles in plants
journal, September 2019


Cyanobacterial carboxysomes contain an unique rubisco‐activase‐like protein
journal, October 2019


Wasteful, essential, evolutionary stepping stone? The multiple personalities of the photorespiratory pathway
journal, February 2020


Faster Removal of 2-Phosphoglycolate through Photorespiration Improves Abiotic Stress Tolerance of Arabidopsis
journal, December 2019