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Title: A limited role for carbonic anhydrase in C4 photosynthesis as revealed by a ca1ca2 double mutant in maize.

Abstract

Carbonic anhydrase (CA) catalyzes the first biochemical step of the carbon concentrating mechanism of C4 plants, and in C4 monocots, it has been suggested that CA activity is near limiting for photosynthesis. Here, we test this hypothesis through the characterization of transposon induced mutant alleles of Ca1 and Ca2 in Zea mays. In addition, these two isoforms account for more than 85% of the CA transcript pool. A significant change in isotopic discrimination is observed in mutant plants, which have as little as 3% of wild-type CA activity, but surprisingly, photosynthesis is not reduced under current or elevated pCO2. However, growth and rates of photosynthesis under sub-ambient pCO2 are significantly impaired in the mutants. These findings suggest, that while CA is not limiting for C4 photosynthesis in Z. mays at current pCO2, it likely maintains high rates of photosynthesis when CO2 availability is reduced. Current atmospheric CO2 levels now exceed 400 ppm (~40.53 Pa) and contrast the low CO2 partial pressure (pCO2) conditions under which C4 plants expanded their range ~10 million years ago when the global atmospheric CO2 was below 300 ppm (~30.40 Pa). Thus, as CO2 levels continue to rise, selective pressures for high levels of CA maymore » be limited to arid climates where stomatal closure reduces CO2 availability to the leaf.« less

Authors:
 [1];  [2];  [1];  [1];  [2];  [1]
  1. Donald Danforth Plant Science Center, St. Louis, MO (United States)
  2. Washington State Univ., Pullman, WA (United States)
Publication Date:
Research Org.:
Life Sciences Research Foundation, Baltimore, MD (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
Contributing Org.:
Life Sciences Research Foundation
OSTI Identifier:
1233449
Grant/Contract Number:  
SC0008510
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Plant Physiology (Bethesda)
Additional Journal Information:
Journal Volume: 165; 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

Studer, Anthony J., Gandin, Anthony, Kolbe, Allison R., Wang, Lin, Cousins, Asaph B., and Brutnell, Thomas P. A limited role for carbonic anhydrase in C4 photosynthesis as revealed by a ca1ca2 double mutant in maize.. United States: N. p., 2014. Web. doi:10.1104/pp.114.237602.
Studer, Anthony J., Gandin, Anthony, Kolbe, Allison R., Wang, Lin, Cousins, Asaph B., & Brutnell, Thomas P. A limited role for carbonic anhydrase in C4 photosynthesis as revealed by a ca1ca2 double mutant in maize.. United States. https://doi.org/10.1104/pp.114.237602
Studer, Anthony J., Gandin, Anthony, Kolbe, Allison R., Wang, Lin, Cousins, Asaph B., and Brutnell, Thomas P. 2014. "A limited role for carbonic anhydrase in C4 photosynthesis as revealed by a ca1ca2 double mutant in maize.". United States. https://doi.org/10.1104/pp.114.237602. https://www.osti.gov/servlets/purl/1233449.
@article{osti_1233449,
title = {A limited role for carbonic anhydrase in C4 photosynthesis as revealed by a ca1ca2 double mutant in maize.},
author = {Studer, Anthony J. and Gandin, Anthony and Kolbe, Allison R. and Wang, Lin and Cousins, Asaph B. and Brutnell, Thomas P.},
abstractNote = {Carbonic anhydrase (CA) catalyzes the first biochemical step of the carbon concentrating mechanism of C4 plants, and in C4 monocots, it has been suggested that CA activity is near limiting for photosynthesis. Here, we test this hypothesis through the characterization of transposon induced mutant alleles of Ca1 and Ca2 in Zea mays. In addition, these two isoforms account for more than 85% of the CA transcript pool. A significant change in isotopic discrimination is observed in mutant plants, which have as little as 3% of wild-type CA activity, but surprisingly, photosynthesis is not reduced under current or elevated pCO2. However, growth and rates of photosynthesis under sub-ambient pCO2 are significantly impaired in the mutants. These findings suggest, that while CA is not limiting for C4 photosynthesis in Z. mays at current pCO2, it likely maintains high rates of photosynthesis when CO2 availability is reduced. Current atmospheric CO2 levels now exceed 400 ppm (~40.53 Pa) and contrast the low CO2 partial pressure (pCO2) conditions under which C4 plants expanded their range ~10 million years ago when the global atmospheric CO2 was below 300 ppm (~30.40 Pa). Thus, as CO2 levels continue to rise, selective pressures for high levels of CA may be limited to arid climates where stomatal closure reduces CO2 availability to the leaf.},
doi = {10.1104/pp.114.237602},
url = {https://www.osti.gov/biblio/1233449}, journal = {Plant Physiology (Bethesda)},
issn = {0032-0889},
number = 2,
volume = 165,
place = {United States},
year = {Fri Apr 04 00:00:00 EDT 2014},
month = {Fri Apr 04 00:00:00 EDT 2014}
}

Journal Article:
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Citation Metrics:
Cited by: 67 works
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Figures / Tables:

Figure 1 Figure 1: Ds insertional mutants disrupt the two most highly expressed CA genes. (a) Unique RNA-seq reads from the tip of the 3rd leaf of a maize seedling were mapped to the 3’ UTR of each carbonic anhydrase gene to quantify the expression of each member of the gene familymore » (see Materials and Methods for description of RNA-seq read mapping). (b) Insertional mutagenesis of the tandemly arranged carbonic anhydrase genes on maize chromosome 3. Gene models are drawn to scale. Red and blue boxes represent exons of Ca1 and Ca2, respectively, and grey boxes denote UTRs. Bronze triangles show the position and orientation of donor Ds elements used to generate the insertion alleles characterized (purple triangles). Black corners of triangles show the promoter proximal end of the Ds element. (c) Immunoblot of wild-type and Ds lines challenged with an antibody raised against rice CA. The black arrow indicates the predominant CA isoform, which is absent in both ca1 single and ca1ca2 double mutants.« less

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Works referencing / citing this record:

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


C 4 photosynthesis in C 3 rice: a theoretical analysis of biochemical and anatomical factors: C 4 photosynthesis in C 3 rice
journal, October 2016


The draft genome of the C3 panicoid grass species Dichanthelium oligosanthes
journal, October 2016


Cross species selection scans identify components of C 4 photosynthesis in the grasses
journal, July 2016


Herbarium genomics retraces the origins of C 4 -specific carbonic anhydrase in Andropogoneae (Poaceae)
journal, March 2018


Translocation of Drought-Responsive Proteins from the Chloroplasts
journal, January 2020


Molecular diversity and selective sweeps in maize inbred lines adapted to African highlands
journal, September 2019


Emerging roles for carbonic anhydrase in mesophyll conductance and photosynthesis
journal, January 2020


Molecular diversity and selective sweeps in maize inbred lines adapted to African highlands
journal, September 2019


Cross species selection scans identify components of C 4 photosynthesis in the grasses
journal, July 2016


Effects of reduced carbonic anhydrase activity on CO 2 assimilation rates in Setaria viridis : a transgenic analysis
journal, October 2016


Translocation of Drought-Responsive Proteins from the Chloroplasts
journal, January 2020


Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.