Interactions of C4 Subtype Metabolic Activities and Transport in Maize Are Revealed through the Characterization of DCT2 Mutants

Weissmann, Sarit; Ma, Fangfang; Furuyama, Koki; Gierse, James; Berg, Howard; Shao, Ying; Taniguchi, Mitsutaka; Allen, Doug K.; Brutnell, Thomas P.

doi:10.1105/tpc.15.00497

Title: Interactions of C₄ Subtype Metabolic Activities and Transport in Maize Are Revealed through the Characterization of DCT2 Mutants

Abstract

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.

Authors:

^[1];

^[2];

^[3]; Berg, Howard ^[1]; Shao, Ying ^[1];

^[2];

^[3];

^[1]

Donald Danforth Plant Science Center, St. Louis, MO (United States)
Nagoya University (Japan). Graduate School of Bioagricultural Sciences
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:: Tue Jan 26 00:00:00 EST 2016

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:: The 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.

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                    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.  https://doi.org/10.1105/tpc.15.00497

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                    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.  https://doi.org/10.1105/tpc.15.00497.  https://www.osti.gov/servlets/purl/1437256.

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@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      = {The Plant Cell},

  number       = 2,

  volume       = 28,

  place        = {United States},

  year         = {Tue Jan 26 00:00:00 EST 2016},

  month        = {Tue Jan 26 00:00:00 EST 2016}

}

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Works referencing / citing this record:

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The transcriptomic responses of C 4 grasses to subambient CO 2 and low light are largely species specific and only refined by photosynthetic subtype
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Watson‐Lazowski, Alexander; Papanicolaou, Alexie; Koller, Fiona
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DOI: 10.1111/tpj.14583

Metabolite pools and carbon flow during C ₄ photosynthesis in maize: ¹³ CO ₂ labeling kinetics and cell type fractionation
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Arrivault, Stéphanie; Obata, Toshihiro; Szecówka, Marek
Journal of Experimental Botany, Vol. 68, Issue 2
DOI: 10.1093/jxb/erw414

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Title: Interactions of C4 Subtype Metabolic Activities and Transport in Maize Are Revealed through the Characterization of DCT2 Mutants

Abstract

Citation Formats

Dissecting metabolic flux in C4 plants: experimental and theoretical approaches journal, June 2018

Investigating the NAD-ME biochemical pathway within C4 grasses using transcript and amino acid variation in C4 photosynthetic genes journal, August 2018

The molecular evolution of C4 photosynthesis: opportunities for understanding and improving the world’s most productive plants journal, November 2018

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The transcriptomic responses of C 4 grasses to subambient CO 2 and low light are largely species specific and only refined by photosynthetic subtype journal, December 2019

Metabolite pools and carbon flow during C 4 photosynthesis in maize: 13 CO 2 labeling kinetics and cell type fractionation journal, November 2016

Title: Interactions of C₄ Subtype Metabolic Activities and Transport in Maize Are Revealed through the Characterization of DCT2 Mutants

Dissecting metabolic flux in C4 plants: experimental and theoretical approaches
journal, June 2018

Investigating the NAD-ME biochemical pathway within C4 grasses using transcript and amino acid variation in C4 photosynthetic genes
journal, August 2018

The molecular evolution of C4 photosynthesis: opportunities for understanding and improving the world’s most productive plants
journal, November 2018

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journal, December 2019

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journal, November 2016