Three distinct biochemical subtypes of C-4 photosynthesis? A modelling analysis

Wang Y, Bräutigam A, Weber APM, Zhu X-G (2014)
Journal of Experimental Botany 65(13): 3567-3578.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
Download
OA 3.55 MB
Autor*in
Wang, Yu; Bräutigam, AndreaUniBi ; Weber, Andreas P. M.; Zhu, Xin-Guang
Abstract / Bemerkung
C-4 photosynthesis has higher light-use, nitrogen-use, and water-use efficiencies than C-3 photosynthesis. Historically, most of C-4 plants were classified into three subtypes (NADP-malic enzyme (ME), NAD-ME, or phosphoenolpyruvate carboxykinase (PEPCK) subtypes) according to their major decarboxylation enzyme. However, a wealth of historic and recent data indicates that flexibility exists between different decarboxylation pathways in many C-4 species, and this flexibility might be controlled by developmental and environmental cues. This work used systems modelling to theoretically explore the significance of flexibility in decarboxylation mechanisms and transfer acids utilization. The results indicate that employing mixed C-4 pathways, either the NADP-ME type with the PEPCK type or the NAD-ME type with the PEPCK type, effectively decreases the need to maintain high concentrations and concentration gradients of transport metabolites. Further, maintaining a mixture of C-4 pathways robustly affords high photosynthetic efficiency under a broad range of light regimes. A pure PEPCK-type C-4 photosynthesis is not beneficial because the energy requirements in bundle sheath cells cannot be fulfilled due to them being shaded by mesophyll cells. Therefore, only two C-4 subtypes should be considered as distinct subtypes, the NADP-ME type and NAD-ME types, which both inherently involve a supplementary PEPCK cycle.
Stichworte
Efficiency; flexibility; mixture; NADP-ME; NAD-ME; PEPCK
Erscheinungsjahr
2014
Zeitschriftentitel
Journal of Experimental Botany
Band
65
Ausgabe
13
Seite(n)
3567-3578
ISSN
0022-0957
eISSN
1460-2431
Page URI
https://pub.uni-bielefeld.de/record/2915135

Zitieren

Wang Y, Bräutigam A, Weber APM, Zhu X-G. Three distinct biochemical subtypes of C-4 photosynthesis? A modelling analysis. Journal of Experimental Botany. 2014;65(13):3567-3578.
Wang, Y., Bräutigam, A., Weber, A. P. M., & Zhu, X. - G. (2014). Three distinct biochemical subtypes of C-4 photosynthesis? A modelling analysis. Journal of Experimental Botany, 65(13), 3567-3578. doi:10.1093/jxb/eru058
Wang, Yu, Bräutigam, Andrea, Weber, Andreas P. M., and Zhu, Xin-Guang. 2014. “Three distinct biochemical subtypes of C-4 photosynthesis? A modelling analysis”. Journal of Experimental Botany 65 (13): 3567-3578.
Wang, Y., Bräutigam, A., Weber, A. P. M., and Zhu, X. - G. (2014). Three distinct biochemical subtypes of C-4 photosynthesis? A modelling analysis. Journal of Experimental Botany 65, 3567-3578.
Wang, Y., et al., 2014. Three distinct biochemical subtypes of C-4 photosynthesis? A modelling analysis. Journal of Experimental Botany, 65(13), p 3567-3578.
Y. Wang, et al., “Three distinct biochemical subtypes of C-4 photosynthesis? A modelling analysis”, Journal of Experimental Botany, vol. 65, 2014, pp. 3567-3578.
Wang, Y., Bräutigam, A., Weber, A.P.M., Zhu, X.-G.: Three distinct biochemical subtypes of C-4 photosynthesis? A modelling analysis. Journal of Experimental Botany. 65, 3567-3578 (2014).
Wang, Yu, Bräutigam, Andrea, Weber, Andreas P. M., and Zhu, Xin-Guang. “Three distinct biochemical subtypes of C-4 photosynthesis? A modelling analysis”. Journal of Experimental Botany 65.13 (2014): 3567-3578.
Alle Dateien verfügbar unter der/den folgenden Lizenz(en):
Copyright Statement:
Dieses Objekt ist durch das Urheberrecht und/oder verwandte Schutzrechte geschützt. [...]
Volltext(e)
Access Level
OA Open Access
Zuletzt Hochgeladen
2019-09-06T09:18:54Z
MD5 Prüfsumme
ee2160d2f12c25186713a2fe048a222d


52 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

The role of alanine and aspartate aminotransferases in C4 photosynthesis.
Schlüter U, Bräutigam A, Droz JM, Schwender J, Weber APM., Plant Biol (Stuttg) 21 Suppl 1(), 2019
PMID: 30126035
The genome of broomcorn millet.
Zou C, Li L, Miki D, Li D, Tang Q, Xiao L, Rajput S, Deng P, Peng L, Jia W, Huang R, Zhang M, Sun Y, Hu J, Fu X, Schnable PS, Chang Y, Li F, Zhang H, Feng B, Zhu X, Liu R, Schnable JC, Zhu JK, Zhang H., Nat Commun 10(1), 2019
PMID: 30683860
Decarboxylation mechanisms of C4 photosynthesis in Saccharum spp.: increased PEPCK activity under water-limiting conditions.
Cacefo V, Ribas AF, Zilliani RR, Neris DM, Domingues DS, Moro AL, Vieira LGE., BMC Plant Biol 19(1), 2019
PMID: 30991938
Key changes in gene expression identified for different stages of C4 evolution in Alloteropsis semialata.
Dunning LT, Moreno-Villena JJ, Lundgren MR, Dionora J, Salazar P, Adams C, Nyirenda F, Olofsson JK, Mapaura A, Grundy IM, Kayombo CJ, Dunning LA, Kentatchime F, Ariyarathne M, Yakandawala D, Besnard G, Quick WP, Bräutigam A, Osborne CP, Christin PA., J Exp Bot 70(12), 2019
PMID: 30949663
The Impacts of Fluctuating Light on Crop Performance.
Slattery RA, Walker BJ, Weber APM, Ort DR., Plant Physiol 176(2), 2018
PMID: 29192028
Maize leaf PPDK regulatory protein isoform-2 is specific to bundle sheath chloroplasts and paradoxically lacks a Pi-dependent PPDK activation activity.
Chastain CJ, Baird LM, Walker MT, Bergman CC, Novbatova GT, Mamani-Quispe CS, Burnell JN., J Exp Bot 69(5), 2018
PMID: 29281064
Multiple mechanisms for enhanced plasmodesmata density in disparate subtypes of C4 grasses.
Danila FR, Quick WP, White RG, Kelly S, von Caemmerer S, Furbank RT., J Exp Bot 69(5), 2018
PMID: 29300922
The intracellular distribution of inorganic carbon fixing enzymes does not support the presence of a C4 pathway in the diatom Phaeodactylum tricornutum.
Ewe D, Tachibana M, Kikutani S, Gruber A, Río Bártulos C, Konert G, Kaplan A, Matsuda Y, Kroth PG., Photosynth Res 137(2), 2018
PMID: 29572588
Shade compromises the photosynthetic efficiency of NADP-ME less than that of PEP-CK and NAD-ME C4 grasses.
Sonawane BV, Sharwood RE, Whitney S, Ghannoum O., J Exp Bot 69(12), 2018
PMID: 29659931
C4 photosynthesis and transition of Kranz anatomy in cotyledons and leaves of Tetraena simplex.
Muhaidat R, McKown AD, Al Zoubi M, Bani Domi Z, Otoum O., Am J Bot 105(5), 2018
PMID: 29791720
Synergistic Binding of bHLH Transcription Factors to the Promoter of the Maize NADP-ME Gene Used in C4 Photosynthesis Is Based on an Ancient Code Found in the Ancestral C3 State.
Borba AR, Serra TS, Górska A, Gouveia P, Cordeiro AM, Reyna-Llorens I, Knerová J, Barros PM, Abreu IA, Oliveira MM, Hibberd JM, Saibo NJM., Mol Biol Evol 35(7), 2018
PMID: 29659975
Investigating the NAD-ME biochemical pathway within C4 grasses using transcript and amino acid variation in C4 photosynthetic genes.
Watson-Lazowski A, Papanicolaou A, Sharwood R, Ghannoum O., Photosynth Res 138(2), 2018
PMID: 30078073
C3 cotyledons are followed by C4 leaves: intra-individual transcriptome analysis of Salsola soda (Chenopodiaceae).
Lauterbach M, Billakurthi K, Kadereit G, Ludwig M, Westhoff P, Gowik U., J Exp Bot 68(2), 2017
PMID: 27660482
C4 photosynthesis in C3 rice: a theoretical analysis of biochemical and anatomical factors.
Wang S, Tholen D, Zhu XG., Plant Cell Environ 40(1), 2017
PMID: 27628301
Metabolite pools and carbon flow during C4 photosynthesis in maize: 13CO2 labeling kinetics and cell type fractionation.
Arrivault S, Obata T, Szecówka M, Mengin V, Guenther M, Hoehne M, Fernie AR, Stitt M., J Exp Bot 68(2), 2017
PMID: 27834209
Walking the C4 pathway: past, present, and future.
Furbank RT., J Exp Bot 68(2), 2017
PMID: 28110279
Freeze-quenched maize mesophyll and bundle sheath separation uncovers bias in previous tissue-specific RNA-Seq data.
Denton AK, Maß J, Külahoglu C, Lercher MJ, Bräutigam A, Weber AP., J Exp Bot 68(2), 2017
PMID: 28043950
Shared characteristics underpinning C4 leaf maturation derived from analysis of multiple C3 and C4 species of Flaveria.
Kümpers BM, Burgess SJ, Reyna-Llorens I, Smith-Unna R, Boursnell C, Hibberd JM., J Exp Bot 68(2), 2017
PMID: 28062590
Phylogenic and phosphorylation regulation difference of phosphoenolpyruvate carboxykinase of C3 and C4 plants.
Shen Z, Dong XM, Gao ZF, Chao Q, Wang BC., J Plant Physiol 213(), 2017
PMID: 28285130
Exploiting the Genetic Diversity of Maize Using a Combined Metabolomic, Enzyme Activity Profiling, and Metabolic Modeling Approach to Link Leaf Physiology to Kernel Yield.
Cañas RA, Yesbergenova-Cuny Z, Simons M, Chardon F, Armengaud P, Quilleré I, Cukier C, Gibon Y, Limami AM, Nicolas S, Brulé L, Lea PJ, Maranas CD, Hirel B., Plant Cell 29(5), 2017
PMID: 28396554
Strategies and tools to improve crop productivity by targeting photosynthesis.
Nuccio ML, Potter L, Stiegelmeyer SM, Curley J, Cohn J, Wittich PE, Tan X, Davis J, Ni J, Trullinger J, Hall R, Bate NJ., Philos Trans R Soc Lond B Biol Sci 372(1730), 2017
PMID: 28808096
Recruitment of pre-existing networks during the evolution of C4 photosynthesis.
Reyna-Llorens I, Hibberd JM., Philos Trans R Soc Lond B Biol Sci 372(1730), 2017
PMID: 28808102
Short-term thermal photosynthetic responses of C4 grasses are independent of the biochemical subtype.
Sonawane BV, Sharwood RE, von Caemmerer S, Whitney SM, Ghannoum O., J Exp Bot 68(20), 2017
PMID: 29045727
De novo Transcriptome Assembly and Comparison of C3, C3-C4, and C4 Species of Tribe Salsoleae (Chenopodiaceae).
Lauterbach M, Schmidt H, Billakurthi K, Hankeln T, Westhoff P, Gowik U, Kadereit G., Front Plant Sci 8(), 2017
PMID: 29184562
C4 Photosynthesis in the Rice Paddy: Insights from the Noxious Weed Echinochloa glabrescens.
Covshoff S, Szecowka M, Hughes TE, Smith-Unna R, Kelly S, Bailey KJ, Sage TL, Pachebat JA, Leegood R, Hibberd JM., Plant Physiol 170(1), 2016
PMID: 26527656
Interactions of C4 Subtype Metabolic Activities and Transport in Maize Are Revealed through the Characterization of DCT2 Mutants.
Weissmann S, Ma F, Furuyama K, Gierse J, Berg H, Shao Y, Taniguchi M, Allen DK, Brutnell TP., Plant Cell 28(2), 2016
PMID: 26813621
Photorespiration connects C3 and C4 photosynthesis.
Bräutigam A, Gowik U., J Exp Bot 67(10), 2016
PMID: 26912798
Temperature response of bundle-sheath conductance in maize leaves.
Yin X, van der Putten PE, Driever SM, Struik PC., J Exp Bot 67(9), 2016
PMID: 26969744
Walking the C4 pathway: past, present, and future.
Furbank RT., J Exp Bot 67(14), 2016
PMID: 27059273
Engineering C4 photosynthesis into C3 chassis in the synthetic biology age.
Schuler ML, Mantegazza O, Weber AP., Plant J 87(1), 2016
PMID: 26945781
Analysis of gene expression and histone modification between C4 and non-C4 homologous genes of PPDK and PCK in maize.
Dong XM, Li Y, Chao Q, Shen J, Gong XJ, Zhao BG, Wang BC., Photosynth Res 129(1), 2016
PMID: 27161567
The Roles of Organic Acids in C4 Photosynthesis.
Ludwig M., Front Plant Sci 7(), 2016
PMID: 27242848
Nitrogen assimilation system in maize is regulated by developmental and tissue-specific mechanisms.
Plett D, Holtham L, Baumann U, Kalashyan E, Francis K, Enju A, Toubia J, Roessner U, Bacic A, Rafalski A, Dhugga KS, Tester M, Garnett T, Kaiser BN., Plant Mol Biol 92(3), 2016
PMID: 27511191
Metabolic Reconstruction of Setaria italica: A Systems Biology Approach for Integrating Tissue-Specific Omics and Pathway Analysis of Bioenergy Grasses.
de Oliveira Dal'Molin CG, Orellana C, Gebbie L, Steen J, Hodson MP, Chrysanthopoulos P, Plan MR, McQualter R, Palfreyman RW, Nielsen LK., Front Plant Sci 7(), 2016
PMID: 27559337
New evidence for grain specific C4 photosynthesis in wheat.
Rangan P, Furtado A, Henry RJ., Sci Rep 6(), 2016
PMID: 27530078
Genetic variability of the phloem sap metabolite content of maize (Zea mays L.) during the kernel-filling period.
Yesbergenova-Cuny Z, Dinant S, Martin-Magniette ML, Quilleré I, Armengaud P, Monfalet P, Lea PJ, Hirel B., Plant Sci 252(), 2016
PMID: 27717471
The draft genome of the C3 panicoid grass species Dichanthelium oligosanthes.
Studer AJ, Schnable JC, Weissmann S, Kolbe AR, McKain MR, Shao Y, Cousins AB, Kellogg EA, Brutnell TP., Genome Biol 17(1), 2016
PMID: 27793170
An assessment of the capacity for phosphoenolpyruvate carboxykinase to contribute to C4 photosynthesis.
Koteyeva NK, Voznesenskaya EV, Edwards GE., Plant Sci 235(), 2015
PMID: 25900567
Insights into C4 metabolism from comparative deep sequencing.
Burgess SJ, Hibberd JM., Curr Opin Plant Biol 25(), 2015
PMID: 26051034
Photosynthetic innovation broadens the niche within a single species.
Lundgren MR, Besnard G, Ripley BS, Lehmann CE, Chatelet DS, Kynast RG, Namaganda M, Vorontsova MS, Hall RC, Elia J, Osborne CP, Christin PA., Ecol Lett 18(10), 2015
PMID: 26248677
2-Hydroxy Acids in Plant Metabolism.
Maurino VG, Engqvist MK., Arabidopsis Book 13(), 2015
PMID: 26380567
Phylogeny and photosynthesis of the grass tribe Paniceae.
Washburn JD, Schnable JC, Davidse G, Pires JC., Am J Bot 102(9), 2015
PMID: 26373976
The evolutionary ecology of C4 plants.
Christin PA, Osborne CP., New Phytol 204(4), 2014
PMID: 25263843

44 References

Daten bereitgestellt von Europe PubMed Central.

An mRNA blueprint for C4 photosynthesis derived from comparative transcriptomics of closely related C3 and C4 species.
Brautigam A, Kajala K, Wullenweber J, Sommer M, Gagneul D, Weber KL, Carr KM, Gowik U, Mass J, Lercher MJ, Westhoff P, Hibberd JM, Weber AP., Plant Physiol. 155(1), 2010
PMID: 20543093
Aspartate decarboxylation in bundle sheath-cells of Zea mays and its possible contribution to C photosynthesis
Chapman KSR, Hatch MD., 1981
Single-cell C(4) photosynthesis versus the dual-cell (Kranz) paradigm.
Edwards GE, Franceschi VR, Voznesenskaya EV., Annu Rev Plant Biol 55(), 2004
PMID: 15377218
Balancing light capture with disturbed metabolic demand during C photosynthesis
Evans JR, Vogelmann TC, von S., 2007
A biochemical model of photosynthetic CO2 assimilation in leaves of C 3 species.
Farquhar GD, von Caemmerer S, Berry JA., Planta 149(1), 1980
PMID: 24306196
Carbon and water economy of Australian NAD-ME and NADP-ME C-4 grasses
Ghannoum O, von S, Conroy JP., 2001
Evolution of C4 photosynthesis in the genus Flaveria: how many and which genes does it take to make C4?
Gowik U, Brautigam A, Weber KL, Weber AP, Westhoff P., Plant Cell 23(6), 2011
PMID: 21705644
Biochemical and cytological relationships in C4 plants.
Gutierrez M, Gracen VE, Edwards GE., Planta 119(4), 1974
PMID: 24442564
Photosynthesis by sugar-cane leaves: a new carboxylation reaction and the pathway of sugar formation
Hatch MD, Slack CR., 1966
C pathway of photosynthesis. Evidence for an intermediate pool of carbon dioxide and identity of donor C dicarboxylic acid
Hatch MD., 1971
Subdivision of C pathway species based on differing C decarboxylating systems and ultrastructural features
Hatch MD, Kagawa T, Craig S., 1975
C photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure
Hatch MD., 1987
Short-term measurements of carbon isotope discrimination in several C4 species
Henderson SA, Voncaemmerer S, Farquhar GD., 1992
The biochemistry of C photosynthesis
Kanai R, Edwards GE., 1999
Structural and metabolic transitions of C4 leaf development and differentiation defined by microscopy and quantitative proteomics in maize.
Majeran W, Friso G, Ponnala L, Connolly B, Huang M, Reidel E, Zhang C, Asakura Y, Bhuiyan NH, Sun Q, Turgeon R, van Wijk KJ., Plant Cell 22(11), 2010
PMID: 21081695
The roles of malate and aspartate in C photosynthetic metabolism of Flaveria bidentis (L)
Meister M, Agostino A, Hatch MD., 1996
Diversity of Kranz anatomy and biochemistry in C4 eudicots.
Muhaidat R, Sage RF, Dengler NG., Am. J. Bot. 94(3), 2007
PMID: 21636407
Significant involvement of PEP-CK in carbon assimilation of C4 eudicots.
Muhaidat R, McKown AD., Ann. Bot. 111(4), 2013
PMID: 23388881
Photosynthetic light-response curves. 1. The influence of CO partial-pressure and leaf inversion
Ögren E, Evans JR., 1993
Systems analysis of a maize leaf developmental gradient redefines the current C4 model and provides candidates for regulation.
Pick TR, Brautigam A, Schluter U, Denton AK, Colmsee C, Scholz U, Fahnenstich H, Pieruschka R, Rascher U, Sonnewald U, Weber AP., Plant Cell 23(12), 2011
PMID: 22186372
Generation and maintenance of concentration gradients between the mesophyll and bundle sheath in maize leaves
Stitt M, Heldt HW., 1985
The influence of light quality on C photosynthesis under steady-state conditions in Zea mays and Miscanthus giganteus: changes in rates of photosynthesis but not the efficiency of the CO concentrating mechanism
Sun W, Ubierna N, Ma JY, Cousins AB., 2012
Profiles of light absorption and chlorophyll within spinach leaves from chlorophyll fluorescence
Vogelmann TC, Evans JR., 2002
Measurement of gradients of absorbed light in spinach leaves from chlorophyll fluorescence profiles
Vogelmann TC, Han T., 2000
Modelling of C photosynthesis
von S, Furbank RT., 1999

von S., 2000
The C(4) pathway: an efficient CO(2) pump.
von Caemmerer S, Furbank RT., Photosyn. Res. 77(2-3), 2003
PMID: 16228376
Phosphoenolpyruvate carboxykinase in C plants: its role and regulation
Walker RP, Acheson RM, Tecsi LI, Leegood RC., 1997
Elements required for an efficient NADP-ME type C photosynthesis—exploration using a systems model of C photosynthesis
Wang Y, Long SP, Zhu XG., 2014
The role of membrane transport in metabolic engineering of plant primary metabolism
Weber APM, Bräutigam A., 2013
Phosphoenolpyruvate carboxykinase is involved in the decarboxylation of aspartate in the bundle sheath of maize
Wingler A, Walker RP, Chen ZH, Leegood RC., Plant Physiol. 120(2), 1999
PMID: 10364405
What is the maximum efficiency with which photosynthesis can convert solar energy into biomass?
Zhu XG, Long SP, Ort DR., 2008
Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®
Quellen

PMID: 24609651
PubMed | Europe PMC

Suchen in

Google Scholar