The role of alanine and aspartate aminotransferases in C<sub>4</sub> photosynthesis

Schlüter U, Bräutigam A, Droz J-M, Schwender J, Weber APM (2019)
Plant Biology 21(S1): 64-76.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
Download
OA 1.06 MB
Autor*in
Schlüter, U.; Bräutigam, AndreaUniBi ; Droz, J.-M.; Schwender, J.; Weber, A. P. M.
Abstract / Bemerkung
• Alanine and aspartate are essential transfer metabolites for C4 species of the NADmalic enzyme and phosphoenolpyruvate carboxykinase subtype. To some degree both amino acids are also part of the metabolite shuttle in NADP-malic enzyme plants. In comparison with C3 species, the majority of C4 species are therefore characterised by enhanced expression and activity of alanine and aspartate aminotransferases (AT) in the photosynthetically active tissue. Both enzymes exist in multiple copies and have been found in different subcellular compartments. We tested whether different C4 species show preferential recruitment of enzymes from specific lineages and subcellular compartments. • Phylogenetic analysis of alanine and aspartate ATs from a variety of monocot and eudicot C4 species and their C3 relatives was combined with subcellular prediction tools and analysis of the subsequent transcript amounts in mature leaves. • Recruitment of aspartate AT from a specific subcellular compartment was strongly connected to the biochemical subtype. Deviation from the main model was however observed in Gynandropsis gynandra. The configuration of alanine AT generally differed in monocot and eudicot species. C4 monocots recruited an alanine AT from a specific cytosolic branch, but eudicots use alanine AT copies from a mitochondrial branch. • Generally, plants display high plasticity in the setup of the C4 pathway. Beside the common models for the different C4 subtypes, individual solutions were found for plant groups or lineages.
Erscheinungsjahr
2019
Zeitschriftentitel
Plant Biology
Band
21
Ausgabe
S1
Seite(n)
64-76
ISSN
1435-8603
eISSN
1438-8677
Page URI
https://pub.uni-bielefeld.de/record/2932897

Zitieren

Schlüter U, Bräutigam A, Droz J-M, Schwender J, Weber APM. The role of alanine and aspartate aminotransferases in C<sub>4</sub> photosynthesis. Plant Biology. 2019;21(S1):64-76.
Schlüter, U., Bräutigam, A., Droz, J. - M., Schwender, J., & Weber, A. P. M. (2019). The role of alanine and aspartate aminotransferases in C<sub>4</sub> photosynthesis. Plant Biology, 21(S1), 64-76. https://doi.org/10.1111/plb.12904
Schlüter, U., Bräutigam, Andrea, Droz, J.-M., Schwender, J., and Weber, A. P. M. 2019. “The role of alanine and aspartate aminotransferases in C<sub>4</sub> photosynthesis”. Plant Biology 21 (S1): 64-76.
Schlüter, U., Bräutigam, A., Droz, J. - M., Schwender, J., and Weber, A. P. M. (2019). The role of alanine and aspartate aminotransferases in C<sub>4</sub> photosynthesis. Plant Biology 21, 64-76.
Schlüter, U., et al., 2019. The role of alanine and aspartate aminotransferases in C<sub>4</sub> photosynthesis. Plant Biology, 21(S1), p 64-76.
U. Schlüter, et al., “The role of alanine and aspartate aminotransferases in C<sub>4</sub> photosynthesis”, Plant Biology, vol. 21, 2019, pp. 64-76.
Schlüter, U., Bräutigam, A., Droz, J.-M., Schwender, J., Weber, A.P.M.: The role of alanine and aspartate aminotransferases in C<sub>4</sub> photosynthesis. Plant Biology. 21, 64-76 (2019).
Schlüter, U., Bräutigam, Andrea, Droz, J.-M., Schwender, J., and Weber, A. P. M. “The role of alanine and aspartate aminotransferases in C<sub>4</sub> photosynthesis”. Plant Biology 21.S1 (2019): 64-76.
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
2019-09-06T09:19:04Z
MD5 Prüfsumme
38282faddb94d888e3b8014fb12f9c56


72 References

Daten bereitgestellt von Europe PubMed Central.

Metabolite pools and carbon flow during C4 photosynthesis in maize: 13CO2 labeling kinetics and cell type fractionation.
Arrivault S, Obata T, Szecowka M, Mengin V, Guenther M, Hoehne M, Fernie AR, Stitt M., J. Exp. Bot. 68(2), 2016
PMID: 27834209
The role of proteins in C(3) plants prior to their recruitment into the C(4) pathway.
Aubry S, Brown NJ, Hibberd JM., J. Exp. Bot. 62(9), 2011
PMID: 21321052
Phylogeny of Sesuvioideae (Aizoaceae) - Biogeography, leaf anatomy and the evolution of C4 photosynthesis
Bohley, Perspectives in Plant Ecology, Evolution and Systematics 17(), 2015
Photorespiration connects C3 and C4 photosynthesis.
Brautigam A, Gowik U., J. Exp. Bot. 67(10), 2016
PMID: 26912798
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
Widespread dual targeting of proteins in land plants: when, where, how and why.
Carrie C, Whelan J., Plant Signal Behav 8(8), 2013
PMID: 23733068
Characterizing regulatory and functional differentiation between maize mesophyll and bundle sheath cells by transcriptomic analysis.
Chang YM, Liu WY, Shih AC, Shen MN, Lu CH, Lu MY, Yang HW, Wang TY, Chen SC, Chen SM, Li WH, Ku MS., Plant Physiol. 160(1), 2012
PMID: 22829318
Aspartate decarboxylation in bundle sheath cells of Zea mays and its possible contribution to C4 photosynthesis
Chapman, Australian Journal of Plant Biology 8(), 1981
Parallel recruitment of multiple genes into c4 photosynthesis.
Christin PA, Boxall SF, Gregory R, Edwards EJ, Hartwell J, Osborne CP., Genome Biol Evol 5(11), 2013
PMID: 24179135
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), 2015
PMID: 26527656
Freeze-quenched maize mesophyll and bundle sheath separation uncovers bias in previous tissue-specific RNA-Seq data.
Denton AK, Maß J, Kulahoglu C, Lercher MJ, Brautigam A, Weber AP., J. Exp. Bot. 68(2), 2017
PMID: 28043950
Photorespiration Is Crucial for Dynamic Response of Photosynthetic Metabolism and Stomatal Movement to Altered CO2 Availability.
Eisenhut M, Brautigam A, Timm S, Florian A, Tohge T, Fernie AR, Bauwe H, Weber APM., Mol Plant 10(1), 2016
PMID: 27702693
A plastidial sodium-dependent pyruvate transporter.
Furumoto T, Yamaguchi T, Ohshima-Ichie Y, Nakamura M, Tsuchida-Iwata Y, Shimamura M, Ohnishi J, Hata S, Gowik U, Westhoff P, Brautigam A, Weber AP, Izui K., Nature 476(7361), 2011
PMID: 21866161
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
De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis.
Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, Couger MB, Eccles D, Li B, Lieber M, MacManes MD, Ott M, Orvis J, Pochet N, Strozzi F, Weeks N, Westerman R, William T, Dewey CN, Henschel R, LeDuc RD, Friedman N, Regev A., Nat Protoc 8(8), 2013
PMID: 23845962
Photorespiration and the potential to improve photosynthesis.
Hagemann M, Bauwe H., Curr Opin Chem Biol 35(), 2016
PMID: 27693890
Predicting C4 photosynthesis evolution: modular, individually adaptive steps on a Mount Fuji fitness landscape.
Heckmann D, Schulze S, Denton A, Gowik U, Westhoff P, Weber AP, Lercher MJ., Cell 153(7), 2013
PMID: 23791184
The regulation of gene expression required for C4 photosynthesis.
Hibberd JM, Covshoff S., Annu Rev Plant Biol 61(), 2010
PMID: 20192753
Identification of photorespiratory glutamate:glyoxylate aminotransferase (GGAT) gene in Arabidopsis.
Igarashi D, Miwa T, Seki M, Kobayashi M, Kato T, Tabata S, Shinozaki K, Ohsumi C., Plant J. 33(6), 2003
PMID: 12631323
Evolutionary convergence of cell-specific gene expression in independent lineages of C4 grasses.
John CR, Smith-Unna RD, Woodfield H, Covshoff S, Hibberd JM., Plant Physiol. 165(1), 2014
PMID: 24676859
Effect of nitrate limitation on the photosynthetically active pool of aspartate and malate in maize, a NADP malic enzyme C4 plant
Khamis, Physiologia Plantarum 85(), 1992
Evolution and expression of C4 photosynthesis genes.
Ku MS, Kano-Murakami Y, Matsuoka M., Plant Physiol. 111(4), 1996
PMID: 8756491
Comparative transcriptome atlases reveal altered gene expression modules between two Cleomaceae C3 and C4 plant species.
Kulahoglu C, Denton AK, Sommer M, Maß J, Schliesky S, Wrobel TJ, Berckmans B, Gongora-Castillo E, Buell CR, Simon R, De Veylder L, Brautigam A, Weber AP., Plant Cell 26(8), 2014
PMID: 25122153
The Roles of Organic Acids in C4 Photosynthesis.
Ludwig M., Front Plant Sci 7(), 2016
PMID: 27242848
The role of photorespiration during the evolution of C4 photosynthesis in the genus Flaveria.
Mallmann J, Heckmann D, Brautigam A, Lercher MJ, Weber AP, Westhoff P, Gowik U., Elife 3(), 2014
PMID: 24935935
The roles of malate and aspartate in C-4 photosynthetic metabolism of Flaveria
Meister, Planta 199(), 1996
Alanine aminotransferase catalyses the breakdown of alanine after hypoxia in Arabidopsis thaliana.
Miyashita Y, Dolferus R, Ismond KP, Good AG., Plant J. 49(6), 2007
PMID: 17319845
Isolation of leaf bundle sheath protoplasts from C4 dicot species and intercellular localization of selected enzymes
Moore, Plant Science Letters 35(), 1984
Two alanine aminotranferases link mitochondrial glycolate oxidation to the major photorespiratory pathway in Arabidopsis and rice.
Niessen M, Krause K, Horst I, Staebler N, Klaus S, Gaertner S, Kebeish R, Araujo WL, Fernie AR, Peterhansel C., J. Exp. Bot. 63(7), 2012
PMID: 22268146
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
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
Glycolysis and the tricarboxylic acid cycle are linked by alanine aminotransferase during hypoxia induced by waterlogging of Lotus japonicus.
Rocha M, Licausi F, Araujo WL, Nunes-Nesi A, Sodek L, Fernie AR, van Dongen JT., Plant Physiol. 152(3), 2010
PMID: 20089769
The evolution of C4 photosynthesis.
Sage RF., New Phytol. 161(2), 2004
PMID: IND43668189
Photosynthetic diversity meets biodiversity: the C4 plant example.
Sage RF, Stata M., J. Plant Physiol. 172(), 2014
PMID: 25264020
The C(4) plant lineages of planet Earth.
Sage RF, Christin PA, Edwards EJ., J. Exp. Bot. 62(9), 2011
PMID: 21414957
Alanine aminotransferase controls seed dormancy in barley.
Sato K, Yamane M, Yamaji N, Kanamori H, Tagiri A, Schwerdt JG, Fincher GB, Matsumoto T, Takeda K, Komatsuda T., Nat Commun 7(), 2016
PMID: 27188711
Understanding metabolite transport and metabolism in C4 plants through RNA-seq.
Schluter U, Denton AK, Brautigam A., Curr. Opin. Plant Biol. 31(), 2016
PMID: 27082280
Estimating the rate of photorespiration in leaves
Sharkey, Physiologia Plantarum 73(), 1988
Photosynthesis and early Earth.
Shih PM., Curr. Biol. 25(19), 2015
PMID: 26439346
Genetic engineering of improved nitrogen use efficiency in rice by the tissue-specific expression of alanine aminotransferase.
Shrawat AK, Carroll RT, DePauw M, Taylor GJ, Good AG., Plant Biotechnol. J. 6(7), 2008
PMID: 18510577
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
Deciphering the role of aspartate and prephenate aminotransferase activities in plastid nitrogen metabolism.
de la Torre F, El-Azaz J, Avila C, Canovas FM., Plant Physiol. 164(1), 2013
PMID: 24296073
Comparative analyses of C₄ and C₃ photosynthesis in developing leaves of maize and rice.
Wang L, Czedik-Eysenberg A, Mertz RA, Si Y, Tohge T, Nunes-Nesi A, Arrivault S, Dedow LK, Bryant DW, Zhou W, Xu J, Weissmann S, Studer A, Li P, Zhang C, LaRue T, Shao Y, Ding Z, Sun Q, Patel RV, Turgeon R, Zhu X, Provart NJ, Mockler TC, Fernie AR, Stitt M, Liu P, Brutnell TP., Nat. Biotechnol. 32(11), 2014
PMID: 25306245
Three distinct biochemical subtypes of C4 photosynthesis? A modelling analysis.
Wang Y, Brautigam A, Weber AP, Zhu XG., J. Exp. Bot. 65(13), 2014
PMID: 24609651
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
Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®
Quellen

PMID: 30126035
PubMed | Europe PMC

Suchen in

Google Scholar