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

Studer, Anthony J.; Gandin, Anthony; Kolbe, Allison R.; Wang, Lin; Cousins, Asaph B.; Brutnell, Thomas P.

doi:10.1104/pp.114.237602

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

Journal Article · Fri Apr 04 00:00:00 EDT 2014 · Plant Physiology (Bethesda)

DOI:https://doi.org/10.1104/pp.114.237602· OSTI ID:1233449

Studer, Anthony J. ^[1]; Gandin, Anthony ^[2]; Kolbe, Allison R. ^[1]; Wang, Lin ^[1]; Cousins, Asaph B. ^[2]; Brutnell, Thomas P. ^[1]

Donald Danforth Plant Science Center, St. Louis, MO (United States)
Washington State Univ., Pullman, WA (United States)

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.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Life Sciences Research Foundation, Baltimore, MD (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Contributing Organization:: Life Sciences Research Foundation

Grant/Contract Number:: SC0008510

OSTI ID:: 1233449

Journal Information:: Plant Physiology (Bethesda), Vol. 165, Issue 2; ISSN 0032-0889

Publisher:: American Society of Plant BiologistsCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 67 works

Citation information provided by
Web of Science

References (46)

Regional mutagenesis using Dissociation in maize Ahern, K. Methods, Vol. 49, Issue 3 https://doi.org/10.1016/j.ymeth.2009.04.009	journal	November 2009
Somatic variegation and germinal mutability reflect the position of transposable element Dissociation within the maize R gene. Alleman, M.; Kermicle, J. L. Genetics, Vol. 135, Issue 1 https://doi.org/10.1093/genetics/135.1.189	journal	September 1993
Carbonic Anhydrase Activity Associated with the Cyanobacterium Synechococcus PCC7942 Badger, Murray R.; Price, G. Dean Plant Physiology, Vol. 89, Issue 1 https://doi.org/10.1104/pp.89.1.51	journal	January 1989
The Role of Carbonic Anhydrase in Photosynthesis Badger, M. R.; Price, G. D. Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 45, Issue 1 https://doi.org/10.1146/annurev.pp.45.060194.002101	journal	June 1994
Tunable diode laser absorption spectroscopy for stable isotope studies of ecosystem–atmosphere CO2 exchange Bowling, David R.; Sargent, Steve D.; Tanner, Bert D. Agricultural and Forest Meteorology, Vol. 118, Issue 1-2 https://doi.org/10.1016/S0168-1923(03)00074-1	journal	August 2003
Ac-Immobilized , a Stable Source of Activator Transposase That Mediates Sporophytic and Gametophytic Excision of Dissociation Elements in Maize Conrad, Liza J.; Brutnell, Thomas P. Genetics, Vol. 171, Issue 4 https://doi.org/10.1534/genetics.105.046623	journal	December 2005
Carbonic Anhydrase and Its Influence on Carbon Isotope Discrimination during C ₄ Photosynthesis. Insights from Antisense RNA in Flaveria bidentis Cousins, Asaph B.; Badger, Murray R.; von Caemmerer, Susanne Plant Physiology, Vol. 141, Issue 1 https://doi.org/10.1104/pp.106.077776	journal	March 2006
A Transgenic Approach to Understanding the Influence of Carbonic Anhydrase on C ¹⁸ OO Discrimination during C ₄ Photosynthesis Cousins, Asaph B.; Badger, Murray R.; von Caemmerer, Susanne Plant Physiology, Vol. 142, Issue 2 https://doi.org/10.1104/pp.106.085167	journal	August 2006
C4 photosynthetic isotope exchange in NAD-ME- and NADP-ME-type grasses Cousins, Asaph B.; Badger, Murray R.; von Caemmerer, Susanne Journal of Experimental Botany, Vol. 59, Issue 7 https://doi.org/10.1093/jxb/ern001	journal	March 2008
The Origins of C4 Grasslands: Integrating Evolutionary and Ecosystem Science Edwards, E. J.; Osborne, C. P.; Stromberg, C. A. E. Science, Vol. 328, Issue 5978 https://doi.org/10.1126/science.1177216	journal	April 2010
Carbon Isotope Discrimination measured Concurrently with Gas Exchange to Investigate CO2 Diffusion in Leaves of Higher Plants Evans, Jr; Sharkey, Td; Berry, Ja Functional Plant Biology, Vol. 13, Issue 2 https://doi.org/10.1071/PP9860281	journal	January 1986
Ternary effects on the gas exchange of isotopologues of carbon dioxide: Ternary effects on CO2 isotopologues Farquhar, Graham D.; Cernusak, Lucas A. Plant, Cell & Environment, Vol. 35, Issue 7 https://doi.org/10.1111/j.1365-3040.2012.02484.x	journal	February 2012
A gene homologous to chloroplast carbonic anhydrase (icfA) is essential to photosynthetic carbon dioxide fixation by Synechococcus PCC7942. Fukuzawa, H.; Suzuki, E.; Komukai, Y. Proceedings of the National Academy of Sciences, Vol. 89, Issue 10 https://doi.org/10.1073/pnas.89.10.4437	journal	May 1992
Intracellular Carbonic Anhydrase Is Essential to Photosynthesis in Chlamydomonas reinhardtii at Atmospheric Levels of CO2 (Demonstration via Genomic Complementation of the High-CO2-Requiring Mutant ca-1) Funke, R. P.; Kovar, J. L.; Weeks, D. P. Plant Physiology, Vol. 114, Issue 1 https://doi.org/10.1104/pp.114.1.237	journal	May 1997
Influence of Carbonic Anhydrase Activity in Terrestrial Vegetation on the 18O Content of Atmospheric CO2 Gillon, J. Science, Vol. 291, Issue 5513 https://doi.org/10.1126/science.1056374	journal	March 2001
Carbonic Anhydrase Activity in Leaves and Its Role in the First Step of C ₄ Photosynthesis Hatch, Marshall D.; Burnell, James N. Plant Physiology, Vol. 93, Issue 2 https://doi.org/10.1104/pp.93.2.825	journal	June 1990
Functional Diversity, Conservation, and Convergence in the Evolution of the α-, β-, and γ-Carbonic Anhydrase Gene Families Hewett-Emmett, David; Tashian, Richard E. Molecular Phylogenetics and Evolution, Vol. 5, Issue 1 https://doi.org/10.1006/mpev.1996.0006	journal	February 1996
The Regulation of Gene Expression Required for C ₄ Photosynthesis Hibberd, Julian M.; Covshoff, Sarah Annual Review of Plant Biology, Vol. 61, Issue 1 https://doi.org/10.1146/annurev-arplant-042809-112238	journal	June 2010
Carbonic anhydrases are upstream regulators of CO2-controlled stomatal movements in guard cells Hu, Honghong; Boisson-Dernier, Aurélien; Israelsson-Nordström, Maria Nature Cell Biology, Vol. 12, Issue 1 https://doi.org/10.1038/ncb2009	journal	December 2009
Inorganic Carbon Diffusion between C ₄ Mesophyll and Bundle Sheath Cells : Direct Bundle Sheath CO Jenkins, Colin L. D.; Furbank, Robert T.; Hatch, Marshall D. Plant Physiology, Vol. 91, Issue 4 https://doi.org/10.1104/pp.91.4.1356	journal	December 1989
Photosynthesis, Productivity, and Yield of Maize Are Not Affected by Open-Air Elevation of CO ₂ Concentration in the Absence of Drought Leakey, Andrew D. B.; Uribelarrea, Martin; Ainsworth, Elizabeth A. Plant Physiology, Vol. 140, Issue 2 https://doi.org/10.1104/pp.105.073957	journal	January 2006
Fast and accurate short read alignment with Burrows-Wheeler transform Li, H.; Durbin, R. Bioinformatics, Vol. 25, Issue 14 https://doi.org/10.1093/bioinformatics/btp324	journal	May 2009
The developmental dynamics of the maize leaf transcriptome Li, Pinghua; Ponnala, Lalit; Gandotra, Neeru Nature Genetics, Vol. 42, Issue 12, p. 1060-1067 https://doi.org/10.1038/ng.703	journal	October 2010
Extrinsic Photosystem II Carbonic Anhydrase in Maize Mesophyll Chloroplasts Lu, Yih-Kuang; Stemler, Alan J. Plant Physiology, Vol. 128, Issue 2 https://doi.org/10.1104/pp.010643	journal	February 2002
Carbonic anhydrase and the molecular evolution of C4 photosynthesis: Carbonic anhydrase and C4 photosynthesis Ludwig, Martha Plant, Cell & Environment, Vol. 35, Issue 1 https://doi.org/10.1111/j.1365-3040.2011.02364.x	journal	July 2011
Carbon kinetic isotope effects on the hydration of carbon dioxide and the dehydration of bicarbonate ion Marlier, John F.; O'Leary, Marion H. Journal of the American Chemical Society, Vol. 106, Issue 18 https://doi.org/10.1021/ja00330a003	journal	September 1984
Carbon isotope fractionation between dissolved bicarbonate and gaseous carbon dioxide Mook, W. G.; Bommerson, J. C.; Staverman, W. H. Earth and Planetary Science Letters, Vol. 22, Issue 2, p. 169-176 https://doi.org/10.1016/0012-821X(74)90078-8	journal	May 1974
Carbonic anhydrases in plants and algae: Carbonic anhydrases in plants and algae Moroney, J. V.; Bartlett, S. G.; Samuelsson, G. Plant, Cell & Environment, Vol. 24, Issue 2 https://doi.org/10.1111/j.1365-3040.2001.00669.x	journal	February 2001
The carbonic anhydrase isoforms of Chlamydomonas reinhardtii: intracellular location, expression, and physiological roles Moroney, James V.; Ma, Yunbing; Frey, Wesley D. Photosynthesis Research, Vol. 109, Issue 1-3 https://doi.org/10.1007/s11120-011-9635-3	journal	March 2011
Carbon isotope fractionation in plants O'Leary, Marion H. Phytochemistry, Vol. 20, Issue 4 https://doi.org/10.1016/0031-9422(81)85134-5	journal	January 1981
Measurement of the isotope fractionation associated with diffusion of carbon dioxide in aqueous solution O'Leary, Marion H. The Journal of Physical Chemistry, Vol. 88, Issue 4 https://doi.org/10.1021/j150648a041	journal	February 1984
Carbon isotope effect on dehydration of bicarbonate ion catalyzed by carbonic anhydrase Paneth, Piotr; O'Leary, Marion H. Biochemistry, Vol. 24, Issue 19 https://doi.org/10.1021/bi00340a028	journal	September 1985
The C4 plant lineages of planet Earth Sage, R. F.; Christin, P. -A.; Edwards, E. J. Journal of Experimental Botany, Vol. 62, Issue 9 https://doi.org/10.1093/jxb/err048	journal	March 2011
Effects of low atmospheric CO2 on plants: more than a thing of the past Sage, Rowan F.; Coleman, John R. Trends in Plant Science, Vol. 6, Issue 1 https://doi.org/10.1016/S1360-1385(00)01813-6	journal	January 2001
Photorespiration and the Evolution of C ₄ Photosynthesis Sage, Rowan F.; Sage, Tammy L.; Kocacinar, Ferit Annual Review of Plant Biology, Vol. 63, Issue 1 https://doi.org/10.1146/annurev-arplant-042811-105511	journal	June 2012
Carboxylating enzymes and carbonic anhydrase functions were suppressed by zinc deficiency in maize and chickpea plants Salama, Zeinab A.; El-Fouly, Mohamed M.; Lazova, Galia Acta Physiologiae Plantarum, Vol. 28, Issue 5 https://doi.org/10.1007/BF02706627	journal	October 2006
Genome-wide atlas of transcription during maize development Sekhon, Rajandeep S.; Lin, Haining; Childs, Kevin L. The Plant Journal, Vol. 66, Issue 4, p. 553-563 https://doi.org/10.1111/j.1365-313X.2011.04527.x	journal	March 2011
Characterization of a mutant lacking carboxysomal carbonic anhydrase from the cyanobacterium Synechocystis PCC6803 So, Anthony K.; John-McKay, Meryl; Espie, George S. Planta, Vol. 214, Issue 3 https://doi.org/10.1007/s004250100638	journal	September 2001
The efficiency of C4 photosynthesis under low light conditions: assumptions and calculations with CO2 isotope discrimination Ubierna, Nerea; Sun, Wei; Cousins, Asaph B. Journal of Experimental Botany, Vol. 62, Issue 9 https://doi.org/10.1093/jxb/err073	journal	April 2011
The efficiency of C ₄ photosynthesis under low light conditions in Zea mays , Miscanthus x giganteus and Flaveria bidentis : Efficiency of light-limited C Ubierna, Nerea; Sun, Wei; Kramer, David M. Plant, Cell & Environment, Vol. 36, Issue 2 https://doi.org/10.1111/j.1365-3040.2012.02579.x	journal	August 2012
Genome-Wide Distribution of Transposed Dissociation Elements in Maize Vollbrecht, Erik; Duvick, Jon; Schares, Justin P. The Plant Cell, Vol. 22, Issue 6 https://doi.org/10.1105/tpc.109.073452	journal	June 2010
Carbonic anhydrase and C4 photosynthesis: a transgenic analysis Von Caemmerer, S.; Quinn, V.; Hancock, N. C. Plant, Cell and Environment, Vol. 27, Issue 6 https://doi.org/10.1111/j.1365-3040.2003.01157.x	journal	June 2004
Temperature response of in vivo Rubisco kinetics and mesophyll conductance in Arabidopsis thaliana : comparisons to Nicotiana tabacum Walker, Berkley; Ariza, Loren S.; Kaines, Sarah Plant, Cell & Environment, Vol. 36, Issue 12 https://doi.org/10.1111/pce.12166	journal	August 2013
A Low-Cost Library Construction Protocol and Data Analysis Pipeline for Illumina-Based Strand-Specific Multiplex RNA-Seq Wang, Lin; Si, Yaqing; Dedow, Lauren K. PLoS ONE, Vol. 6, Issue 10 https://doi.org/10.1371/journal.pone.0026426	journal	October 2011
Comparative genomic analysis of C4 photosynthetic pathway evolution in grasses Wang, Xiyin; Gowik, Udo; Tang, Haibao Genome Biology, Vol. 10, Issue 6 https://doi.org/10.1186/gb-2009-10-6-r68	journal	January 2009
Genome sequence of foxtail millet (Setaria italica) provides insights into grass evolution and biofuel potential Zhang, Gengyun; Liu, Xin; Quan, Zhiwu Nature Biotechnology, Vol. 30, Issue 6 https://doi.org/10.1038/nbt.2195	journal	May 2012

Cited By (16)

The molecular evolution of C4 photosynthesis: opportunities for understanding and improving the world’s most productive plants Niklaus, Michael; Kelly, Steven Journal of Experimental Botany, Vol. 70, Issue 3 https://doi.org/10.1093/jxb/ery416	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 Wang, Shuyue; Tholen, Danny; Zhu, Xin-Guang Plant, Cell & Environment, Vol. 40, Issue 1 https://doi.org/10.1111/pce.12834	journal	October 2016
The draft genome of the C3 panicoid grass species Dichanthelium oligosanthes Studer, Anthony J.; Schnable, James C.; Weissmann, Sarit Genome Biology, Vol. 17, Issue 1 https://doi.org/10.1186/s13059-016-1080-3	journal	October 2016
Cross species selection scans identify components of C ₄ photosynthesis in the grasses Huang, Pu; Studer, Anthony J.; Schnable, James C. Journal of Experimental Botany, Vol. 68, Issue 2 https://doi.org/10.1093/jxb/erw256	journal	July 2016
Insights from transcriptome profiling on the non-photosynthetic and stomatal signaling response of maize carbonic anhydrase mutants to low CO2 Kolbe, Allison R.; Studer, Anthony J.; Cornejo, Omar E. BMC Genomics, Vol. 20, Issue 1 https://doi.org/10.1186/s12864-019-5522-7	journal	February 2019
Herbarium genomics retraces the origins of C ₄ -specific carbonic anhydrase in Andropogoneae (Poaceae) Besnard, Guillaume; Bianconi, Matheus E.; Hackel, Jan Botany Letters, Vol. 165, Issue 3-4 https://doi.org/10.1080/23818107.2018.1469429	journal	March 2018
Three-dimensional microscale modelling of CO ₂ transport and light propagation in tomato leaves enlightens photosynthesis : 3-D modelling of photosynthesis in leaves Ho, Quang Tri; Berghuijs, Herman N. C.; Watté, Rodrigo Plant, Cell & Environment, Vol. 39, Issue 1 https://doi.org/10.1111/pce.12590	journal	July 2015
Identification and characterization of long non-coding RNAs involved in osmotic and salt stress in Medicago truncatula using genome-wide high-throughput sequencing Wang, Tian-Zuo; Liu, Min; Zhao, Min-Gui BMC Plant Biology, Vol. 15, Issue 1 https://doi.org/10.1186/s12870-015-0530-5	journal	June 2015
Translocation of Drought-Responsive Proteins from the Chloroplasts Li, Ping; Liu, Haoju; Yang, Hong Cells, Vol. 9, Issue 1 https://doi.org/10.3390/cells9010259	journal	January 2020
Online CO ₂ and H ₂ O oxygen isotope fractionation allows estimation of mesophyll conductance in C ₄ plants, and reveals that mesophyll conductance decreases as leaves age in both C ₄ and C ₃ plants Barbour, Margaret M.; Evans, John R.; Simonin, Kevin A. New Phytologist, Vol. 210, Issue 3 https://doi.org/10.1111/nph.13830	journal	January 2016
Molecular diversity and selective sweeps in maize inbred lines adapted to African highlands Wegary, Dagne; Teklewold, Adefris; Prasanna, Boddupalli M. Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-49861-z	journal	September 2019
Emerging roles for carbonic anhydrase in mesophyll conductance and photosynthesis Momayyezi, Mina; McKown, Athena D.; Bell, Shannon C. S. The Plant Journal, Vol. 101, Issue 4 https://doi.org/10.1111/tpj.14638	journal	January 2020
Effects of reduced carbonic anhydrase activity on CO ₂ assimilation rates in Setaria viridis : a transgenic analysis Osborn, Hannah L.; Alonso-Cantabrana, Hugo; Sharwood, Robert E. Journal of Experimental Botany, Vol. 68, Issue 2 https://doi.org/10.1093/jxb/erw357	journal	October 2016
Identification of Photosynthesis-Associated C4 Candidate Genes through Comparative Leaf Gradient Transcriptome in Multiple Lineages of C3 and C4 Species Ding, Zehong; Weissmann, Sarit; Wang, Minghui PLOS ONE, Vol. 10, Issue 10 https://doi.org/10.1371/journal.pone.0140629	journal	October 2015
Multiscale Metabolic Modeling of C4 Plants: Connecting Nonlinear Genome-Scale Models to Leaf-Scale Metabolism in Developing Maize Leaves Bogart, Eli; Myers, Christopher R. PLOS ONE, Vol. 11, Issue 3 https://doi.org/10.1371/journal.pone.0151722	journal	March 2016
Real-Time Determination of Photosynthesis, Transpiration, Water-Use Efficiency and Gene Expression of Two Sorghum bicolor (Moench) Genotypes Subjected to Dry-Down Fracasso, Alessandra; Magnanini, Eugenio; Marocco, Adriano Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00932	journal	May 2017