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Title: Interactions of C 4 Subtype Metabolic Activities and Transport in Maize Are Revealed through the Characterization of DCT2 Mutants

Abstract

C 4 photosynthesis in grasses requires the coordinated movement of metabolites through two specialized leaf cell types, mesophyll (M) and bundle sheath (BS), to concentrate CO 2 around Rubisco. Despite the importance of transporters in this process, few have been identified or rigorously characterized. In maize (Zea mays), DCT2 has been proposed to function as a plastid-localizedmalate transporter and is preferentially expressed in BS cells. Here, we characterized the role of DCT2 in maize leaves using Activator-tagged mutant alleles. Our results indicate that DCT2 enables the transport of malate into the BS chloroplast. Isotopic labeling experiments show that the loss of DCT2 results in markedly different metabolic network operation and dramatically reduced biomass production. In the absence of a functioning malate shuttle, dct2 lines survive through the enhanced use of the phosphoenolpyruvate carboxykinase carbon shuttle pathway that in wild-type maize accounts for ;25% of the photosynthetic activity. The results emphasize the importance of malate transport during C 4 photosynthesis, define the role of a primary malate transporter in BS cells, and support a model for carbon exchange between BS and M cells in maize.

Authors:
ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [3];  [1];  [1]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [1]
  1. Donald Danforth Plant Science Center, St. Louis, MO (United States)
  2. Nagoya University (Japan). Graduate School of Bioagricultural Sciences
  3. Donald Danforth Plant Science Center, St. Louis, MO (United States); U.S. Department of Agriculture, Agricultural Research Service, St. Louis, MO (United States)
Publication Date:
Research Org.:
Donald Danforth Plant Science Center, St. Louis, MO (United States)
Sponsoring Org.:
USDOE Advanced Research Projects Agency - Energy (ARPA-E)
OSTI Identifier:
1437256
Grant/Contract Number:  
AR0000202
Resource Type:
Accepted Manuscript
Journal Name:
Plant Cell
Additional Journal Information:
Journal Volume: 28; Journal Issue: 2; Journal ID: ISSN 1040-4651
Publisher:
American Society of Plant Biologists
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Weissmann, Sarit, Ma, Fangfang, Furuyama, Koki, Gierse, James, Berg, Howard, Shao, Ying, Taniguchi, Mitsutaka, Allen, Doug K., and Brutnell, Thomas P.. Interactions of C4 Subtype Metabolic Activities and Transport in Maize Are Revealed through the Characterization of DCT2 Mutants. United States: N. p., 2016. Web. doi:10.1105/tpc.15.00497.
Weissmann, Sarit, Ma, Fangfang, Furuyama, Koki, Gierse, James, Berg, Howard, Shao, Ying, Taniguchi, Mitsutaka, Allen, Doug K., & Brutnell, Thomas P.. Interactions of C4 Subtype Metabolic Activities and Transport in Maize Are Revealed through the Characterization of DCT2 Mutants. United States. doi:10.1105/tpc.15.00497.
Weissmann, Sarit, Ma, Fangfang, Furuyama, Koki, Gierse, James, Berg, Howard, Shao, Ying, Taniguchi, Mitsutaka, Allen, Doug K., and Brutnell, Thomas P.. Tue . "Interactions of C4 Subtype Metabolic Activities and Transport in Maize Are Revealed through the Characterization of DCT2 Mutants". United States. doi:10.1105/tpc.15.00497. https://www.osti.gov/servlets/purl/1437256.
@article{osti_1437256,
title = {Interactions of C4 Subtype Metabolic Activities and Transport in Maize Are Revealed through the Characterization of DCT2 Mutants},
author = {Weissmann, Sarit and Ma, Fangfang and Furuyama, Koki and Gierse, James and Berg, Howard and Shao, Ying and Taniguchi, Mitsutaka and Allen, Doug K. and Brutnell, Thomas P.},
abstractNote = {C4 photosynthesis in grasses requires the coordinated movement of metabolites through two specialized leaf cell types, mesophyll (M) and bundle sheath (BS), to concentrate CO2 around Rubisco. Despite the importance of transporters in this process, few have been identified or rigorously characterized. In maize (Zea mays), DCT2 has been proposed to function as a plastid-localizedmalate transporter and is preferentially expressed in BS cells. Here, we characterized the role of DCT2 in maize leaves using Activator-tagged mutant alleles. Our results indicate that DCT2 enables the transport of malate into the BS chloroplast. Isotopic labeling experiments show that the loss of DCT2 results in markedly different metabolic network operation and dramatically reduced biomass production. In the absence of a functioning malate shuttle, dct2 lines survive through the enhanced use of the phosphoenolpyruvate carboxykinase carbon shuttle pathway that in wild-type maize accounts for ;25% of the photosynthetic activity. The results emphasize the importance of malate transport during C4 photosynthesis, define the role of a primary malate transporter in BS cells, and support a model for carbon exchange between BS and M cells in maize.},
doi = {10.1105/tpc.15.00497},
journal = {Plant Cell},
number = 2,
volume = 28,
place = {United States},
year = {2016},
month = {1}
}

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